Minireview: algal natural compounds and extracts as antifoulants

Mahasweta Saha; Franz Goecke; Punyasloke Bhadury

doi:10.1007/s10811-017-1322-0

Minireview: algal natural compounds and extracts as antifoulants

Saha, Mahasweta; Goecke, Franz; Bhadury, Punyasloke 2017-11-06 00:00:00 J Appl Phycol (2018) 30:1859–1874 https://doi.org/10.1007/s10811-017-1322-0 1,2 3 4 Mahasweta Saha & Franz Goecke & Punyasloke Bhadury Received: 11 February 2017 /Revised and accepted: 17 October 2017 /Published online: 6 November 2017 The Author(s) 2018 Abstract Marine biofouling is a paramount phenomenon in rather scarce. Thus, we have also discussed the need to con- the marine environment and causes serious problems to mar- duct more chemical ecology based research in relatively less itime industries worldwide. Marine algae are known to pro- explored areas with high algal biodiversity like Southeast duce a wide variety of chemical compounds with antibacterial, Asia. antifungal, antialgal, and anti-macrofouling properties, . . . inhibiting the settlement and growth of other marine fouling Keywords Algae Biofouling Natural products . . . organisms. Significant investigations and progress have been Antifouling defense Antibacterial Anti-diatom made in this field in the last two decades and several antifoul- Anti-macrofouling ing extracts and compounds have been isolated from micro- and macroalgae. In this minireview, we have summarized and evaluated antifouling compounds isolated and identified from Introduction macroalgae and microalgae between January 2010 and June 2016. Future directions for their commercialization Marine biofouling—the colonization and growth of micro- through metabolic engineering and industrial scale up have and macro-organisms on any submerged surface (living and been discussed. Upon comparing biogeographical regions, in- man-made structures) is paramount in the marine environment vestigations from Southeast Asian waters were found to be (Wahl 1989). An average milliliter of natural seawater con- 6 3 2 tains 10 cells of bacteria, 10 microalgae, and 10 propagules of algae and benthic invertebrate larvae (Harder 2009)making any undefended surface quite likely to be colonized by micro- The original version of this article was revised due to a retrospective Open and macro-foulers. Uncontrolled biotic coverage is heavily Access order. detrimental for efficient operation and functioning of such submerged man-made structures (reviewed in Maréchal and * Mahasweta Saha Hellio 2009; Callow and Callow 2011). Biofouling on struc- sahamahasweta@gmail.com tures like ships not only increase ownership costs but are also accompanied with environmental pollution through increased Benthic Ecology, Helmholtz Center for Ocean Research, emission of gases like carbon dioxide, carbon monoxide, and Düsternbrooker weg, 24105 Kiel, Germany sulfur dioxide (Chambers et al. 2006) and is also involved Present address: School of Biological Science, University of Essex, with transport of invasive species (Gollasch 2002). Colchester, CO 43 SQ, UK Remediation of biofouling on ship hulls only costs approxi- Department of Plant and Environmental Science (IPV), Norwegian mately € 120 billion per year (Chapman et al. 2014). To coun- University of Life Sciences (NMBU), Ås, Norway ter such detrimental effects, biofouling was previously con- Integrative Taxonomy and Microbial Ecology Research Group, trolled using toxic antifouling coatings. While the use of anti- Department of Biological Sciences, Indian Institute of Science fouling compounds like tributlyl tin (TBT) and copper oxide Education and Research Kolkata, Mohanpur, Nadia, West Bengal 741246, India have been found to be the most effective method, their non- 1860 J Appl Phycol (2018) 30:1859–1874 targeted effect on other marine organisms like toxicity, large surface area for settlement in benthic marine habitats imposex, bioaccumulative effect, and contamination of the (Seed 1985). Thus, macroalgae are highly susceptible to food chain (Fernández-Alba et al. 2002; Bellas 2006;) has epibiosis in comparison to other potential basibionts. led to a total ban of TBT-based coatings in 2008 by the Macroalgae have evolved efficient defense mechanisms as a International Maritome Organization. Although new biocide mean of protection and thus have been found to be producers formulations like irgarol, chlorothalonil, dichlofluanid, and of wealth of antifouling compounds (reviewed by Bhadury diuron were introduced in marine antifouling AF coatings and Wright 2004;Da Gama et al. 2014). Unlike macroalgae, and initially thought to be environment friendly, later they microalgae are not susceptible to colonization by macro- were reported to be toxic, accumulating in marinas and har- epibionts, but they also experience intense competition for bors (Chapman et al. 2014). The ban of TBT and other toxic space and other resources with their neighbors. Certain AF coatings has drawn a huge amount of interest towards bio- microalgae are known to control their microenvironment inspired AF approaches, i.e., the investigation of novel, through the employment of allelochemicals which have been environment-friendly AF compounds from organisms that suggested to be responsible for observed patchy distribution in are mostly free from foulers colonizing their surfaces. Latest species composition around these microalgae (Saburova et al. strategies towards development of environment-friendly AF 1995; Borowitzka 2016). Such synergistic and antagonistic coatings included biomimetic approaches, Bbiomimicry^ ecological interactions through employment of chemicals (reviewed by Scardino and de Nys 2011), and incorporation have triggered interest among marine natural product chemists of natural antifouling compounds into marine paints leading to the examination of numerous natural products as a (Chambers et al. 2006). However, for their potential appli- possible basis for novel anti-biofilm compounds like cyano- cation in industries, such compounds must be cost effec- gen bromide produced by Nitzschia cf. pellucida tive in terms of production, long lasting, easy to use, and (Vanelslander et al. 2012). non-toxic to marine biota (Ralston and Swain 2009). In the last 5 years, a large number of macroalgal species (89 Efforts made and the systems tested till date have not species in total) and few microalgal species (13 species in been enough successful as they failed to meet all or partly total) have been tested for antifouling activity and several the criteria stated above since such compounds are usually metabolites have been isolated with related bioactivity. The not stable once exposed to the natural environment scope of the current review is to cover their activity against (Maréchal and Hellio 2009); making them durable is a maritime fouling and not medical and industrial fouling. In current challenge. Also, development of a natural product this review, we have summarized the current status of marine is time consuming and a rigorous process. Further, their algal antifouling compounds and extracts isolated and identi- non-toxicity towards non-target species needs to be as- fied between January 2010 and June 2016. We also present sured before being deployed in the field. current challenges and future perspectives on development of Benthic marine environments are quite diverse and charac- antifouling strategies from marine algae. Currently, there is an terized by extreme competition for light, space, nutrient, and important amount of information on metabolic routes, physi- other resources (Wahl 2009). Space being a limiting factor all ological responses, and algal cultivation, and there are an in- potential benthic organisms are also confronted and colonized creasing number of studies on algal genomics (Radakovits by micro and macro settlers—a phenomenon typically termed et al. 2010;Ai et al. 2015; Hlavová et al. 2015; Perez Garcia as epibiosis when the substrate involved is a living one (Wahl and Bashan 2015) which, when grouped together, we consider 1989). As epibiosis is usually detrimental to the (basibiont) essential for the development of algal biotechnology. For a host (Wahl 2008), many basibionts have developed either a potential sustainable development of natural algae-related an- physical or chemical (or both) protection mechanism against tifouling strategies, we have two main focuses: (a) the use of such colonizers, either by themselves (reviewed by Da Gama available and upcoming genomic information to understand et al. 2014) or through symbiotic relationships with bacterial biofouling from the algal genomic perspective (we present the epibionts (reviewed by Singh et al. 2015). Over the past case of diatom genes linked to biofilm formation) and thereby 25 years, several investigations have reported many natural develop gene knock-out-based (or modification) antifouling antifouling compounds being extracted and characterized strategies and (b) it is necessary to couple screening, isolation from varied marine prokaryotes and eukaryotes in assays of compounds, and the genomic studies with industrial against relevant fouling organisms and a number of excellent upscaling and metabolic engineering for a sustainable com- reviews reporting their potential use as antifouling compounds mercial production of natural micro algal compounds. Also, have been published (reviewed by Fusetani 2011;Dobretsov summing up all the ecologically and industrially relevant an- et al. 2013; Puglisi et al. 2014; Qin et al. 2013). tifouling investigations, it is noteworthy that the majority of Being sessile and restricted to the photic zone, macroalgae investigations have focused on algae from temperate waters offer optimal growth conditions to many epibiotic organisms despite the fact that tropical waters are rich in biodiversity. (Harder 2008). Their three-dimensional structure also offers a Therefore, in this review, we have highlighted the importance J Appl Phycol (2018) 30:1859–1874 1861 of expanding the area of sampling to still un-explored zones fucoxanthin and dimethylsulfoniopropionate (DMSP), which (we present Southeast Asia as a case study) with chemical were previously considered to have just primary functions, ecology research objectives, i.e., isolating and testing natural have been reported to function as regulators of the microbial compounds in ecologically relevant bioassays. density and composition over Fucus vesiculosus (Lachnit et al. 2013; Saha et al. 2011, 2012, 2014). Identified com- pounds with AF activity are provided in Fig. 2. Antifouling compounds from macroalgae Furthermore, many other studies have investigated the ac- tivities of both polar and non-polar extracts and reported anti- Apart from being the major primary producers in temperate bacterial, antimicroalgal, and antifungal properties from a va- ecosystems and the largest biomass producers in marine envi- riety of algae belonging to the genera Caulerpa, Chondrus, ronment, macroalgae produce a diverse array of natural com- Dictyota, Padina, Sargassum,and Ulva (Chambers et al. pounds as mode of protection against natural enemies 2011;Cho 2013; Ktari et al. 2010; Silva et al. 2013,see (Goecke et al. 2010). Over the last 5 years, a number of studies Table 1). (some of which are discussed below) have reported new anti- In terms of number of species, more than a quarter of the fouling compounds from macroalgal extracts like the studies involved red macroalgae and the remaining two third cystophloroketals and chromanols, along with an increasing was composed of brown and green seaweeds (Fig. 1). In terms number of reports of activities from crude extracts of different of the chosen bioactivity, most of the studies demonstrated an polarities (Table 1,Fig. 1). antimacrofouling activity (e.g., Maréchal and Hellio 2011; Certain genera, like the red algae Asparagopsis and Van Alstyne et al. 2014) followed by antibacterial (e.g., Laurencia,andthebrownalga Sargassum continue to be Silva et al. 2013;Natrah et al. 2015) and antimicroalgal activ- source of new active antifouling compounds. Asparagopsis ity (e.g. Silkina et al. 2012; Sun et al. 2015). This may be spp. belong to the order Bonnemaisoniales, which is known based on the fact that, space being limited in the benthic en- to be a rich source of halogenated bioactive compounds (Jha vironment, macrofoulers usually tend to settle on macroalgal et al. 2013). Recent study of the introduced red alga surfaces thereby selecting for antimacrofouling defenses. Asparagopsis taxiformis collected from the Indian Ocean Also, epibacterial colonization is ubiquitous on algal surfaces has led to the discovery of two new highly brominated with the ability to negatively impact macroalgal fitness (Wahl cyclopentenones: mahorone and 5-bromomahorone with an- et al. 2012) thereby selecting for antibacterial defenses. timicrobial activity against both marine and terrestrial mi- crobes (Greff et al. 2014). Another investigation on the same species, collected from the intertidal region of the Arabian Sea Antifouling compounds from dinoflagellates, and Bay of Bengal, has found the methanolic extract to have diatoms, and other marine microalgae anti-quorum sensing activity (Jha et al. 2013). Other seaweed species have also been shown to produce quorum-sensing Several studies have been conducted to investigate the prod- inhibitors (Carvalho et al. 2017). Members of the genus ucts of microalgal metabolism, not only to understand its na- Laurencia (Ceramiales) are also known to be a rich source ture but also to search for substances with possible applica- of halogenated secondary metabolites (Blunt et al. 2009)and tions to humans in different fields of interest (de De Morais they continue to be source of new compounds. Recently, a et al. 2015). Some of the earliest and most extensive research new omaezallene and four new polyether triterpenoids with on microalgal secondary metabolites has been on anti-macrofouling activity have been discovered from cyanobacteria, dinoflagellates (Dinophyceae), a few other Laurencia sp. and Laurencia viridis, respectively (Umezawa microflagellates, and diatoms (Bacillariophyceae) (Garcia et al. 2014; Cen-Pacheco et al. 2015). Camacho et al. 2007). This is because of the ability of certain Brown algae of the genus Cystoseira (Fucales) are known bloom-forming species to produce structurally quite diverse to be good source of bioactive terpenoid derivates, specially toxins like brevetoxins produced by Karenia brevis (Fig. 3). meroterpenoids and diterpenoids (reviewed by Gouveia et al. Such bloom phenomena by toxic microalgae are generally 2013). A monocyclic meroditerpenoid isolated from known as harmful algal blooms (HABs). HABs can be highly Cystoseira tamariscifolia has shown high potential for inhibi- toxic to humans and other animals and have further dramatic tion of common foulers like Balanus amphitrite and Mytilus health and socio-economic impacts (Pearson et al. 2010; edulis. Cystophloroketals A and B from the same alga have Clément et al. 2016;Mazard et al. 2016). shown high inhibition activity against two species of fouling Different species from divergent phylogenetic orders of the microalgae and moderate antimicrobial activity against a dinoflagellates produce phytotoxins, e.g., Alexandrium spp. range of bacteria, fungi, and microalgae (Hattab et al. 2015). and Protoceratium spp. (Gonyaulacales), Azadinium sp. Along with the reported role of pholorotannins as antifoulants (Dinophyceae incertae sedis), Dinophysis spp. from certain fucoid species, certain metabolites like (Dinophysiales), Gymnodinium spp. and Karenia spp. 1862 J Appl Phycol (2018) 30:1859–1874 Table 1 Antifouling compounds and extracts from macroalgae Source Biogenic compound(s)/type of extract Bioactivity Origin Reference RHO Asparagopsis taxiformis Mahorone AB Mayotte Greff et al. 2014 5-bromomahorone RHO Asparagopsis taxiformis Methanolic extract AB, QSD India Jha et al. 2013 RHO 2 Bonnemaisonia hamifera 1,1,3,3-Tetrabromo-2-heptanone ABF Sweden Persson et al. 2011 CHL Caulerpa prolifera Ethanol and methanol extracts AB Brazil Silva et al. 2013 RHO Ceramium botryocarpum Ethanol fraction AA France Silkina et al. 2012 RHO Ceramium rubrum Dichloromethane extract AF Chile Cortés et al. 2014 RHO Chondrus crispus Toluene-soluble ABF Ireland Salta et al. 2013 crude ethanolic extract RHO Chondrus crispus Crude ethanol extracts AA, AB Ireland Chambers et al. 2011 CHL Cladophora clavuligera Methanolic and dichloromethane extract AB India Bragadeeswaran et al. 2011a PHE Cystoseira tamariscifolia Cystophloroketals A-B AA, AB, AF Algeria Hattab et al. 2015 PHE Cystoseira tamariscifolia monocyclic meroditerpenoid AMF Algeria Hattab et al. 2015 PHE Dictyota spp. Diterpenes, glicerol derivatives AB, AF France Othmani et al. 2014 PHE Dictyota fasciola Dichloromethane and methanol extract AA, AB, AMF Tunisia Ktari et al. 2010 CHL Dictyosphaeria ocellata Methanol extract AB, ABF USA Sneed and Pohnert 2011a, b PHE 3 4 5 Fucus vesiculosus Fucoxanthin , dimethyl sulphopropionate ,proline AB, ABF Germany Saha et al. 2011, 2012, Wahl et al. 2010, Lachnit et al. 2013 RHO Gracilaria edulis Isoamyl alcohol extract AB India Rajan et al. 2015 RHO Hypnea musciformes Ethanol and methanol extracts AB Brazil Silva et al. 2013 RHO Laurencia johnstonii Ethly ether extract AA, AB, AF Mexico Águila-Ramírez et al. 2012 RHO 6 Laurencia sp. Omaezallene AMF Japan Umezawa et al. 2014 intricatetraol RHO Laurencia translucida Fatty acid derivatives AMF Brazil Paradas et al. 2016 RHO Laurencia viridis 28-Hydroxysaiyacenol B AMF Spain Cen-Pacheco et al. 2015 Saiyacenol C 15,16-epoxythyrsiferol A 15,16-Epoxythyrsiferol B PHE Padina gymnospora Ethanol and methanol extracts AB Brazil Silva et al. 2013 PHE 8 Sargassum horneri Chromanols AA, AB, AMF South Korea Cho 2013 PHE Sargassum muticum Galactoglycerolipids AB, AF, AMF France Plouguerné et al. 2010b PHE Sargassum muticum Ethanol fraction AA France Silkina et al. 2012 PHE Sargassum polyceratium Hexane extract AB Martinique Thabard et al. (2011) PHE Sargassum wightii Methanol extract AB India Bragadeeswaran et al. 2011b PHE Sargassum vulgare Unidentified polar compounds AMF Brazil Plouguerné et al. 2012 PHE Sargassum vulgare Hexane extracts AA, AB, AMF Brazil Plouguerné et al. 2010a methanol and dichloromethane extracts polyphenolic extracts RHO 9 Sphaerococcus coronopifolius Bromosphaerol AMF Greece Piazza et al. 2011 PHE Taonia atomaria sesquiterpenes AB, AMF France Othmani et al. 2015 polyunsaturated fatty acids CHL Ulva fasciata Ethanol and methanol extracts AB Brazil Silva et al. 2013 CHL Ulva intestinalis Hexane extract AB Thailand * Srikong et al. 2015 CHL Ulva lactuca Ethyl ethanol extract AA, AB, AF Mexico Águila-Ramírez et al. 2012 CHL Ulva pertusa Alkaloids, phenolic acid AA China Sun et al. 2015 CHL Ulvaria obscura Dopamine AA, AMF USA Van Alstyne et al. 2014 CHL,PHE,RHO 8spp.macroalgae Methanol extract AB Malaysia* Natrah et al. 2015 CHL,PHE,RHO 11 spp. macroalgae Polar and non-polar extracts QSD Brazil Batista et al. 2014 CHL,PHE,RHO 30 spp. macroalgae Diverse aqueous and organic extracts AMF France Maréchal and Hellio 2011 The bioactivities are the following: antibacterial activity (AB), antifungal (AF), anti-microalgal including diatoms and cyanobacteria (AA), anti- macrofouling including mollusks (AMF), quorum sensing disruptor (QSD), and anti-biofilm (ABF). Also the algae groups: Chlorophyta (CHL), Phaeophyceae (PHE), and Rhodophyta (RHO). Studies made in Southeast Asia are highlighted with an asterisk. 1–9 = compounds listed in Fig. 2 (Gymnodiniales), and Prorocentrum spp. (Prorocentrales), and production of such toxins has been seen as an ecological ad- diatoms as well as Pseudonitzschia spp. (Bacillariales). Such vantage since the release of those chemicals into the environ- diversity is magnified at a rich subspecies level, and in conse- ment may deter, inhibit growth, or kill competing species and quence, the heterogeneity of associated phycotoxins and its predators (Caroppo and Pagliara 2011;Maetal. 2011;Poulson- derivatives are quite variable and big (Orr et al. 2013). The Ellestad et al. 2014; Rolton et al. 2014; Bagwell et al. 2016). J Appl Phycol (2018) 30:1859–1874 1863 Fig. 1 Bioactivity of metabolites or extract fractions from a total of 24 species of red algae, 13 species of green algae, and 18 species of brown algae, active against marine relevant species during the period 2010–2016. Antibacterial activity (AB), antifungal (AF), anti-microalgal including diatoms and cyanobacteria (AA), anti- macrofouling including mollusks and crustacean (AMF), quorum sensing disruptor (QSD), toxins (TX), and anti-biofilm (ABF) No. of studies Allelopathic interactions between microalgal species also may Between January 2010 and June 2016, only 14 relevant contribute to the formation and succession of red tides (Cai studies were conducted on marine microalgal species, which et al. 2014). As the interactions with many potential foulers tested extracts against other marine organisms. Only few com- are regulated by chemical cues, there is a high potential in the pounds (e.g., fatty acids) were isolated from diatoms and di- identification and use of such compounds for biotechnological noflagellates which have demonstrated antimicrobial or anti- applications like antifouling compounds. fouling activities (Desbois et al. 2010). Although the number With respect to other microalgae groups, in the last decade, of isolated compounds is clearly less than in cyanobacteria most of the studies had focused on the content of fatty acids (data not shown), the potential exists to increase that number, and pigments aiming for their use in biotechnology, e.g., ca- because most of these studies have reported bioactivity of rotenoids and polyunsaturated fatty acids (PUFAs) for feed, diverse cultures and their organic extracts but did not isolate and as active ingredients for cosmetics, among others (Abida the active compounds as yet (Table 2). et al. 2013; Borowitzka 2013a). Even though green In terms of number of species, half of the studies involved microalgae are generally regarded safe for human consump- dinoflagellates and most of the second half was composed of tion, there is still a knowledge gap in understanding the met- diatoms. Only one study incorporated a marine haptophyte, abolic and biochemical potential of these algae (Bagwell et al. and thus, many other microalgal groups remain unstudied 2016). (Fig. 4). In terms of the chosen bioactivity, most of the studies (1) 5-bromomahorone (2) 1,1,3,3- tetrabromo-2-heptanone (3) Fucoxanthin (4) DMSP R=Br (5) Proline (6) Omaezallene (7) Intricatetraol (8) Chromanol (9) Bromosphaerol Fig. 2 .Selected antifouling compounds from macroalgae 1864 J Appl Phycol (2018) 30:1859–1874 Fig. 3 Brevetoxins from microalgae Karenia brevis (10) Brevetoxins demonstrated an antialgal activity (Fig. 4). The latter may be of ecosystems, ranging from extensive lagoons, estuaries, and based on the fact that the production of antialgal metabolites mangroves, to rocky shores and coral reefs, which provide would be an ecological advantage in a specific niche and/or suitable habitats for luxuriant algal growth (Nguyen et al. space. Furthermore, organisms like mollusks and crustaceans 2013). In fact, the triangle formed by the Malay Peninsula, not only compete with benthic microalgae for space, but are The Philippines, plus New Guinea (BThe Coral Triangle^)is also important microalgal consumers, with the ability to affect recognized as a global biodiversity hotspot where most trop- microalgal populations. ical marine groups have their greatest diversity of species (Todd et al. 2010; Selig et al. 2014). Researchers have noticed that a high diversity of species may be translated in a higher A case study: antifouling compounds from Southeast diversity of secondary metabolites. But not only that, those Asia species may harbor silent gene clusters coding the production of Bnew^ metabolites, which may be expressed under differ- ent environmental conditions (Bode et al. 2002; Brakhage and Southeast Asia has an outstanding species richness and ende- mism. It has an extensive coastline (e.g., Indonesia, Schroeckh 2011). Thus, biogeography may multiply this num- ber and even enhance bioactivity of such metabolites. 81.000 km; Vietnam, 3.260 km) with many islands and rivers flowing into the extended and large continental shelf The exact number of macro- and micro-algal species for (Aungtonya and Liao 2002; Gerung et al. 2006; Soe-Htun Southeast Asia is still unknown and there are many species yet et al. 2009; Phang et al. 2015). This produces a diverse variety to be discovered (Kawaguchi and Hayashizaki 2011). Table 2 Antifouling compounds and extracts from dinoflagellates and diatoms Source Biogenic compound(s)/ type of extract Bioactivity Origin Reference DF Alexandrium tamarense Lipidic extracts AA Scotland Ma et al. 2011 DI Amphora cf. capitellata Ethanol extract AF Turkey Montalvaõ et al. 2016 HA Isochrysis galbana Fatty acids AB Isle of Man Molina-Cárdenas et al. 2014 DF Karenia brevis Culture extracts, 6 unidentified compounds AA USA Poulson et al. 2010 DF Karenia brevis Diverse metabolites AA USA Prince et al. 2010 DF Karenia brevis Culture extracts, unidentified compounds AA USA Poulson-Ellestad et al. 2014 DF 10 Karenia brevis Culture extracts, brevetoxins AMF, TX USA Rolton et al. 2014 DF Lingulodinium polyedrum Diverse extracts AB Mexico Quijano-Scheggia 2016 DI Nitzschia communis Ethanol extract AB Turkey Montalvaõ et al. 2016 DI Odontella aurita Ethanol extract AB India Hemalatha et al. 2016 DF Ostreopsis cf. ovata Culture extracts AMF, TX Italy Caroppo and Pagliara 2011 DF Ostreopsis cf. ovata Palytoxin-like compounds AMF, TX Italy Gorbi et al. 2012 DI Phaeodactylum tricornutum Culture extracts AA China Cai et al. 2014 DF Prorocentrum donghaiense Culture extracts AA China Cai et al. 2014 DF Protoceratium reticulatum Culture extracts AA Greenland Sala-Pérez et al. 2016 DI Skeletonema marinoi Acetonic extracts AB Italy Lauritano et al. 2016 DI Thalassiosira rotula Diverse extracts AB Australia Qin et al. 2013 The bioactivities are the following: antibacterial activity (AB), antifungal (AF), anti-macroalgal (AM), anti-microalgal including diatoms and cyanobacteria (AA), anti-macrofouling including mollusks (AMF), quorum sensing disruptor (QSD), anti-biofilm (ABF), and toxins (TX). Also the algae groups: diatoms (DI), dinoflagellates (DF), and haptophytes (HA). 10 = compound listed in Fig. 3 J Appl Phycol (2018) 30:1859–1874 1865 Fig. 4 Bioactivity of metabolites or extracts fractions from a total of six species of dinoflagellates, five species of diatoms and one haptophyte, active against marine relevant species during the period 2010–2016. Antibacterial activity (AB), antifungal (AF), anti- microalgal including diatoms and cyanobacteria (AA), anti- macrofouling including mollusks and crustacean (AMF), quorum sensing disruptor (QSD), toxins (TX), and anti-biofilm (ABF) No. of studies Research has mostly focused on economic resources, as sev- Antifouling compounds from S.E.A eral macroalgae are important economic resources in Southeast Asia (S.E.A.). Thus, the existing coverage of spe- Although, studies looking at the antifouling activity of algae cies is conspicuous by the omission of small groups (Wafar (micro and macro) are limited in S.E.A. compared to et al. 2011), or other Bless important^ economic species, and European and North American waters (Fig. 5), nevertheless therefore, we understand little of their distributions and poten- studies over the last decade have shown promising antifouling tial uses (Webb et al. 2010). Given the unlocked potential of activities from Southeast Asian algae. Majority of the studies algal compounds from S.E.A, in this review, we have from Southeast Asian waters have been largely focused on highlighted the importance of exploring this area with more marine macroalgae, and antifouling activity was examined depth. based on crude extract assays (e.g. Bhadury and Wright 2004 and references within; Sidharthan et al. 2004;Qian et al. 2010 and references within; Satheesh et al. 2016 and Algal compounds in general from S.E.A references within). Identified compounds so far from Southeast Asia with AF activity are provided in Fig. 6.An If we compare the collection effort globally of all type of integrative approach involving identification of secondary organisms, the S.E.A region has been well explored and metabolites from the crude extracts has been far less studied reporting of compounds from these regions has been rapidly compared to information available from other geographical accelerating since 1990 (Blunt et al. 2016). According to origins. This reflects the need to undertake approaches involv- Blunt et al. (2016), maritime Southeast Asia (and Papua ing GC-MS and NMR for identification of potential potent New Guinea) has produced in 50 years 1340 compounds as antifouling secondary metabolites. While, Southeast Asia har- reported in 502 publications, plus the mainland of Southeast bors high biodiversity including rich marine microalgae and Asia (including East Malaysia) has produced 457 compounds macroalgal diversity, their potential for antifouling activity in in 173 publications. However, considering the information in an ecological context is yet to be effectively explored. the excellent reviews of new marine natural products pub- lished by Blunt et al. (2011, 2012, 2013, 2014, 2015, 2016), Linking genes to biofilm formation between the years 2008 to 2014, the contribution of com- pounds isolated from marine algae species growing in S.E.A Among the early colonizers, diatoms play a significant role in is limited to only 29 compounds, from which only 23 are biofilm development and are able to colonize on even most newly described for science (Table 3), when compared to the fouling-resistant surfaces (Molino and Wetherbee 2008). compounds described from algae collected worldwide. It is Currently, our understanding of the role of genes during also interesting to note that the investigations were mostly bacteria-diatom interaction as part of biofilm formation is rel- limited to red algae of the genus Laurencia (Table 4). When atively well understood (e.g., Buhmann et al. 2012 and we compare the total amount of new natural compounds re- references within). However, limited knowledge exists in ported from marine algae worldwide, the yield of natural com- terms of the genes that are exclusively found in marine dia- pounds from marine algae reported from Southeast Asia is not toms and their link to marine biofilm formation. The recent significant (Fig. 5), contradicting the great diversity of the availability of phytoplankton genome sequence data, in area. particular diatom genomes, has resulted in improved 1866 J Appl Phycol (2018) 30:1859–1874 Table 3 Detail of the yearly new identified natural compounds isolated from different marine algae groups (data based on Blunt et al. 2016). The contribution of compounds isolated from species growing in Southeast Asia (S.E.A) is specified New identified compounds Organisms 2008 2008 2009 2009 2010 2010 2011 2011 2012 2012 2013 2013 2014 2014 total SEA total SEA total SEA total SEA total SEA total SEA total SEA Dinoflagellates 8 0 12 0 17 0 2 0 2 0 9 0 19 0 Diatoms, other 10 00 0 0 3 0 00 4 0 00 microalgae Chlorophyta 4 0 6 08 03 0 2 05 013 0 Phaeophyceae 45 0 25 0 10 0 25 0 32 0 17 0 17 0 Rhodophyta 24 3 49 0 47 7 41 1 45 1 9 0 41 1 understanding of mechanisms that control their growth and Thalassiosira pseudonana shows that degree of polymeriza- distribution in the marine environment (e.g., Armbrust et al. tion and distribution of EPSs can vary in response to nutrient 2004;Bowler etal. 2008). Thus, the rapidly available diatom depletion and different nutrient sources (Ai et al. 2015). genome datasets can help in understanding the role of biosyn- Proteins and glycoproteins have been studied by chemical thetic pathways towards production and regulation of extra- methods and by atomic force microscopy (Lind et al. 1997; cellular polymeric substances (EPS) during the process of Wustman et al. 1997; Dugdale et al. 2006; Chiovitti et al. biofouling. 2008). It has been shown that the adhesive molecules appear From the cellular viewpoint, the adhesive components of to be highly glycosylated with novel glycans that are highly EPS are involved in diatom cell-substratum adhesion, in ad- sulphated (Chiovitti et al. 2003, 2008). dition to motility. EPS molecules are secreted from frustules In a recent study, from the available genome dataset of the through pores in the girdle bands and valves. The carbohy- pennate diatom Phaeodactylum tricornutum, bioinformatic drate components of the EPS have been characterized in var- analysis was undertaken to identify putative diatom cell sub- ious benthic diatoms (e.g., Chiovitti et al. 2008; Abdullahi stratum adhesion molecules (PDC) (Willis et al. 2014). In et al. 2006). It is already well known that EPS secretion in total, 37 PDCs were identified from the P. tricornutum ge- diatoms depends on numerous factors including nutrient avail- nome, of which some showed similarities to genes found in ability, daily fluctuations, irradiance, and even metal toxicity a diverse range of organisms, including metazoans, plants, and (Staats et al. 1999;Ai et al. 2015). This is particularly signif- prokaryotes, as well as algae, encoding components of the icant since EPSs can be a food source for heterotrophic organ- extracellular matrix (ECM) or cell adhesion complexes isms and affect the detachment of biofilms (e.g., De Brouwer (Yamada and Geiger 1997;Zhao and Waite 2006). It has been and Stal 2002; Bellinger et al. 2005). For example, nitrogen found that genes that code for PDCs have characterizing fea- and phosphate limitations affect production rate of EPSs in- tures that are common to a set of cell adhesion molecule cluding chemical composition in various diatoms (Magaletti (CAM) genes (Willis et al. 2014). Indeed, using bioinformatic et al. 2014;Ai et al. 2015). Mass spectrometry of EPSs of approach, we detected the presence of CAM genes across Table 4 Natural compounds isolated from different marine algae groups from Southeast Asia (data based on Blunt et al. 2016). The geographical origin and bioactivity of compounds are specified Taxa Compound Bioactivity Origin Reference RH n Gracilaria edulis Levuglandin D – The Philippines Kanai et al. 2011 RH n Laurencia nangii Dihydroitomanallene B – Malaysia Kamada and Vairappan 2012 pannosallene itomanallene B RH n, 13 Laurencia snackeyi 5β-Hydroxypalisadin B – Malaysia Wijesinghe et al. 2014 RH n, 14,15,16 Laurencia sp. Laurefurenyne A-F cytotoxic The Philippines Abdel-Mageed et al. 2010 RH n Laurencia sp. Tiomanene – Malaysia Vairappan et al. 2008 n, 17 acetylmajapolene A-B n new compounds RH rhodophyta 11–17 Compounds listed in Fig. 6 J Appl Phycol (2018) 30:1859–1874 1867 Fig. 5 Studies conducted between January 2010 and June 2016 based on geographical locations. % by zone = America 32%, Europe 34%, Africa 6%, Oceania 2%, Asia 23%, S.E.A. 4% (of the 23% of Asia) sequenced marine micro- and macroalgal genomes (Fig. 7). diatom cell adhesion. Based on the analysis of the As evident from Fig. 4, these amino acid sequences T. pseudonana genome, several putative cell adhesion mole- representing CAM are conserved across different marine cules have been identified using bioinformatics approach. algae and thus may also indicate the possible existence of From the available transcriptome data of the model adhe- putative PDCs in published marine algal genomes. Willis sion diatom, Amphora coffeaeformis, five proteins have been et al. (2014) reported that some of the PDCs were diatom identified that exhibit unique amino acid sequences resem- specific and encoded unclear functions. These putative genes bling the amino acid composition of the tyrosine-rich adhe- indicate that there is likely a diverse range of molecules that sion proteins from mussel footpads (Buhmann et al. 2014). diatoms use for cell substratum adhesion and therefore these Buhmann et al. (2014) looked into the function of one of these genes potentially may play key role in biofouling. Seven of proteins, AC3362 by undertaking genetic transformation of A. these PDC have been characterized in vivo, by generation of coffeaeformis. They found that AC3362 plays a role in bio- transgenic diatom lines over-expressing genes encoding C- synthesis and or structural stability of the cell wall of this terminal yellow fluorescent protein (YFP) fusion proteins, pennate diatom. The findings of AC3362 protein is particular- and showed that these candidate proteins are involved in ly significant since in many mussel foot proteins, tyrosine (11) Pannosallene (12) Itomanallene B (13) 5β-hydroxypalisadin B (14) LaurefurenyneA-B R=OH (Z and E denotes isomer) (15) Laurefurenyne C (16) Laurefurenyne F (17) Acetylmajapolene A Fig. 6 Antifouling compounds isolated from Southeast Asian macroalgae 1868 J Appl Phycol (2018) 30:1859–1874 Fig. 7 Amino acid sequence alignment of CAM gene from Thalassiosira tricornutum CCAP1055 (Acc No. XP_002185049), Guillardia theta pseudonana CCMP1335 (Acc No. XM_002295719), Aureococcus CCMP2712 (Acc No. XP_005836584) and Gracilariopsis anophagefferens (Acc No XP_009033803), Phaeodactylum lemaneiformis (Acc No. AKG55580) showing highly conserved regions residues have been post-translationally hydroxylated to 3,4- understand specific role of genes and proteins of microalgal dihydroxyphenyl-L-alanine (Dopa) (Waite and Tanzer 1981). origin in marine biofilm, the above information could help us The presence of Dopa seems to play an important role in both to delineate basis of physiological complexity within a single structural integrities of the filaments and underwater adhesion microalgal species biofilm. Such morphological, physiologi- to surfaces by forming covalent cross-links and coordination cal, and genetic basis of complexity is already under investi- bonds with metal ions, as well as by forming hydrogen bonds gation with respect to prokaryotic single species biofilms (e.g., with the surface. The AC3362 protein identified in A. Archaea: Brazelton et al. 2011; Bacteria: Seth et al. 2012). coffeaeformis resembles the cingulins from the diatom Moreover, the identification of genes that implicitly regulates T. pseudonana, whicharealsorichintyrosineresidues microalgal biofilm formation could form the basis for in- (Kröger and Poulsen 2008; Sumper and Brunner 2008). It will biofilm expression technology for understanding other be therefore important to investigate using bioinformatics and microalgal-mediated biofilms as the above approach has been experimental approaches the existence of similar homologs of undertaken in case of bacterial biofilms (e.g., Finelli et al. this protein in other marine diatoms which are known to con- 2003). Since diatoms play a crucial role in biofilm formation, tribute to biofilm formation. it is essential therefore to undertake further identification of While the importance of EPS in biofilm formation is well such genes, develop knockouts for disruption of biofilm, de- known, other metabolic pathways are increasingly important velop robust screening methodologies based on genetic data to in controlling diatom biofilm formation (e.g., Thompson et al. identify stages of biofim, and ultimately strategize manipula- 2008). For example, it has been shown that a novel gene tion methods that could be used to biofouling under control (PtNOA) linked to nitric oxide production (NO) along with from commercial viewpoint. its role in ribosome biogenesis and sporulation has been iden- tified in P. tricornutum (Vardi et al. 2008). When this gene is Industrial scale-up of compounds production over-expressed in transgenic diatoms, higher NO production is displayed and ultimately there is reduced ability to adhere to Detection of antifouling potential from natural resources like surfaces which is important in biofilm formation (Vardi et al. macroalgae is not enough to meet the actual global demand. 2008). It is interesting to note that NOA-like sequences have Thus, industrial scale up of novel antifouling compounds is a been encountered in other marine diatoms and thus the role of prerequisite. However, there are important limitations to in- this gene needs further investigation from the perspective of dustrially scale-up the production of antifouling metabolites from macroalgae. In general, extracting sufficient amounts of biofilm formation. Given that we are now starting to J Appl Phycol (2018) 30:1859–1874 1869 these metabolites may be extremely difficult due to limited production of promising marine algal bioactive metabolites quantity of the producer organism, the small amount of a with antifouling potential (Bhadury and Wright 2004). For specific compound within the target organism, or the variabil- example, the possibility of using metabolic engineering ap- ity of the concentration of these metabolites in response to proach to scale-up production of poly-unsaturated fatty acids biotic and abiotic factors. In consequence, the extraction of has beenexploredinmarinemicroalgae withsomesuccess natural beds of seaweeds is not only ecologically destructive (e.g., Courchesne et al. 2009, Khozin-Goldberg and Cohen but it can also be unstable over time (Proksch et al. 2003; 2011; see review by Mühlroth et al. 2013). Pereira and Costa-Lotufo 2012), although large-scale extrac- Metabolic engineering tools have been also used for over- tion from drift algae may be possible (Siless et al. 2017). production of astaxanthin in microalgae by looking into the Given the limitations encountered with macroalgae, photosyn- over-expression of PSY and CrtR-b genes in Haematococcus thetic microorganisms are attracting considerable interest to- pluvialis (Chlorophyceae) (Li et al. 2008). Given that several wards a sustainable production of natural products. This is due marine algal genomes have been sequenced, such large-scale to their relatively high photosynthetic conversion efficiency, dataset has been also integrated as part of metabolic engineer- novel and diverse metabolic capabilities, faster growth rates, ing tools. In the model marine diatom, P. tricornutum,inter- ability to thrive in diverse ecosystems, and ability to store or vention of metabolic engineering has enhanced accumulation secrete energy-rich hydrocarbons (Radakovits et al. 2010). In of omega-3 long chain polyunsaturated fatty acids through theory, by using (cheap) sunlight and carbon dioxide (which is generation of transgenic strains (Hamilton et al. 2014). Very normally a waste), microalgae can produce high value metab- recently, integration of flux balance analysis (FBA) and in olites of economic importance (such as antifouling metabo- silico proteomics has also shown promising results in terms lites). The potential productivity can be tenfold greater than of metabolic engineering application for sustainable that of agricultural crops and it can take place on non-arable microalgal energy development (e.g., Banerjee et al. 2016). land (Wijffels 2007). Thus, all these factors taken together As mentioned, the industrial scale up of microalgae still makes them economically attractive and more environmental- faces several technological limitations which have to be con- ly friendly source of antifouling compounds. sidered for competing with commodities such as cuprous ox- Commercial large-scale culture of microalgae started in the ide, but we consider it important to explore the possibility of early 1960s with Chlorella, and in a short period, the associated producing effective and more environmental friendly prod- biotechnology industry has grown and diversified significantly ucts. There is huge potential for application of metabolic en- (Spolaore et al. 2006; Borowitzka 2013b). These microorgan- gineering techniques for ultimate industrial scale-up of anti- isms are important sources of commercially produced high- fouling metabolites from marine microalgal origin. In theory, value chemicals including carotenoids, long-chain polyunsatu- it offers not only the possibility to overcome Bsecondary pro- rated fatty acids, and phycobilins (Borowitzka 2013a). Markets duction bottlenecks^ but also to allow us to direct the produc- of microalgae products already exist and are growing, but the tion of secondary metabolites, or of important substrates for growth of the markets is limited by the production technology later synthesis of such antifouling compounds. Since estab- used and cost-price of products, mostly limiting the commercial lishment of transgenic microalgal strains has been production to high-value products (Wijffels 2007). Among the (relatively) easy, a large production of metabolites with anti- main limitations for a successful algal industrial cultivation is fouling applications possibly can be achieved. This is support- the development of easy to use/low cost large operations sys- ed by the increasing availability of genome level data gener- tems, which also combine a sustainable use of water, tempera- ated from Bomics^-based approaches which can be used as ture, light, nutrients, and gas resources, with limited microbial part of RNAi and riboswitch engineering approaches and contamination, necessary to reduce the cost of production while may lead to enhanced production of antifouling metabolites. maintaining and improving product quality (Courchesne et al. At the same time, it can be synchronized with rational bio- 2009;Ugoalaetal. 2012). chemical engineering design for large-scale production of ma- Strain selection is also an important factor. So far, cultiva- rine algal antifouling metabolites using photobioreactor tech- tion of microalgae has been limited to wild type strains of nology. Given that there has been significant technological different species and bioprospecting has been used to isolate development in the field of metabolic engineering, one could new strains with interesting and optimally combined proper- expect that in coming years, this approach could prove to be ties (Hlavová et al. 2015). Microalgae are an extremely di- useful for development of antifouling paints. However, the verse group of organisms, which has not yet been fully ex- genetic improvement of algal strains is a current (moral and plored in terms of diversity (Borowitzka 2013a). However, practical) challenge till now. Modified strains could overpro- researchers are starting to believe that the most cost-effective duce traditional or newly discovered algal compounds and way for industrial production lies in further improvements of also serve to express specific genes that cannot be expressed current strains (Hlavová et al. 2015). It is believed that meta- into other organisms (Spolaore et al. 2006) and, therefore, bolic engineering is the way forward in case of large scale produce different products under specific cultivation 1870 J Appl Phycol (2018) 30:1859–1874 on polysaccharide synthesis in the model diatom, Phaeodactylum conditions. Radakovits et al. (2010) mentioned that more than tricornutum. J Phycol 42:363–378 30 different strains of microalgae have been transformed suc- Abida H, Ruchaud S, Rios L, Humeau A, Probert I, De Vargas C, Bach S, cessfully, but the use of transgenic microalgae for commercial Bowler C (2013) Bioprospecting marine plankton. Mar Drugs 11: applications has not been reported yet. 4594–4611 Águila-Ramírez RN, Arenas-González A, Hernández-Guerrero CJ, As new species are discovered and sequenced, and new tools González-Acosta B, Borges-Souza JM, Verón B, Pope J, Hellio C become available for genetic manipulation, the rich diversity of (2012) Antimicrobial and antifouling activities achieved by extracts microalgae can be exploited for new applications (Ruffing of seaweeds from gulf of California, Mexico. Hidrobiológica 22(1): 2011). The possibility of producing a large amount of biomass 8–15 Ai X-X, Liang J-R, Gao Y-H, Lo SC-L, Lee FW-F, Chen C-P, Luo C-S, in more environmentally friendly conditions offers higher Du C (2015) MALDI-TOF MS analysis of the extracellular poly- chances for a successful industrial scale-up of the process. It is saccharides released by the diatom Thalassiosira pseudonana under likely that such advances can be extended to industrially rele- various nutrient conditions. 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Publisher: Springer Journals
Copyright: Copyright © 2018 by The Author(s)
Subject: Life Sciences; Plant Sciences; Freshwater & Marine Ecology; Plant Physiology; Ecology
ISSN: 0921-8971
eISSN: 1573-5176
DOI: 10.1007/s10811-017-1322-0
Publisher site: See Article on Publisher Site

Abstract

J Appl Phycol (2018) 30:1859–1874 https://doi.org/10.1007/s10811-017-1322-0 1,2 3 4 Mahasweta Saha & Franz Goecke & Punyasloke Bhadury Received: 11 February 2017 /Revised and accepted: 17 October 2017 /Published online: 6 November 2017 The Author(s) 2018 Abstract Marine biofouling is a paramount phenomenon in rather scarce. Thus, we have also discussed the need to con- the marine environment and causes serious problems to mar- duct more chemical ecology based research in relatively less itime industries worldwide. Marine algae are known to pro- explored areas with high algal biodiversity like Southeast duce a wide variety of chemical compounds with antibacterial, Asia. antifungal, antialgal, and anti-macrofouling properties, . . . inhibiting the settlement and growth of other marine fouling Keywords Algae Biofouling Natural products . . . organisms. Significant investigations and progress have been Antifouling defense Antibacterial Anti-diatom made in this field in the last two decades and several antifoul- Anti-macrofouling ing extracts and compounds have been isolated from micro- and macroalgae. In this minireview, we have summarized and evaluated antifouling compounds isolated and identified from Introduction macroalgae and microalgae between January 2010 and June 2016. Future directions for their commercialization Marine biofouling—the colonization and growth of micro- through metabolic engineering and industrial scale up have and macro-organisms on any submerged surface (living and been discussed. Upon comparing biogeographical regions, in- man-made structures) is paramount in the marine environment vestigations from Southeast Asian waters were found to be (Wahl 1989). An average milliliter of natural seawater con- 6 3 2 tains 10 cells of bacteria, 10 microalgae, and 10 propagules of algae and benthic invertebrate larvae (Harder 2009)making any undefended surface quite likely to be colonized by micro- The original version of this article was revised due to a retrospective Open and macro-foulers. Uncontrolled biotic coverage is heavily Access order. detrimental for efficient operation and functioning of such submerged man-made structures (reviewed in Maréchal and * Mahasweta Saha Hellio 2009; Callow and Callow 2011). Biofouling on struc- sahamahasweta@gmail.com tures like ships not only increase ownership costs but are also accompanied with environmental pollution through increased Benthic Ecology, Helmholtz Center for Ocean Research, emission of gases like carbon dioxide, carbon monoxide, and Düsternbrooker weg, 24105 Kiel, Germany sulfur dioxide (Chambers et al. 2006) and is also involved Present address: School of Biological Science, University of Essex, with transport of invasive species (Gollasch 2002). Colchester, CO 43 SQ, UK Remediation of biofouling on ship hulls only costs approxi- Department of Plant and Environmental Science (IPV), Norwegian mately € 120 billion per year (Chapman et al. 2014). To coun- University of Life Sciences (NMBU), Ås, Norway ter such detrimental effects, biofouling was previously con- Integrative Taxonomy and Microbial Ecology Research Group, trolled using toxic antifouling coatings. While the use of anti- Department of Biological Sciences, Indian Institute of Science fouling compounds like tributlyl tin (TBT) and copper oxide Education and Research Kolkata, Mohanpur, Nadia, West Bengal 741246, India have been found to be the most effective method, their non- 1860 J Appl Phycol (2018) 30:1859–1874 targeted effect on other marine organisms like toxicity, large surface area for settlement in benthic marine habitats imposex, bioaccumulative effect, and contamination of the (Seed 1985). Thus, macroalgae are highly susceptible to food chain (Fernández-Alba et al. 2002; Bellas 2006;) has epibiosis in comparison to other potential basibionts. led to a total ban of TBT-based coatings in 2008 by the Macroalgae have evolved efficient defense mechanisms as a International Maritome Organization. Although new biocide mean of protection and thus have been found to be producers formulations like irgarol, chlorothalonil, dichlofluanid, and of wealth of antifouling compounds (reviewed by Bhadury diuron were introduced in marine antifouling AF coatings and Wright 2004;Da Gama et al. 2014). Unlike macroalgae, and initially thought to be environment friendly, later they microalgae are not susceptible to colonization by macro- were reported to be toxic, accumulating in marinas and har- epibionts, but they also experience intense competition for bors (Chapman et al. 2014). The ban of TBT and other toxic space and other resources with their neighbors. Certain AF coatings has drawn a huge amount of interest towards bio- microalgae are known to control their microenvironment inspired AF approaches, i.e., the investigation of novel, through the employment of allelochemicals which have been environment-friendly AF compounds from organisms that suggested to be responsible for observed patchy distribution in are mostly free from foulers colonizing their surfaces. Latest species composition around these microalgae (Saburova et al. strategies towards development of environment-friendly AF 1995; Borowitzka 2016). Such synergistic and antagonistic coatings included biomimetic approaches, Bbiomimicry^ ecological interactions through employment of chemicals (reviewed by Scardino and de Nys 2011), and incorporation have triggered interest among marine natural product chemists of natural antifouling compounds into marine paints leading to the examination of numerous natural products as a (Chambers et al. 2006). However, for their potential appli- possible basis for novel anti-biofilm compounds like cyano- cation in industries, such compounds must be cost effec- gen bromide produced by Nitzschia cf. pellucida tive in terms of production, long lasting, easy to use, and (Vanelslander et al. 2012). non-toxic to marine biota (Ralston and Swain 2009). In the last 5 years, a large number of macroalgal species (89 Efforts made and the systems tested till date have not species in total) and few microalgal species (13 species in been enough successful as they failed to meet all or partly total) have been tested for antifouling activity and several the criteria stated above since such compounds are usually metabolites have been isolated with related bioactivity. The not stable once exposed to the natural environment scope of the current review is to cover their activity against (Maréchal and Hellio 2009); making them durable is a maritime fouling and not medical and industrial fouling. In current challenge. Also, development of a natural product this review, we have summarized the current status of marine is time consuming and a rigorous process. Further, their algal antifouling compounds and extracts isolated and identi- non-toxicity towards non-target species needs to be as- fied between January 2010 and June 2016. We also present sured before being deployed in the field. current challenges and future perspectives on development of Benthic marine environments are quite diverse and charac- antifouling strategies from marine algae. Currently, there is an terized by extreme competition for light, space, nutrient, and important amount of information on metabolic routes, physi- other resources (Wahl 2009). Space being a limiting factor all ological responses, and algal cultivation, and there are an in- potential benthic organisms are also confronted and colonized creasing number of studies on algal genomics (Radakovits by micro and macro settlers—a phenomenon typically termed et al. 2010;Ai et al. 2015; Hlavová et al. 2015; Perez Garcia as epibiosis when the substrate involved is a living one (Wahl and Bashan 2015) which, when grouped together, we consider 1989). As epibiosis is usually detrimental to the (basibiont) essential for the development of algal biotechnology. For a host (Wahl 2008), many basibionts have developed either a potential sustainable development of natural algae-related an- physical or chemical (or both) protection mechanism against tifouling strategies, we have two main focuses: (a) the use of such colonizers, either by themselves (reviewed by Da Gama available and upcoming genomic information to understand et al. 2014) or through symbiotic relationships with bacterial biofouling from the algal genomic perspective (we present the epibionts (reviewed by Singh et al. 2015). Over the past case of diatom genes linked to biofilm formation) and thereby 25 years, several investigations have reported many natural develop gene knock-out-based (or modification) antifouling antifouling compounds being extracted and characterized strategies and (b) it is necessary to couple screening, isolation from varied marine prokaryotes and eukaryotes in assays of compounds, and the genomic studies with industrial against relevant fouling organisms and a number of excellent upscaling and metabolic engineering for a sustainable com- reviews reporting their potential use as antifouling compounds mercial production of natural micro algal compounds. Also, have been published (reviewed by Fusetani 2011;Dobretsov summing up all the ecologically and industrially relevant an- et al. 2013; Puglisi et al. 2014; Qin et al. 2013). tifouling investigations, it is noteworthy that the majority of Being sessile and restricted to the photic zone, macroalgae investigations have focused on algae from temperate waters offer optimal growth conditions to many epibiotic organisms despite the fact that tropical waters are rich in biodiversity. (Harder 2008). Their three-dimensional structure also offers a Therefore, in this review, we have highlighted the importance J Appl Phycol (2018) 30:1859–1874 1861 of expanding the area of sampling to still un-explored zones fucoxanthin and dimethylsulfoniopropionate (DMSP), which (we present Southeast Asia as a case study) with chemical were previously considered to have just primary functions, ecology research objectives, i.e., isolating and testing natural have been reported to function as regulators of the microbial compounds in ecologically relevant bioassays. density and composition over Fucus vesiculosus (Lachnit et al. 2013; Saha et al. 2011, 2012, 2014). Identified com- pounds with AF activity are provided in Fig. 2. Antifouling compounds from macroalgae Furthermore, many other studies have investigated the ac- tivities of both polar and non-polar extracts and reported anti- Apart from being the major primary producers in temperate bacterial, antimicroalgal, and antifungal properties from a va- ecosystems and the largest biomass producers in marine envi- riety of algae belonging to the genera Caulerpa, Chondrus, ronment, macroalgae produce a diverse array of natural com- Dictyota, Padina, Sargassum,and Ulva (Chambers et al. pounds as mode of protection against natural enemies 2011;Cho 2013; Ktari et al. 2010; Silva et al. 2013,see (Goecke et al. 2010). Over the last 5 years, a number of studies Table 1). (some of which are discussed below) have reported new anti- In terms of number of species, more than a quarter of the fouling compounds from macroalgal extracts like the studies involved red macroalgae and the remaining two third cystophloroketals and chromanols, along with an increasing was composed of brown and green seaweeds (Fig. 1). In terms number of reports of activities from crude extracts of different of the chosen bioactivity, most of the studies demonstrated an polarities (Table 1,Fig. 1). antimacrofouling activity (e.g., Maréchal and Hellio 2011; Certain genera, like the red algae Asparagopsis and Van Alstyne et al. 2014) followed by antibacterial (e.g., Laurencia,andthebrownalga Sargassum continue to be Silva et al. 2013;Natrah et al. 2015) and antimicroalgal activ- source of new active antifouling compounds. Asparagopsis ity (e.g. Silkina et al. 2012; Sun et al. 2015). This may be spp. belong to the order Bonnemaisoniales, which is known based on the fact that, space being limited in the benthic en- to be a rich source of halogenated bioactive compounds (Jha vironment, macrofoulers usually tend to settle on macroalgal et al. 2013). Recent study of the introduced red alga surfaces thereby selecting for antimacrofouling defenses. Asparagopsis taxiformis collected from the Indian Ocean Also, epibacterial colonization is ubiquitous on algal surfaces has led to the discovery of two new highly brominated with the ability to negatively impact macroalgal fitness (Wahl cyclopentenones: mahorone and 5-bromomahorone with an- et al. 2012) thereby selecting for antibacterial defenses. timicrobial activity against both marine and terrestrial mi- crobes (Greff et al. 2014). Another investigation on the same species, collected from the intertidal region of the Arabian Sea Antifouling compounds from dinoflagellates, and Bay of Bengal, has found the methanolic extract to have diatoms, and other marine microalgae anti-quorum sensing activity (Jha et al. 2013). Other seaweed species have also been shown to produce quorum-sensing Several studies have been conducted to investigate the prod- inhibitors (Carvalho et al. 2017). Members of the genus ucts of microalgal metabolism, not only to understand its na- Laurencia (Ceramiales) are also known to be a rich source ture but also to search for substances with possible applica- of halogenated secondary metabolites (Blunt et al. 2009)and tions to humans in different fields of interest (de De Morais they continue to be source of new compounds. Recently, a et al. 2015). Some of the earliest and most extensive research new omaezallene and four new polyether triterpenoids with on microalgal secondary metabolites has been on anti-macrofouling activity have been discovered from cyanobacteria, dinoflagellates (Dinophyceae), a few other Laurencia sp. and Laurencia viridis, respectively (Umezawa microflagellates, and diatoms (Bacillariophyceae) (Garcia et al. 2014; Cen-Pacheco et al. 2015). Camacho et al. 2007). This is because of the ability of certain Brown algae of the genus Cystoseira (Fucales) are known bloom-forming species to produce structurally quite diverse to be good source of bioactive terpenoid derivates, specially toxins like brevetoxins produced by Karenia brevis (Fig. 3). meroterpenoids and diterpenoids (reviewed by Gouveia et al. Such bloom phenomena by toxic microalgae are generally 2013). A monocyclic meroditerpenoid isolated from known as harmful algal blooms (HABs). HABs can be highly Cystoseira tamariscifolia has shown high potential for inhibi- toxic to humans and other animals and have further dramatic tion of common foulers like Balanus amphitrite and Mytilus health and socio-economic impacts (Pearson et al. 2010; edulis. Cystophloroketals A and B from the same alga have Clément et al. 2016;Mazard et al. 2016). shown high inhibition activity against two species of fouling Different species from divergent phylogenetic orders of the microalgae and moderate antimicrobial activity against a dinoflagellates produce phytotoxins, e.g., Alexandrium spp. range of bacteria, fungi, and microalgae (Hattab et al. 2015). and Protoceratium spp. (Gonyaulacales), Azadinium sp. Along with the reported role of pholorotannins as antifoulants (Dinophyceae incertae sedis), Dinophysis spp. from certain fucoid species, certain metabolites like (Dinophysiales), Gymnodinium spp. and Karenia spp. 1862 J Appl Phycol (2018) 30:1859–1874 Table 1 Antifouling compounds and extracts from macroalgae Source Biogenic compound(s)/type of extract Bioactivity Origin Reference RHO Asparagopsis taxiformis Mahorone AB Mayotte Greff et al. 2014 5-bromomahorone RHO Asparagopsis taxiformis Methanolic extract AB, QSD India Jha et al. 2013 RHO 2 Bonnemaisonia hamifera 1,1,3,3-Tetrabromo-2-heptanone ABF Sweden Persson et al. 2011 CHL Caulerpa prolifera Ethanol and methanol extracts AB Brazil Silva et al. 2013 RHO Ceramium botryocarpum Ethanol fraction AA France Silkina et al. 2012 RHO Ceramium rubrum Dichloromethane extract AF Chile Cortés et al. 2014 RHO Chondrus crispus Toluene-soluble ABF Ireland Salta et al. 2013 crude ethanolic extract RHO Chondrus crispus Crude ethanol extracts AA, AB Ireland Chambers et al. 2011 CHL Cladophora clavuligera Methanolic and dichloromethane extract AB India Bragadeeswaran et al. 2011a PHE Cystoseira tamariscifolia Cystophloroketals A-B AA, AB, AF Algeria Hattab et al. 2015 PHE Cystoseira tamariscifolia monocyclic meroditerpenoid AMF Algeria Hattab et al. 2015 PHE Dictyota spp. Diterpenes, glicerol derivatives AB, AF France Othmani et al. 2014 PHE Dictyota fasciola Dichloromethane and methanol extract AA, AB, AMF Tunisia Ktari et al. 2010 CHL Dictyosphaeria ocellata Methanol extract AB, ABF USA Sneed and Pohnert 2011a, b PHE 3 4 5 Fucus vesiculosus Fucoxanthin , dimethyl sulphopropionate ,proline AB, ABF Germany Saha et al. 2011, 2012, Wahl et al. 2010, Lachnit et al. 2013 RHO Gracilaria edulis Isoamyl alcohol extract AB India Rajan et al. 2015 RHO Hypnea musciformes Ethanol and methanol extracts AB Brazil Silva et al. 2013 RHO Laurencia johnstonii Ethly ether extract AA, AB, AF Mexico Águila-Ramírez et al. 2012 RHO 6 Laurencia sp. Omaezallene AMF Japan Umezawa et al. 2014 intricatetraol RHO Laurencia translucida Fatty acid derivatives AMF Brazil Paradas et al. 2016 RHO Laurencia viridis 28-Hydroxysaiyacenol B AMF Spain Cen-Pacheco et al. 2015 Saiyacenol C 15,16-epoxythyrsiferol A 15,16-Epoxythyrsiferol B PHE Padina gymnospora Ethanol and methanol extracts AB Brazil Silva et al. 2013 PHE 8 Sargassum horneri Chromanols AA, AB, AMF South Korea Cho 2013 PHE Sargassum muticum Galactoglycerolipids AB, AF, AMF France Plouguerné et al. 2010b PHE Sargassum muticum Ethanol fraction AA France Silkina et al. 2012 PHE Sargassum polyceratium Hexane extract AB Martinique Thabard et al. (2011) PHE Sargassum wightii Methanol extract AB India Bragadeeswaran et al. 2011b PHE Sargassum vulgare Unidentified polar compounds AMF Brazil Plouguerné et al. 2012 PHE Sargassum vulgare Hexane extracts AA, AB, AMF Brazil Plouguerné et al. 2010a methanol and dichloromethane extracts polyphenolic extracts RHO 9 Sphaerococcus coronopifolius Bromosphaerol AMF Greece Piazza et al. 2011 PHE Taonia atomaria sesquiterpenes AB, AMF France Othmani et al. 2015 polyunsaturated fatty acids CHL Ulva fasciata Ethanol and methanol extracts AB Brazil Silva et al. 2013 CHL Ulva intestinalis Hexane extract AB Thailand * Srikong et al. 2015 CHL Ulva lactuca Ethyl ethanol extract AA, AB, AF Mexico Águila-Ramírez et al. 2012 CHL Ulva pertusa Alkaloids, phenolic acid AA China Sun et al. 2015 CHL Ulvaria obscura Dopamine AA, AMF USA Van Alstyne et al. 2014 CHL,PHE,RHO 8spp.macroalgae Methanol extract AB Malaysia* Natrah et al. 2015 CHL,PHE,RHO 11 spp. macroalgae Polar and non-polar extracts QSD Brazil Batista et al. 2014 CHL,PHE,RHO 30 spp. macroalgae Diverse aqueous and organic extracts AMF France Maréchal and Hellio 2011 The bioactivities are the following: antibacterial activity (AB), antifungal (AF), anti-microalgal including diatoms and cyanobacteria (AA), anti- macrofouling including mollusks (AMF), quorum sensing disruptor (QSD), and anti-biofilm (ABF). Also the algae groups: Chlorophyta (CHL), Phaeophyceae (PHE), and Rhodophyta (RHO). Studies made in Southeast Asia are highlighted with an asterisk. 1–9 = compounds listed in Fig. 2 (Gymnodiniales), and Prorocentrum spp. (Prorocentrales), and production of such toxins has been seen as an ecological ad- diatoms as well as Pseudonitzschia spp. (Bacillariales). Such vantage since the release of those chemicals into the environ- diversity is magnified at a rich subspecies level, and in conse- ment may deter, inhibit growth, or kill competing species and quence, the heterogeneity of associated phycotoxins and its predators (Caroppo and Pagliara 2011;Maetal. 2011;Poulson- derivatives are quite variable and big (Orr et al. 2013). The Ellestad et al. 2014; Rolton et al. 2014; Bagwell et al. 2016). J Appl Phycol (2018) 30:1859–1874 1863 Fig. 1 Bioactivity of metabolites or extract fractions from a total of 24 species of red algae, 13 species of green algae, and 18 species of brown algae, active against marine relevant species during the period 2010–2016. Antibacterial activity (AB), antifungal (AF), anti-microalgal including diatoms and cyanobacteria (AA), anti- macrofouling including mollusks and crustacean (AMF), quorum sensing disruptor (QSD), toxins (TX), and anti-biofilm (ABF) No. of studies Allelopathic interactions between microalgal species also may Between January 2010 and June 2016, only 14 relevant contribute to the formation and succession of red tides (Cai studies were conducted on marine microalgal species, which et al. 2014). As the interactions with many potential foulers tested extracts against other marine organisms. Only few com- are regulated by chemical cues, there is a high potential in the pounds (e.g., fatty acids) were isolated from diatoms and di- identification and use of such compounds for biotechnological noflagellates which have demonstrated antimicrobial or anti- applications like antifouling compounds. fouling activities (Desbois et al. 2010). Although the number With respect to other microalgae groups, in the last decade, of isolated compounds is clearly less than in cyanobacteria most of the studies had focused on the content of fatty acids (data not shown), the potential exists to increase that number, and pigments aiming for their use in biotechnology, e.g., ca- because most of these studies have reported bioactivity of rotenoids and polyunsaturated fatty acids (PUFAs) for feed, diverse cultures and their organic extracts but did not isolate and as active ingredients for cosmetics, among others (Abida the active compounds as yet (Table 2). et al. 2013; Borowitzka 2013a). Even though green In terms of number of species, half of the studies involved microalgae are generally regarded safe for human consump- dinoflagellates and most of the second half was composed of tion, there is still a knowledge gap in understanding the met- diatoms. Only one study incorporated a marine haptophyte, abolic and biochemical potential of these algae (Bagwell et al. and thus, many other microalgal groups remain unstudied 2016). (Fig. 4). In terms of the chosen bioactivity, most of the studies (1) 5-bromomahorone (2) 1,1,3,3- tetrabromo-2-heptanone (3) Fucoxanthin (4) DMSP R=Br (5) Proline (6) Omaezallene (7) Intricatetraol (8) Chromanol (9) Bromosphaerol Fig. 2 .Selected antifouling compounds from macroalgae 1864 J Appl Phycol (2018) 30:1859–1874 Fig. 3 Brevetoxins from microalgae Karenia brevis (10) Brevetoxins demonstrated an antialgal activity (Fig. 4). The latter may be of ecosystems, ranging from extensive lagoons, estuaries, and based on the fact that the production of antialgal metabolites mangroves, to rocky shores and coral reefs, which provide would be an ecological advantage in a specific niche and/or suitable habitats for luxuriant algal growth (Nguyen et al. space. Furthermore, organisms like mollusks and crustaceans 2013). In fact, the triangle formed by the Malay Peninsula, not only compete with benthic microalgae for space, but are The Philippines, plus New Guinea (BThe Coral Triangle^)is also important microalgal consumers, with the ability to affect recognized as a global biodiversity hotspot where most trop- microalgal populations. ical marine groups have their greatest diversity of species (Todd et al. 2010; Selig et al. 2014). Researchers have noticed that a high diversity of species may be translated in a higher A case study: antifouling compounds from Southeast diversity of secondary metabolites. But not only that, those Asia species may harbor silent gene clusters coding the production of Bnew^ metabolites, which may be expressed under differ- ent environmental conditions (Bode et al. 2002; Brakhage and Southeast Asia has an outstanding species richness and ende- mism. It has an extensive coastline (e.g., Indonesia, Schroeckh 2011). Thus, biogeography may multiply this num- ber and even enhance bioactivity of such metabolites. 81.000 km; Vietnam, 3.260 km) with many islands and rivers flowing into the extended and large continental shelf The exact number of macro- and micro-algal species for (Aungtonya and Liao 2002; Gerung et al. 2006; Soe-Htun Southeast Asia is still unknown and there are many species yet et al. 2009; Phang et al. 2015). This produces a diverse variety to be discovered (Kawaguchi and Hayashizaki 2011). Table 2 Antifouling compounds and extracts from dinoflagellates and diatoms Source Biogenic compound(s)/ type of extract Bioactivity Origin Reference DF Alexandrium tamarense Lipidic extracts AA Scotland Ma et al. 2011 DI Amphora cf. capitellata Ethanol extract AF Turkey Montalvaõ et al. 2016 HA Isochrysis galbana Fatty acids AB Isle of Man Molina-Cárdenas et al. 2014 DF Karenia brevis Culture extracts, 6 unidentified compounds AA USA Poulson et al. 2010 DF Karenia brevis Diverse metabolites AA USA Prince et al. 2010 DF Karenia brevis Culture extracts, unidentified compounds AA USA Poulson-Ellestad et al. 2014 DF 10 Karenia brevis Culture extracts, brevetoxins AMF, TX USA Rolton et al. 2014 DF Lingulodinium polyedrum Diverse extracts AB Mexico Quijano-Scheggia 2016 DI Nitzschia communis Ethanol extract AB Turkey Montalvaõ et al. 2016 DI Odontella aurita Ethanol extract AB India Hemalatha et al. 2016 DF Ostreopsis cf. ovata Culture extracts AMF, TX Italy Caroppo and Pagliara 2011 DF Ostreopsis cf. ovata Palytoxin-like compounds AMF, TX Italy Gorbi et al. 2012 DI Phaeodactylum tricornutum Culture extracts AA China Cai et al. 2014 DF Prorocentrum donghaiense Culture extracts AA China Cai et al. 2014 DF Protoceratium reticulatum Culture extracts AA Greenland Sala-Pérez et al. 2016 DI Skeletonema marinoi Acetonic extracts AB Italy Lauritano et al. 2016 DI Thalassiosira rotula Diverse extracts AB Australia Qin et al. 2013 The bioactivities are the following: antibacterial activity (AB), antifungal (AF), anti-macroalgal (AM), anti-microalgal including diatoms and cyanobacteria (AA), anti-macrofouling including mollusks (AMF), quorum sensing disruptor (QSD), anti-biofilm (ABF), and toxins (TX). Also the algae groups: diatoms (DI), dinoflagellates (DF), and haptophytes (HA). 10 = compound listed in Fig. 3 J Appl Phycol (2018) 30:1859–1874 1865 Fig. 4 Bioactivity of metabolites or extracts fractions from a total of six species of dinoflagellates, five species of diatoms and one haptophyte, active against marine relevant species during the period 2010–2016. Antibacterial activity (AB), antifungal (AF), anti- microalgal including diatoms and cyanobacteria (AA), anti- macrofouling including mollusks and crustacean (AMF), quorum sensing disruptor (QSD), toxins (TX), and anti-biofilm (ABF) No. of studies Research has mostly focused on economic resources, as sev- Antifouling compounds from S.E.A eral macroalgae are important economic resources in Southeast Asia (S.E.A.). Thus, the existing coverage of spe- Although, studies looking at the antifouling activity of algae cies is conspicuous by the omission of small groups (Wafar (micro and macro) are limited in S.E.A. compared to et al. 2011), or other Bless important^ economic species, and European and North American waters (Fig. 5), nevertheless therefore, we understand little of their distributions and poten- studies over the last decade have shown promising antifouling tial uses (Webb et al. 2010). Given the unlocked potential of activities from Southeast Asian algae. Majority of the studies algal compounds from S.E.A, in this review, we have from Southeast Asian waters have been largely focused on highlighted the importance of exploring this area with more marine macroalgae, and antifouling activity was examined depth. based on crude extract assays (e.g. Bhadury and Wright 2004 and references within; Sidharthan et al. 2004;Qian et al. 2010 and references within; Satheesh et al. 2016 and Algal compounds in general from S.E.A references within). Identified compounds so far from Southeast Asia with AF activity are provided in Fig. 6.An If we compare the collection effort globally of all type of integrative approach involving identification of secondary organisms, the S.E.A region has been well explored and metabolites from the crude extracts has been far less studied reporting of compounds from these regions has been rapidly compared to information available from other geographical accelerating since 1990 (Blunt et al. 2016). According to origins. This reflects the need to undertake approaches involv- Blunt et al. (2016), maritime Southeast Asia (and Papua ing GC-MS and NMR for identification of potential potent New Guinea) has produced in 50 years 1340 compounds as antifouling secondary metabolites. While, Southeast Asia har- reported in 502 publications, plus the mainland of Southeast bors high biodiversity including rich marine microalgae and Asia (including East Malaysia) has produced 457 compounds macroalgal diversity, their potential for antifouling activity in in 173 publications. However, considering the information in an ecological context is yet to be effectively explored. the excellent reviews of new marine natural products pub- lished by Blunt et al. (2011, 2012, 2013, 2014, 2015, 2016), Linking genes to biofilm formation between the years 2008 to 2014, the contribution of com- pounds isolated from marine algae species growing in S.E.A Among the early colonizers, diatoms play a significant role in is limited to only 29 compounds, from which only 23 are biofilm development and are able to colonize on even most newly described for science (Table 3), when compared to the fouling-resistant surfaces (Molino and Wetherbee 2008). compounds described from algae collected worldwide. It is Currently, our understanding of the role of genes during also interesting to note that the investigations were mostly bacteria-diatom interaction as part of biofilm formation is rel- limited to red algae of the genus Laurencia (Table 4). When atively well understood (e.g., Buhmann et al. 2012 and we compare the total amount of new natural compounds re- references within). However, limited knowledge exists in ported from marine algae worldwide, the yield of natural com- terms of the genes that are exclusively found in marine dia- pounds from marine algae reported from Southeast Asia is not toms and their link to marine biofilm formation. The recent significant (Fig. 5), contradicting the great diversity of the availability of phytoplankton genome sequence data, in area. particular diatom genomes, has resulted in improved 1866 J Appl Phycol (2018) 30:1859–1874 Table 3 Detail of the yearly new identified natural compounds isolated from different marine algae groups (data based on Blunt et al. 2016). The contribution of compounds isolated from species growing in Southeast Asia (S.E.A) is specified New identified compounds Organisms 2008 2008 2009 2009 2010 2010 2011 2011 2012 2012 2013 2013 2014 2014 total SEA total SEA total SEA total SEA total SEA total SEA total SEA Dinoflagellates 8 0 12 0 17 0 2 0 2 0 9 0 19 0 Diatoms, other 10 00 0 0 3 0 00 4 0 00 microalgae Chlorophyta 4 0 6 08 03 0 2 05 013 0 Phaeophyceae 45 0 25 0 10 0 25 0 32 0 17 0 17 0 Rhodophyta 24 3 49 0 47 7 41 1 45 1 9 0 41 1 understanding of mechanisms that control their growth and Thalassiosira pseudonana shows that degree of polymeriza- distribution in the marine environment (e.g., Armbrust et al. tion and distribution of EPSs can vary in response to nutrient 2004;Bowler etal. 2008). Thus, the rapidly available diatom depletion and different nutrient sources (Ai et al. 2015). genome datasets can help in understanding the role of biosyn- Proteins and glycoproteins have been studied by chemical thetic pathways towards production and regulation of extra- methods and by atomic force microscopy (Lind et al. 1997; cellular polymeric substances (EPS) during the process of Wustman et al. 1997; Dugdale et al. 2006; Chiovitti et al. biofouling. 2008). It has been shown that the adhesive molecules appear From the cellular viewpoint, the adhesive components of to be highly glycosylated with novel glycans that are highly EPS are involved in diatom cell-substratum adhesion, in ad- sulphated (Chiovitti et al. 2003, 2008). dition to motility. EPS molecules are secreted from frustules In a recent study, from the available genome dataset of the through pores in the girdle bands and valves. The carbohy- pennate diatom Phaeodactylum tricornutum, bioinformatic drate components of the EPS have been characterized in var- analysis was undertaken to identify putative diatom cell sub- ious benthic diatoms (e.g., Chiovitti et al. 2008; Abdullahi stratum adhesion molecules (PDC) (Willis et al. 2014). In et al. 2006). It is already well known that EPS secretion in total, 37 PDCs were identified from the P. tricornutum ge- diatoms depends on numerous factors including nutrient avail- nome, of which some showed similarities to genes found in ability, daily fluctuations, irradiance, and even metal toxicity a diverse range of organisms, including metazoans, plants, and (Staats et al. 1999;Ai et al. 2015). This is particularly signif- prokaryotes, as well as algae, encoding components of the icant since EPSs can be a food source for heterotrophic organ- extracellular matrix (ECM) or cell adhesion complexes isms and affect the detachment of biofilms (e.g., De Brouwer (Yamada and Geiger 1997;Zhao and Waite 2006). It has been and Stal 2002; Bellinger et al. 2005). For example, nitrogen found that genes that code for PDCs have characterizing fea- and phosphate limitations affect production rate of EPSs in- tures that are common to a set of cell adhesion molecule cluding chemical composition in various diatoms (Magaletti (CAM) genes (Willis et al. 2014). Indeed, using bioinformatic et al. 2014;Ai et al. 2015). Mass spectrometry of EPSs of approach, we detected the presence of CAM genes across Table 4 Natural compounds isolated from different marine algae groups from Southeast Asia (data based on Blunt et al. 2016). The geographical origin and bioactivity of compounds are specified Taxa Compound Bioactivity Origin Reference RH n Gracilaria edulis Levuglandin D – The Philippines Kanai et al. 2011 RH n Laurencia nangii Dihydroitomanallene B – Malaysia Kamada and Vairappan 2012 pannosallene itomanallene B RH n, 13 Laurencia snackeyi 5β-Hydroxypalisadin B – Malaysia Wijesinghe et al. 2014 RH n, 14,15,16 Laurencia sp. Laurefurenyne A-F cytotoxic The Philippines Abdel-Mageed et al. 2010 RH n Laurencia sp. Tiomanene – Malaysia Vairappan et al. 2008 n, 17 acetylmajapolene A-B n new compounds RH rhodophyta 11–17 Compounds listed in Fig. 6 J Appl Phycol (2018) 30:1859–1874 1867 Fig. 5 Studies conducted between January 2010 and June 2016 based on geographical locations. % by zone = America 32%, Europe 34%, Africa 6%, Oceania 2%, Asia 23%, S.E.A. 4% (of the 23% of Asia) sequenced marine micro- and macroalgal genomes (Fig. 7). diatom cell adhesion. Based on the analysis of the As evident from Fig. 4, these amino acid sequences T. pseudonana genome, several putative cell adhesion mole- representing CAM are conserved across different marine cules have been identified using bioinformatics approach. algae and thus may also indicate the possible existence of From the available transcriptome data of the model adhe- putative PDCs in published marine algal genomes. Willis sion diatom, Amphora coffeaeformis, five proteins have been et al. (2014) reported that some of the PDCs were diatom identified that exhibit unique amino acid sequences resem- specific and encoded unclear functions. These putative genes bling the amino acid composition of the tyrosine-rich adhe- indicate that there is likely a diverse range of molecules that sion proteins from mussel footpads (Buhmann et al. 2014). diatoms use for cell substratum adhesion and therefore these Buhmann et al. (2014) looked into the function of one of these genes potentially may play key role in biofouling. Seven of proteins, AC3362 by undertaking genetic transformation of A. these PDC have been characterized in vivo, by generation of coffeaeformis. They found that AC3362 plays a role in bio- transgenic diatom lines over-expressing genes encoding C- synthesis and or structural stability of the cell wall of this terminal yellow fluorescent protein (YFP) fusion proteins, pennate diatom. The findings of AC3362 protein is particular- and showed that these candidate proteins are involved in ly significant since in many mussel foot proteins, tyrosine (11) Pannosallene (12) Itomanallene B (13) 5β-hydroxypalisadin B (14) LaurefurenyneA-B R=OH (Z and E denotes isomer) (15) Laurefurenyne C (16) Laurefurenyne F (17) Acetylmajapolene A Fig. 6 Antifouling compounds isolated from Southeast Asian macroalgae 1868 J Appl Phycol (2018) 30:1859–1874 Fig. 7 Amino acid sequence alignment of CAM gene from Thalassiosira tricornutum CCAP1055 (Acc No. XP_002185049), Guillardia theta pseudonana CCMP1335 (Acc No. XM_002295719), Aureococcus CCMP2712 (Acc No. XP_005836584) and Gracilariopsis anophagefferens (Acc No XP_009033803), Phaeodactylum lemaneiformis (Acc No. AKG55580) showing highly conserved regions residues have been post-translationally hydroxylated to 3,4- understand specific role of genes and proteins of microalgal dihydroxyphenyl-L-alanine (Dopa) (Waite and Tanzer 1981). origin in marine biofilm, the above information could help us The presence of Dopa seems to play an important role in both to delineate basis of physiological complexity within a single structural integrities of the filaments and underwater adhesion microalgal species biofilm. Such morphological, physiologi- to surfaces by forming covalent cross-links and coordination cal, and genetic basis of complexity is already under investi- bonds with metal ions, as well as by forming hydrogen bonds gation with respect to prokaryotic single species biofilms (e.g., with the surface. The AC3362 protein identified in A. Archaea: Brazelton et al. 2011; Bacteria: Seth et al. 2012). coffeaeformis resembles the cingulins from the diatom Moreover, the identification of genes that implicitly regulates T. pseudonana, whicharealsorichintyrosineresidues microalgal biofilm formation could form the basis for in- (Kröger and Poulsen 2008; Sumper and Brunner 2008). It will biofilm expression technology for understanding other be therefore important to investigate using bioinformatics and microalgal-mediated biofilms as the above approach has been experimental approaches the existence of similar homologs of undertaken in case of bacterial biofilms (e.g., Finelli et al. this protein in other marine diatoms which are known to con- 2003). Since diatoms play a crucial role in biofilm formation, tribute to biofilm formation. it is essential therefore to undertake further identification of While the importance of EPS in biofilm formation is well such genes, develop knockouts for disruption of biofilm, de- known, other metabolic pathways are increasingly important velop robust screening methodologies based on genetic data to in controlling diatom biofilm formation (e.g., Thompson et al. identify stages of biofim, and ultimately strategize manipula- 2008). For example, it has been shown that a novel gene tion methods that could be used to biofouling under control (PtNOA) linked to nitric oxide production (NO) along with from commercial viewpoint. its role in ribosome biogenesis and sporulation has been iden- tified in P. tricornutum (Vardi et al. 2008). When this gene is Industrial scale-up of compounds production over-expressed in transgenic diatoms, higher NO production is displayed and ultimately there is reduced ability to adhere to Detection of antifouling potential from natural resources like surfaces which is important in biofilm formation (Vardi et al. macroalgae is not enough to meet the actual global demand. 2008). It is interesting to note that NOA-like sequences have Thus, industrial scale up of novel antifouling compounds is a been encountered in other marine diatoms and thus the role of prerequisite. However, there are important limitations to in- this gene needs further investigation from the perspective of dustrially scale-up the production of antifouling metabolites from macroalgae. In general, extracting sufficient amounts of biofilm formation. Given that we are now starting to J Appl Phycol (2018) 30:1859–1874 1869 these metabolites may be extremely difficult due to limited production of promising marine algal bioactive metabolites quantity of the producer organism, the small amount of a with antifouling potential (Bhadury and Wright 2004). For specific compound within the target organism, or the variabil- example, the possibility of using metabolic engineering ap- ity of the concentration of these metabolites in response to proach to scale-up production of poly-unsaturated fatty acids biotic and abiotic factors. In consequence, the extraction of has beenexploredinmarinemicroalgae withsomesuccess natural beds of seaweeds is not only ecologically destructive (e.g., Courchesne et al. 2009, Khozin-Goldberg and Cohen but it can also be unstable over time (Proksch et al. 2003; 2011; see review by Mühlroth et al. 2013). Pereira and Costa-Lotufo 2012), although large-scale extrac- Metabolic engineering tools have been also used for over- tion from drift algae may be possible (Siless et al. 2017). production of astaxanthin in microalgae by looking into the Given the limitations encountered with macroalgae, photosyn- over-expression of PSY and CrtR-b genes in Haematococcus thetic microorganisms are attracting considerable interest to- pluvialis (Chlorophyceae) (Li et al. 2008). Given that several wards a sustainable production of natural products. This is due marine algal genomes have been sequenced, such large-scale to their relatively high photosynthetic conversion efficiency, dataset has been also integrated as part of metabolic engineer- novel and diverse metabolic capabilities, faster growth rates, ing tools. In the model marine diatom, P. tricornutum,inter- ability to thrive in diverse ecosystems, and ability to store or vention of metabolic engineering has enhanced accumulation secrete energy-rich hydrocarbons (Radakovits et al. 2010). In of omega-3 long chain polyunsaturated fatty acids through theory, by using (cheap) sunlight and carbon dioxide (which is generation of transgenic strains (Hamilton et al. 2014). Very normally a waste), microalgae can produce high value metab- recently, integration of flux balance analysis (FBA) and in olites of economic importance (such as antifouling metabo- silico proteomics has also shown promising results in terms lites). The potential productivity can be tenfold greater than of metabolic engineering application for sustainable that of agricultural crops and it can take place on non-arable microalgal energy development (e.g., Banerjee et al. 2016). land (Wijffels 2007). Thus, all these factors taken together As mentioned, the industrial scale up of microalgae still makes them economically attractive and more environmental- faces several technological limitations which have to be con- ly friendly source of antifouling compounds. sidered for competing with commodities such as cuprous ox- Commercial large-scale culture of microalgae started in the ide, but we consider it important to explore the possibility of early 1960s with Chlorella, and in a short period, the associated producing effective and more environmental friendly prod- biotechnology industry has grown and diversified significantly ucts. There is huge potential for application of metabolic en- (Spolaore et al. 2006; Borowitzka 2013b). These microorgan- gineering techniques for ultimate industrial scale-up of anti- isms are important sources of commercially produced high- fouling metabolites from marine microalgal origin. In theory, value chemicals including carotenoids, long-chain polyunsatu- it offers not only the possibility to overcome Bsecondary pro- rated fatty acids, and phycobilins (Borowitzka 2013a). Markets duction bottlenecks^ but also to allow us to direct the produc- of microalgae products already exist and are growing, but the tion of secondary metabolites, or of important substrates for growth of the markets is limited by the production technology later synthesis of such antifouling compounds. Since estab- used and cost-price of products, mostly limiting the commercial lishment of transgenic microalgal strains has been production to high-value products (Wijffels 2007). Among the (relatively) easy, a large production of metabolites with anti- main limitations for a successful algal industrial cultivation is fouling applications possibly can be achieved. This is support- the development of easy to use/low cost large operations sys- ed by the increasing availability of genome level data gener- tems, which also combine a sustainable use of water, tempera- ated from Bomics^-based approaches which can be used as ture, light, nutrients, and gas resources, with limited microbial part of RNAi and riboswitch engineering approaches and contamination, necessary to reduce the cost of production while may lead to enhanced production of antifouling metabolites. maintaining and improving product quality (Courchesne et al. At the same time, it can be synchronized with rational bio- 2009;Ugoalaetal. 2012). chemical engineering design for large-scale production of ma- Strain selection is also an important factor. So far, cultiva- rine algal antifouling metabolites using photobioreactor tech- tion of microalgae has been limited to wild type strains of nology. Given that there has been significant technological different species and bioprospecting has been used to isolate development in the field of metabolic engineering, one could new strains with interesting and optimally combined proper- expect that in coming years, this approach could prove to be ties (Hlavová et al. 2015). Microalgae are an extremely di- useful for development of antifouling paints. However, the verse group of organisms, which has not yet been fully ex- genetic improvement of algal strains is a current (moral and plored in terms of diversity (Borowitzka 2013a). However, practical) challenge till now. Modified strains could overpro- researchers are starting to believe that the most cost-effective duce traditional or newly discovered algal compounds and way for industrial production lies in further improvements of also serve to express specific genes that cannot be expressed current strains (Hlavová et al. 2015). It is believed that meta- into other organisms (Spolaore et al. 2006) and, therefore, bolic engineering is the way forward in case of large scale produce different products under specific cultivation 1870 J Appl Phycol (2018) 30:1859–1874 on polysaccharide synthesis in the model diatom, Phaeodactylum conditions. Radakovits et al. (2010) mentioned that more than tricornutum. J Phycol 42:363–378 30 different strains of microalgae have been transformed suc- Abida H, Ruchaud S, Rios L, Humeau A, Probert I, De Vargas C, Bach S, cessfully, but the use of transgenic microalgae for commercial Bowler C (2013) Bioprospecting marine plankton. 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Journal

Journal of Applied Phycology – Springer Journals

Published: Nov 6, 2017

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Mode of action of membrane-disruptive lytic compounds from the marine dinoflagellate Alexandrium tamarense

Ma, H; Krock, B; Tillmann, U; Bickmeyer, U; Graeve, M; Cembella, A
Abundance and chemical characterization of extracellular carbohydrates released by the marine diatom Cylindrotheca fusiformis under N- and P-limitation

Magaletti, E; Urbani, R; Sist, P; Cicero, AM
Challenges for the development of new non-toxic antifouling solutions

Maréchal, J-P; Hellio, C
Antifouling activity against barnacle cypris larvae: do target species matter (Amphibalanus amphitrite versus Semibalanus balanoides)?

Maréchal, J-P; Hellio, C
Tiny microbes with a big impact: The role of Cyanobacteria and their metabolites in shaping our future

Mazard, S; Penesyan, A; Ostrowski, M; Paulsen, IT; Egan, S
Inhibition of pathogenic Vibrio by the microalgae Isochrysis galbana

Molina-Cárdenas, CA; Sánchez-Saavedra, MP; Lizárraga-Partida, ML
The biology of biofouling diatoms and their role in the development of microbial slimes

Molino, PJ; Wetherbee, R
Large-scale bioprospecting of cyanobacteria, micro- and macroalgae from the Aegean Sea

Montalvaõ, S; Demirel, Z; Devi, P; Lombardi, V; Hongisto, V; Perälä, M; Hattara, J; Imamoglu, E; Shet Tilvi, S; Turan, G; Conk Dalay, M; Tammela, P
Pathways of lipid metabolism in marine algae, co-expression network, bottlenecks and candidate genes for enhanced production of EPA and DHA in species of Chromista

Mühlroth, A; Li, K; Røkke, G; Winge, P; Olsen, Y; Hohmann-Marriott, MF; Vadstein, O; Bones, AM
Antibacterial activities of selected seaweed and seagrass from port Dickson coastal water against different aquaculture pathogens

Natrah, FMI; Muta Harah, Z; Japar Sidik, B; Izzatul, NMS; Syahida, A
Checklist of the marine macroalgae of Vietnam

Nguyen, VT; Le, NH; Lin, SM; Steen, F; Clerck, O
Evolution and distribution of saxitoxin biosynthesis in dinoflagellates

Orr, RJS; Stüken, A; Murray, SA; Jakobsen, KS
Anti-microfouling properties of compounds isolated from several Mediterranean Dictyota spp

Othmani, A; Bouzidi, N; Viano, Y; Alliche, Z; Seridi, H; Blache, Y; Hattab, M; Briand, J-F; Culioli, G
Settlement inhibition of marine biofilm bacteria and barnacle larvae by compounds isolated from the Mediterranean brown alga Taonia atomaria

Othmani, A; Bunet, R; Bonnefont, J; Briand, JF; Culioli, G
A novel antifouling defense strategy from red seaweed: exocytosis and deposition of fatty acid derivatives at the cell wall surface

Paradas, WC; Tavares Salgado, L; Pereira, RC; Hellio, C; Atella, GC; Lima Moreira, D; Carmo, AP; Soares, AR; Menezes Amado-Filho, G
On the chemistry, toxicology and genetics of the cyanobacterial toxins, microcystin, nodularin, saxitoxin and cylindrospermopsin

Pearson, L; Mihali, T; Moffitt, M; Kellmann, R; Neilan, B
Bioprospecting for bioactives from seaweeds: potential, obstacles and alternatives

Pereira, RC; Costa-Lotufo, LV
Algal biorefineries Vol. 2: products and refinery design

Perez Garcia, O; Bashan, Y
Ecological role of a seaweed secondary metabolite for a colonizing bacterial community

Persson, F; Svensson, R; Nylund, GM; Fredriksson, NJ; Pavia, H; Hermansson, M
Checklist of microalgae collected from different habitats in peninsular Malaysia for selection of algal biofuel feedstocks

Phang, S-M; Mustafa, EM; Rao Ambati, R; Sulaiman, NMN; Lim, P-E; Majid, NA; Dommange, X; Schwob, C; Liew, K-E
Terpenes from the red alga Sphaerococcus coronopifolius inhibit the settlement of barnacles

Piazza, V; Roussis, V; Garaventa, F; Greco, G; Smyrniotopoulos, V; Vagias, C; Faimali, M
Antifouling activity as a function of population variation in Sargassum vulgare from the littoral of Rio de Janeiro

Plouguerné, E; Hellio, C; Cesconetto, C; Thabard, M; Mason, K; Véron, B; Pereira, RC; Gama, BA
Anti-microfouling activity of lipidic metabolites from the invasive brown alga Sargassum muticum (Yendo) fensholt

Plouguerné, E; Ioannou, E; Georgantea, P; Vagias, C; Roussis, V; Hellio, C; Kraffe, E; Stiger-Pouvreau, V
Within-thallus variation in polyphenolic content and antifouling activity in Sargassum vulgare

Plouguerné, E; Cesconetto, C; Cruz, CP; Pereira, RC; Gama, BAP
Allelopathic compounds of a red tide dinoflagellate have species-specific and context-dependent impacts on phytoplankton

Poulson, KL; Sieg, RD; Prince, EK; Kubanek, J
Are offshore phytoplankton susceptible to Karenia brevis allelopathy?

Poulson-Ellestad, K; McMillan, E; Montoya, JP; Kubanek, J
Characterization of allelopathic compounds from the red tide dinoflagellate Karenia brevis

Prince, EK; Poulson, KL; Myers, TL; Sieg, RD; Kubanek, J
Drugs from the sea - opportunities and obstacles

Proksch, P; Edrada-Ebel, RA; Ebel, R
Natural products as antifouling compounds: recent progress and future perspectives

Qian, P-Y; Xu, Y; Fusetani, N
Discovery of antimicrobial activities of a marine diatom Thalassiosira rotula

Qin, JG; D’Antignana, T; Zhang, W; Franco, C
The inhibitory effect of a non-yessotoxin-producing dinoflagellate, Lingulodinium polyedrum (stein) dodge, towards Vibrio vulnificus and Staphylococcus aureus

Quijano-Scheggia, S
Genetic engineering of algae for enhanced biofuel production

Radakovits, R; Jinkerson, RE; Darzins, A; Posewitz, MS
Studies on the anticorrosive and antifouling properties of the Gracilaria edulis extract incorporated epoxy paint in the Gulf of Mannar coast, Mandapam, India

Rajan, R; Meena, K; Ralraj, S; Subramanian, G
Bioinspiration: the solution for biofouling control?

Ralston, E; Swain, G
Effects of the red tide dinoflagellate, Karenia brevis, on early development of the eastern oyster Crassostrea virginica and northern quahog Mercenaria mercenaria

Rolton, A; Vignier, J; Soudant, P; Shumway, SE; Bricelj, VM; Volety, AK
Engineered cyanobacteria: teaching an old bug new tricks

Ruffing, AM
Spatial structure of an intertidal sandflat microphytobenthic community as related to different spatial scales

Saburova, MA; Polikarpov, IG; Burkovsky, IV
Surface-associated fucoxanthin mediates settlement of bacterial epiphytes on the rockweed Fucus vesiculosus

Saha, M; Rempt, M; Grosser, K; Pohnert, G; Weinberger, F
Dimethylsulphopropionate (DMSP) and proline from the surface of the brown alga Fucus vesiculosus inhibit bacterial attachment

Saha, M; Rempt, M; Gebser, B; Grueneberg, J; Pohnert, G; Weinberger, F
Defence chemistry modulation by light and temperature shifts and the resulting effects on associated epibacteria of Fucus vesiculosus

Saha, M; Rempt, M; Stratil, SB; Wahl, M; Pohnert, G; Weinberger, F
Growth and bioactive secondary metabolites of arctic Protoceratium reticulatum (Dinophyceae)

Sala-Pérez, M; Alpermann, TJ; Krock, B; Tillmann, U
Anti-biofilm performance of three natural products against initial bacterial attachment

Salta, M; Wharton, JA; Dennington, SP; Stoodley, P; Stokes, KR
Mini review: biomimetic models and bioinspired surfaces for fouling control

Scardino, AJ; Nys, R
The ecology of rocky coasts

Seed, R
Global priorities for marine biodiversity conservation

Selig, ER; Turner, WR; Troëng, S; Wallace, BP; Halpern, BS; Kaschner, K; Lascelles, BG; Carpenter, KE; Mittermeier, RA
Comparative analysis of single-species and polybacterial wound biofilms using a quantitative, in vivo, rabbit ear model

Seth, AK; Geringer, MR; Hong, SJ; Leung, KP; Galiano, RD; Mustoe, TA
Fouling coverage of a green tide alga, Ulva pertusa on some antifouling test surfaces exposed to Ayagin harbor waters, east coast of South Korea

Sidharthan, M; Shin, HW; Joo, JH
Comparative efficiency of macroalgal extracts and booster biocides as antifouling agents to control growth of the diatom species

Silkina, A; Bazes, A; Mouget, L; Bourgaugnon, N
Tropical Atlantic marine macroalgae with bioactivity against virulent and antibiotic resistant Vibrio

Silva, GC; Albuquerque-Costa, R; Oliveira-Peixoto, JR; Pessoa-Nascimento, FE; Macedo-Carneiro, PB; Silva dos Fernandes-Vieira, RH
Antimicrobial compounds from seaweeds-associated bacteria and fungi

Singh, R; Kumari, P; Reddy, C
The green alga Dicytosphaeria ocellata and its organic extracts alter natural bacterial biofilm communities

Sneed, JM; Pohnert, G
The green macroalga Dictyosphaeria ocellata influences the structure of the bacterioplankton community through differential effects on individual bacterial phylotypes

Sneed, JM; Pohnert, G
Checklist, distribution and potential utilization of marine algae of Myanmar I: Chlorophyta (green algae) and Phaeophyta (brown algae)

Soe-Htun, U; Wai, MK; Nyunt, T; Kyaw, SPP; Htay, YY; Aye, MM
Antimicrobial activity of seaweed extracts from Pattani, Southeast coast of Thailand

Srikong, W; Mittraparp-arthorn, P; Rattanaporn, O; Bovornreungroj, N; Bovornreungroj, P
Isolation and characterization of extracellular polysaccharides from the epipelic diatoms Cylindrotheca closterium and Navicula salinarum

Staats, N; Winder, B; Stal, LJ; Mur, LR
Silica biomineralisation in diatoms: the model organism Thalassiosira pseudonana

Sumper, M; Brunner, E
Green alga Ulva pertusa—a new source of bioactive compounds with antialgal activity

Sun, Y-Y; Wang, H; Guo, G-l; Pu, Y-F; Yan, B-L; Wang, C-H
Sargassum polyceratium (Phaeophyceae, Fucaceae) surface molecule activity towards fouling organisms and embryonic development of benthic species

Thabard, M; Gros, O; Hellio, C; Maréchal, JP
The role of nitric oxide in diatom adhesion in relation to substratum properties

Thompson, SEM; Taylor, AR; Brownlee, C; Callow, ME; Callow, JA
Impacts of pollution on marine life in Southeast Asia

Todd, PA; Ong, X; Chou, LM
Contraints to large scale algae biomass production and utilization

Ugoala, E; Ndukwe, GI; Mustapha, KB; Ayo, RI
Omaezallene from red alga Laurencia sp.: structure elucidation, total synthesis, and antifouling activity

Umezawa, T; Oguri, Y; Matsuura, H; Yamazaki, S; Suzuki, M; Yoshimura, E; Furuta, T; Nogata, Y; Serisawa, Y; Matsuyama-Serisawa, K; Abe, T; Matsuda, F; Suzuki, M; Okino, T
Antibacterial activity of halogenated sesquiterpenes from Malaysian Laurencia spp

Vairappan, CS; Suzuki, M; Ishii, T; Okino, T; Abe, T; Masuda, M
Effects of dopamine, a compound released by the green-tide macroalga Ulvaria obscura (Chlorophyta), on marine algae and invertebrate larvae and juveniles

Alstyne, KL; Harvey, EL; Cataldo, M
Daily bursts of biogenic cyanogen bromide (BrCN) control biofilm formation around a marine benthic diatom

Vanelslander, B; Paul, C; Grueneberg, J
A diatom gene regulating nitric-oxide signaling and susceptibility to diatom-derived aldehydes

Vardi, A; Bidle, KD; Kwityn, C; Hirsh, DJ; Thompson, SM; Callow, JA; Falkowski, P; Bowler, C
State of knowledge of coastal and marine biodiversity of Indian Ocean countries

Wafar, M; Venkataraman, K; Ingole, B; Ajmal Khan, S; LokaBharathi, P
Marine epibiosis. I. Fouling and antifouling: some basic aspects

Wahl, M
Ecological lever and interface ecology: epibiosis modulates the interactions between host and environment

Wahl, M
Ecology of antifouling resistance in the bladder wrack Fucus vesiculosus: patterns of microfouling and antimicrobial protection

Wahl, M; Shahnaz, L; Dobretsov, S; Saha, M; Symanowski, F; David, K; Lachnit, T; Vasel, M; Weinberger, F
The second skin: ecological role of epibiotic biofilms on marine organisms

Wahl, M; Goecke, F; Labes, A; Dobretsov, S; Weinberger, F
Polyphenolic substance of Mytilus edulis: novel adhesive containing L-Dopa and hydroxyproline

Waite, JH; Tanzer, ML
Biodiversity inventory and informatics in Southeast Asia

Webb, CO; Slik, JWF; Triono, T
Assessment of antiinflammatory effect of 5β-hydroxypalisadin B isolated from red seaweed Laurencia snackeyi in zebrafish embryo in vivo model

Wijesinghe, WA; Kim, EA; Kang, MC; Lee, WW; Lee, HS; Vairappan, CS; Jeon, YJ
Potential of sponges and microalgae for marine biotechnology

Wijffels, RH
Adhesion molecules from the diatom Phaeodactylum tricornutum (Bacillariophyceae): genomic identification by amino-acid profiling and in vivo analysis

Willis, A; Eason-Hubbard, M; Hodson, O; Maheswari, U; Bowler, C; Wetherbee, R
Extracellular matrix in diatoms (Bacillariophyceae). A model of adhesives based on chemical characterization and localization of polysaccharides from the marine diatom Achnanthes longipes and other diatoms

Wustman, BA; Gretz, MR; Hoagland, KD
Molecular interactions in cell adhesion complexes

Yamada, KM; Geiger, B
Linking adhesive and structural proteins in the attachment plaque of Mytilus californianus

Zhao, H; Waite, JH

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Minireview: algal natural compounds and extracts as antifoulants

Minireview: algal natural compounds and extracts as antifoulants

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Minireview: algal natural compounds and extracts as antifoulants

Minireview: algal natural compounds and extracts as antifoulants

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