TY - JOUR
AU - Rossetti, S
AB - Abstract Matrix-embedded, surface-attached microbial communities, known as biofilms, profusely colonise industrial cooling water systems, where the availability of nutrients and organic matter favours rapid microbial proliferation and their adhesion to surfaces in the evaporative fill material, heat exchangers, water reservoir and cooling water sections and pipelines. The extensive growth of biofilms can promote micro-biofouling and microbially induced corrosion (MIC) as well as pose health problems associated with the presence of pathogens like Legionella pneumophila. This review examines critically biofilm occurrence in cooling water systems and the main factors potentially affecting biofilm growth, biodiversity and structure. A broad evaluation of the most relevant biofilm monitoring and control strategies currently used or potentially useful in cooling water systems is also provided. biofilm, cooling water system, monitoring and control measures, biodiversity INTRODUCTION Cooling water systems are widely used to dissipate the heat generated by process operations in many industries including refineries, steel mills, food, petrochemical, chemical and power plants (Venugopalan, Rajagopal and Jenner 2012). Efficient heat removal requires the optimal circulation of cooling water, which is often compromised by microbial overgrowth (Rao 2012; Venugopalau et al. 2012). These cooling systems provide an excellent environment for planktonic and benthonic growth, supported by temperatures ranging between 25°C and 35°C, a pH close to neutrality, sunlight exposure and continuous aeration (Liu et al. 2009). Microbes enter cooling systems from the atmosphere and the water source (make up water), which is mainly seawater, freshwater and groundwater. Here, the presence of nutrients and organic matter, concentrated by evaporation, together with anti-scalants and corrosion inhibitors, normally used in the treatment of cooling waters, favour rapid microbial proliferation. The availability of surfaces in the evaporative fill material, heat exchangers, water reservoir and cooling water pipelines contributes to the extensive growth of biofilms (Liu et al. 2011; Rao 2012). Biofilms are complex surface-attached microbial communities whose cells are embedded in a self-produced matrix of extracellular polymeric substances (EPS) responsible for the integrity of their three-dimensional structure (Flemming and Wingender 2010). The biofilm matrix is arranged in a gel-like structure (Mayer et al. 1999; Sutherland 2001), consisting of a network of polymeric chains stabilised by intra- and intermolecular linkages, generating a high water retaining capability (Decho 2016). This polymeric material can have a heterogeneous composition and includes a wide range of biopolymers of differing chemical and physical properties (Flemming et al. 2016). These are mainly polysaccharides, proteins, amyloids, extracellular nucleic acids and amphiphilic compounds such as glycolipids and peptidolipids (Neu and Laurence 2016; Sutherland 2016). The polymeric matrix encloses and binds together the microbes in the biofilm, thus providing considerable mechanical stability (Mayer et al. 1999; Sutherland 2016), recognised as one of the major advantages of the biofilm mode of life (Flemming, Neu and Wozniak 2007; Flemming 2016). The sorption properties of the matrix facilitates the exchange of nutrients, gases and other molecules with the environment (Flemming and Wingender 2010). Biofilms are the prevailing mode of microbial life in most natural and manmade environments including industrial cooling water systems, where they can promote micro-biofouling and thus interfere with operational requirements (Fig. 1). Biofilms reduce conductive heat transfer across surfaces and may clog hydraulic systems with consequent energy losses and possible production cutbacks and shutdowns (Rao et al. 2012; Venugopalau et al. 2012). Furthermore, microbes occupying niches in the deeper layers of biofilm communities can promote microbially induced corrosion (MIC) (Fig. 1) that increases the corrosion rate of the metal/alloy by altering its surface electrochemical properties (Cloete and Flemming 2012). Besides high economic loss, biofilm formation may also pose serious health problems associated with the presence there of pathogens including thermotolerant Legionella species and free-living protozoa and may enable their widespread survival and propagation (Brouse, Brouse and Brouse 2017) over long distances by the aerosol dispersal in air conditioner cooling systems. Figure 1. View largeDownload slide Examples of biofouling (A and B), https://www.drydenaqua.com/water-treatment; http://amsainc.com/cooling-tower-maintenance/) and MIC (C and D) in cooling water industrial systems Figure 1. View largeDownload slide Examples of biofouling (A and B), https://www.drydenaqua.com/water-treatment; http://amsainc.com/cooling-tower-maintenance/) and MIC (C and D) in cooling water industrial systems Therefore, biofilm monitoring and control are essential to ensure optimal cooling water system reliability and efficiency. Practical experience has led to the development of strategies principally based on the addition of chemical additives to the water, including corrosion inhibitors, dispersants, scale inhibitors and biocides (Cloete, Jacobs and Brozel 1998). However, antimicrobial compounds may not be fully effective in their removal resulting from the protection provided by the biofilm matrix (Stewart 2002; Hall-Stoodley, Costerton and Stoodley 2004; Fux et al. 2005). High concentrations of biocide, mainly chlorine, are therefore used currently to control microbiofouling, despite increased levels of environmental awareness and additional pressure from tighter legislation that suggest that alternative control strategies should be explored (Bognolo, John and Evans 1992; Turnpenny et al. 2012). Interest in this topic is high because of the serious problems that biofilms may cause in industrial settings worldwide. Despite the considerable information now available on the diversity, structure and ecology of biofilms in many natural habitats (Stal 2010; Peter et al. 2011; Besemer et al. 2012; Battin et al. 2016; Proia, Romaní and Sabater 2017) and mechanisms involved in biofilm formation in medical fields (Donlan and Costerton 2002; Costerton, Montanaro and Arciola 2005; Fux et al. 2005; Landini et al. 2010; Archer et al. 2011), an integrated approach as to how future investigations should be conducted in cooling systems is still missing. This review aims to analyse critically the available literature on biofilm occurrence in such systems to pinpoint crucial aspects that deserve further investigations, in the hope that the biofouling process in industrial water systems will be better understood. This review updates what is known already about the factors affecting biofilm development and biodiversity, the mechanisms involved in biofilm formation, highlighting the complexity of genetic and environmental features involved. The review also describes the relevant monitoring systems currently used in cooling water systems and provides an overview of novel monitoring approaches with potential use in industrial plants. Finally, the review discusses the most common practices in use to control biofilm development and evaluates several novel approaches now being applied. OCCURRENCE OF BIOFILMS IN COOLING WATER INDUSTRIAL SYSTEMS Biofilm diversity and structure in cooling water industrial systems Complex, multi-species biofilm communities colonise extensively the available surfaces of most cooling water industrial systems. Although they may cause serious operational issues, little information is available on their microbial community composition and structure (Hauer 2010; Balamurugan, Hiren Joshi and Rao 2011; Wang et al. 2013; Hauer, Čapek and Böhmová 2016; Di Gregorio et al. 2017; Pereira et al. 2017). Such scarcity of information is attributable largely to the difficulties in collecting samples arising from the limited accessibility to the towers and to authorisation constraints. Analysis of the available literature reveals that Proteobacteria, particularly members of the Alpha and Beta subgroups, Cyanobacteria and Acidobacteria dominate climax communities of these biofilms (Wang et al. 2013; Di Gregorio et al. 2017) (Table 1). Thus, populations, mainly affiliated to Rhodobacteriaceae and Sphingomonadaceae, dominated communities grown in ‘enclosed’ counter-flow cooling towers located in China (Wang et al. 2013) and in Italy (Di Gregorio et al. 2017). On the other hand, biofilms grown in two cross-flow cooling towers ‘open’ to the atmosphere and hence light, located in Eastern Europe, were dominated by Cyanobacteria together with Alpha- and Beta-Proteobacteria. The Cyanobacteria (mainly Calothrix, Leptolyngbya, Microcoleus and Phormidium) coexisted with photosynthetic eukaryotes as diatoms, principally Achanthes, Diadesmis and Gomphonema species, and green algae, mainly Cladophora and Stigeoclonium spp. (Di Gregorio et al. 2017). Similar communities were reported in 18 ‘open’ natural, draft cooling towers at nine sites in different geographic areas of the Czech Republic (Hauer 2010; Hauer, Čapek and Böhmová 2016), suggesting that biofilm community composition was influenced markedly by their exposure to light. Hauer, Capek and Bohmova (2016) also showed that the phototrophic population compositions changed following establishment of a light gradient from the periphery to the centre of the studied ‘open’ cooling towers. Sulphate-reducing bacteria, mainly Delta-Proteobacteria, were also detected in biofilms colonising carbon steel pipelines of the water cooling system of a nuclear test reactor (Balamurugan, Hiren Joshi and Rao 2011), as well as in communities on galvanised steel surfaces of an open, recirculating cooling tower of a hotel plant in Istanbul, Turkey (Minnos et al. 2013). This information, albeit scant, would seem to suggest that biofilm communities developed in the screened cooling systems are affected markedly by existing environmental physical factors (i.e. irradiance), cooling tower design and their construction material. Table 1. List of the main species found in biofilms occurring in different cooling water systems (Hauer 2010; Wang et al. 2013; Hauer, Čapek and Böhmová 2016; Di Gregorio et al. 2017; Kadaifciler and Demirel 2017). Bacteria  Eukarya  Alphaproteobacteria  Cyanobacteria  Gammaproteobacteria  Diatoms  Aliihoefleasp.  Aphanothece spp.  Acinetobactersp.  Achnanhes sp.  Bosea sp.  Brasilonema sp.  Erwiniasp.  Amphora sp.  Brevundimonassp.  Calothrix sp.  Pseudoxanthomonassp.  Cymbella sp.  Devosiasp.  Chroococcidiopsistermalis  Rhizobactersp.  Diadesmis sp.  Erythrobactersp.  Chroococcus spp.     Gomphonema sp.  Hyphomicrobiumsp.  Cyanobium sp.  Firmicutes  Navicula sp.  Methylobacteriumsp.  Cyanothece sp.  Clostridium sp.  Nitzschia sp.  Paracoccussp.  Cyanosarcina sp.  Exiguobacterium sp.  Pinnularia sp.  Porphyrobactersp.  Geitlerinema sp.     Surirella sp.  Sphingomonassp.  Gloeocapsa spp.  Actinobacteria  Green algae  Sphingopyxissp.  Gloeocapsopsis sp.  Microbacteriumsp.  Cladophora sp.  Paracoccussp.  Gloeothece palea  Microcella sp.  Chlorella sp.  Parvularculasp.  Hassallia sp.  Serinicoccussp.  Cosmarium sp.  Rhodobactersp.  Leptolyngbya spp.     Gloeocystis sp.  Roseococcussp.  Merismopedia sp.  Planctomycetes  Monodopsis sp.  Rubellimicrobiumsp.  Microcoleus sp.  Planctomycetes  Pseudococcomyxa simplex     Nodularia sp.     Scenedesmus sp.     Nostoccf.microscopicum  Acidobacteria  Stigeoclonium sp.  Betaproteobacteria  Phormidium spp.  Acidobacterium sp.  Ulothrix variabilis  Cupriavidussp.  Pleurocapsa sp.     Vischeria sp.  Delftiasp.  Pseudanabaenacf.minima  Bacteroidetes  Fungi  Hydrogenophagasp.  Scytonema sp.  Arenibactersp.  Aspergillus versicolor  Massiliasp.  Symploca muralis  Flavobacteriumsp.  Aspergillus niger  Rubrivivaxsp.  Tolypothrix sp.  Flexibactersp.  Penicillium dipodomyicola.  Bacteria  Eukarya  Alphaproteobacteria  Cyanobacteria  Gammaproteobacteria  Diatoms  Aliihoefleasp.  Aphanothece spp.  Acinetobactersp.  Achnanhes sp.  Bosea sp.  Brasilonema sp.  Erwiniasp.  Amphora sp.  Brevundimonassp.  Calothrix sp.  Pseudoxanthomonassp.  Cymbella sp.  Devosiasp.  Chroococcidiopsistermalis  Rhizobactersp.  Diadesmis sp.  Erythrobactersp.  Chroococcus spp.     Gomphonema sp.  Hyphomicrobiumsp.  Cyanobium sp.  Firmicutes  Navicula sp.  Methylobacteriumsp.  Cyanothece sp.  Clostridium sp.  Nitzschia sp.  Paracoccussp.  Cyanosarcina sp.  Exiguobacterium sp.  Pinnularia sp.  Porphyrobactersp.  Geitlerinema sp.     Surirella sp.  Sphingomonassp.  Gloeocapsa spp.  Actinobacteria  Green algae  Sphingopyxissp.  Gloeocapsopsis sp.  Microbacteriumsp.  Cladophora sp.  Paracoccussp.  Gloeothece palea  Microcella sp.  Chlorella sp.  Parvularculasp.  Hassallia sp.  Serinicoccussp.  Cosmarium sp.  Rhodobactersp.  Leptolyngbya spp.     Gloeocystis sp.  Roseococcussp.  Merismopedia sp.  Planctomycetes  Monodopsis sp.  Rubellimicrobiumsp.  Microcoleus sp.  Planctomycetes  Pseudococcomyxa simplex     Nodularia sp.     Scenedesmus sp.     Nostoccf.microscopicum  Acidobacteria  Stigeoclonium sp.  Betaproteobacteria  Phormidium spp.  Acidobacterium sp.  Ulothrix variabilis  Cupriavidussp.  Pleurocapsa sp.     Vischeria sp.  Delftiasp.  Pseudanabaenacf.minima  Bacteroidetes  Fungi  Hydrogenophagasp.  Scytonema sp.  Arenibactersp.  Aspergillus versicolor  Massiliasp.  Symploca muralis  Flavobacteriumsp.  Aspergillus niger  Rubrivivaxsp.  Tolypothrix sp.  Flexibactersp.  Penicillium dipodomyicola.  View Large Table 1. List of the main species found in biofilms occurring in different cooling water systems (Hauer 2010; Wang et al. 2013; Hauer, Čapek and Böhmová 2016; Di Gregorio et al. 2017; Kadaifciler and Demirel 2017). Bacteria  Eukarya  Alphaproteobacteria  Cyanobacteria  Gammaproteobacteria  Diatoms  Aliihoefleasp.  Aphanothece spp.  Acinetobactersp.  Achnanhes sp.  Bosea sp.  Brasilonema sp.  Erwiniasp.  Amphora sp.  Brevundimonassp.  Calothrix sp.  Pseudoxanthomonassp.  Cymbella sp.  Devosiasp.  Chroococcidiopsistermalis  Rhizobactersp.  Diadesmis sp.  Erythrobactersp.  Chroococcus spp.     Gomphonema sp.  Hyphomicrobiumsp.  Cyanobium sp.  Firmicutes  Navicula sp.  Methylobacteriumsp.  Cyanothece sp.  Clostridium sp.  Nitzschia sp.  Paracoccussp.  Cyanosarcina sp.  Exiguobacterium sp.  Pinnularia sp.  Porphyrobactersp.  Geitlerinema sp.     Surirella sp.  Sphingomonassp.  Gloeocapsa spp.  Actinobacteria  Green algae  Sphingopyxissp.  Gloeocapsopsis sp.  Microbacteriumsp.  Cladophora sp.  Paracoccussp.  Gloeothece palea  Microcella sp.  Chlorella sp.  Parvularculasp.  Hassallia sp.  Serinicoccussp.  Cosmarium sp.  Rhodobactersp.  Leptolyngbya spp.     Gloeocystis sp.  Roseococcussp.  Merismopedia sp.  Planctomycetes  Monodopsis sp.  Rubellimicrobiumsp.  Microcoleus sp.  Planctomycetes  Pseudococcomyxa simplex     Nodularia sp.     Scenedesmus sp.     Nostoccf.microscopicum  Acidobacteria  Stigeoclonium sp.  Betaproteobacteria  Phormidium spp.  Acidobacterium sp.  Ulothrix variabilis  Cupriavidussp.  Pleurocapsa sp.     Vischeria sp.  Delftiasp.  Pseudanabaenacf.minima  Bacteroidetes  Fungi  Hydrogenophagasp.  Scytonema sp.  Arenibactersp.  Aspergillus versicolor  Massiliasp.  Symploca muralis  Flavobacteriumsp.  Aspergillus niger  Rubrivivaxsp.  Tolypothrix sp.  Flexibactersp.  Penicillium dipodomyicola.  Bacteria  Eukarya  Alphaproteobacteria  Cyanobacteria  Gammaproteobacteria  Diatoms  Aliihoefleasp.  Aphanothece spp.  Acinetobactersp.  Achnanhes sp.  Bosea sp.  Brasilonema sp.  Erwiniasp.  Amphora sp.  Brevundimonassp.  Calothrix sp.  Pseudoxanthomonassp.  Cymbella sp.  Devosiasp.  Chroococcidiopsistermalis  Rhizobactersp.  Diadesmis sp.  Erythrobactersp.  Chroococcus spp.     Gomphonema sp.  Hyphomicrobiumsp.  Cyanobium sp.  Firmicutes  Navicula sp.  Methylobacteriumsp.  Cyanothece sp.  Clostridium sp.  Nitzschia sp.  Paracoccussp.  Cyanosarcina sp.  Exiguobacterium sp.  Pinnularia sp.  Porphyrobactersp.  Geitlerinema sp.     Surirella sp.  Sphingomonassp.  Gloeocapsa spp.  Actinobacteria  Green algae  Sphingopyxissp.  Gloeocapsopsis sp.  Microbacteriumsp.  Cladophora sp.  Paracoccussp.  Gloeothece palea  Microcella sp.  Chlorella sp.  Parvularculasp.  Hassallia sp.  Serinicoccussp.  Cosmarium sp.  Rhodobactersp.  Leptolyngbya spp.     Gloeocystis sp.  Roseococcussp.  Merismopedia sp.  Planctomycetes  Monodopsis sp.  Rubellimicrobiumsp.  Microcoleus sp.  Planctomycetes  Pseudococcomyxa simplex     Nodularia sp.     Scenedesmus sp.     Nostoccf.microscopicum  Acidobacteria  Stigeoclonium sp.  Betaproteobacteria  Phormidium spp.  Acidobacterium sp.  Ulothrix variabilis  Cupriavidussp.  Pleurocapsa sp.     Vischeria sp.  Delftiasp.  Pseudanabaenacf.minima  Bacteroidetes  Fungi  Hydrogenophagasp.  Scytonema sp.  Arenibactersp.  Aspergillus versicolor  Massiliasp.  Symploca muralis  Flavobacteriumsp.  Aspergillus niger  Rubrivivaxsp.  Tolypothrix sp.  Flexibactersp.  Penicillium dipodomyicola.  View Large Several methodologies developed, or adapted for multispecies biofilm studies, are now available (see the review Azeredo et al. 2017), and these will provide data that contribute to a deeper understanding of biofilm structure and composition. For example, improved microscope imaging technology, biochemical methods and biomolecular tools now offer the possibility of resolving at nano-scale level an overall view of the three-dimensional biofilm structure (Neu and Lawrence, 2015, 2016) and provide a deeper understanding of the physiology of biofilm cells and their genotypic and phenotypic variation (Raes and Bork 2008). Only a few of these techniques have been applied to study biofilms in cooling towers. High-throughput next-generation DNA sequencing protocols have exposed the full breadth and complexity of their community biodiversities in these systems, revealing the presence of an elevated number of taxa, where a few species dominate and rare taxa form a long tail (Di Gregorio et al. 2017). In addition, the three-dimensional reconstruction of biofilms from two ‘open’ cooling towers, obtained with Confocal Laser Scanning Microscopy (CLSM) after Catalyzed Reporter Deposition Fluorescence in situ Hybridisation (CARD-FISH) (Figs 2, 3 and 4) show them to be highly complex and multi-stratified communities, where bacterial micro-colonies, closely associated with other prokaryotic and/or eukaryotic photosynthetic microbes, have a patchy distribution and appear to be embedded in matrix material mainly composed of proteins and α- and β-glucans (Di Gregorio et al. 2017). Figure 2. View largeDownload slide CLSM 3D reconstructions of winter biofilm samples from a cooling tower located in Eastern Europe. Structural complexity, biofilm thickness and diversity are evident after CARD-FISH, DAPI staining and photosynthetic pigment excitation. Multichannel mode acquisition of a biofilm fragment signals. Biofilm bacteria targeted by EUB338mix probe (green signal, (A) appear enmeshed with clusters of green algae cells (red signal of chlorophyll a autofluorescence, (B) and total biofilm members are visible after DAPI staining in blue (C) while spatial relationships between all biofilm components are clearly evidenced in the merged image (D). Figure 2. View largeDownload slide CLSM 3D reconstructions of winter biofilm samples from a cooling tower located in Eastern Europe. Structural complexity, biofilm thickness and diversity are evident after CARD-FISH, DAPI staining and photosynthetic pigment excitation. Multichannel mode acquisition of a biofilm fragment signals. Biofilm bacteria targeted by EUB338mix probe (green signal, (A) appear enmeshed with clusters of green algae cells (red signal of chlorophyll a autofluorescence, (B) and total biofilm members are visible after DAPI staining in blue (C) while spatial relationships between all biofilm components are clearly evidenced in the merged image (D). Figure 3. View largeDownload slide 3D renderings of four different biofilm fragments: in (A) dominance of Bacteria over photosythetic microorganisms (chlorophyll a signal in red) is evidenced here after hybridisation with EUB338mix probes and DAPI staining (green and blue signals, respectively); (B) large filamentous green algae in red (chlorophyll a autofluorescence); (C) photosynthetic biofilm members are discriminated by excitation of chlorophyll a (grey signal) and phycobiliprotein (red) autofluorescence along with total bacteria after hybridisation with EUB338mix probe. Diatoms, large desmids and filamentous green algae (grey) appeared scattered among cyanobacterial unicells of different size (red) and bacteria (green signal). All community members were homogeneously distributed through biofilm thickness as shown in the profiles; in (D) a wide and diffuse blue signal, after DAPI staining, is particularly evident indicating high amounts of compact, matrix material enmeshing bacteria (in red) and phototrophs Figure 3. View largeDownload slide 3D renderings of four different biofilm fragments: in (A) dominance of Bacteria over photosythetic microorganisms (chlorophyll a signal in red) is evidenced here after hybridisation with EUB338mix probes and DAPI staining (green and blue signals, respectively); (B) large filamentous green algae in red (chlorophyll a autofluorescence); (C) photosynthetic biofilm members are discriminated by excitation of chlorophyll a (grey signal) and phycobiliprotein (red) autofluorescence along with total bacteria after hybridisation with EUB338mix probe. Diatoms, large desmids and filamentous green algae (grey) appeared scattered among cyanobacterial unicells of different size (red) and bacteria (green signal). All community members were homogeneously distributed through biofilm thickness as shown in the profiles; in (D) a wide and diffuse blue signal, after DAPI staining, is particularly evident indicating high amounts of compact, matrix material enmeshing bacteria (in red) and phototrophs Figure 4. View largeDownload slide 3D reconstructions after excitation of photosynthetic pigments, clorophyll a in red and phycobiliproteins in green, showing the variability in taxonomy, size and morphology of biofilm photototrophs. Figure 4. View largeDownload slide 3D reconstructions after excitation of photosynthetic pigments, clorophyll a in red and phycobiliproteins in green, showing the variability in taxonomy, size and morphology of biofilm photototrophs. The few available studies have also suggested that the communities of biofilms growing in cooling systems are substantially different from the corresponding planktonic communities, sharing only a few taxa (Wang et al. 2013; Di Gregorio et al. 2017). Thus, it appears that only certain members of the suspended communities can adhere to the surfaces available in these cooling systems. It seems likely that existing operating factors like constant high temperatures and pH, together with the presence of biocides, would determine which populations in the source water can participate in the initial colonisation of such habitats. Of these, pioneer biofilm microbes (e.g. Sphingopyxis, see Di Gregorio et al. 2017, Acidovorax, see Wang et al. 2013) are possible candidates, able to attach to the appropriate substrata and initiate biofilm formation, thus modifying the surfaces and allowing further colonisation by other populations. Subsequent biofilm development to a mature/climax community, characterised by high species diversity composition, then occurs together with the characteristic structural arrangement of biofilms. Biofilm formation mechanisms and their molecular basis Although biofilm formation has been studied extensively with cultured mono-specific communities, little is known about the molecular mechanisms involved in the regulation of mixed-species biofilm adhesion and development in either natural or man-made environments, because of the complexities of such dynamic communities. It is well known that biofilm formation is a complex process that includes several stages. These are (i) attachment of individual cells to surfaces, (ii) reversible, followed by irreversible, binding of these to the surface (iii) development of microcolonies and (iv) maturation of biofilm architecture (Donlan 2001). A large body of literature emphasises that biofilm formation and dispersal are highly controlled processes regulated at the genetic level, and by a range of environmental cues and signals (Burmølle et al. 2014; Wolska et al. 2016). These include changes in nutrient concentrations, oxygen levels and temperature, as well as organic carbon source and predatory stresses (Bassler et al. 1993; Matz and Kjielleberg 2005; McDougald et al. 2011; Mitri, Xavier and Foster 2011). Genetic and molecular approaches have identified genes and regulatory circuits important for initial cell–surface interactions and subsequent biofilm maturation, and also the return of biofilm microbes to a planktonic mode of growth (Davey and O'Toole 2000; Wolska et al. 2016). Current knowledge points to bis-(3΄-5΄)- cyclic diguanosine monophosphate (c-di-GMP) and quorum sensing (QS) as the main regulators of bacterial biofilms (Boyd and O'Toole 2012; Fazli et al. 2014; Liang 2015). The crucial phase in the formation of bacterial biofilms is the transition from a motile to a sessile cell lifestyle (Jenal, Reinders and Lori 2017), mediated by the intracellular secondary messenger c-di-GMP, mainly in response to environmental stresses (Jenal, Reinders and Lori 2017). Generally, high c-di-GMP levels induce the biosynthesis of adhesins and matrix polysaccharides, and inhibit cell motility therefore initiating biofilm formation. With low c-di-GMP levels, the synthesis of adhesins and exopolysaccharide material is downregulated, and bacterial motility enhanced, leading to biofilm dispersal. These processes have been discussed in more detail by Hengge (2009), Liang (2015) and Jenal, Reinders and Lori (2017). Two classes of enzymes control the level of c-di-GMP in bacteria. Diguanylate cyclases, which contain the typical domain, CGDEF, produce this nucleotide from two molecules of GTP, whereas c-di-GMP is broken down into 5΄-phosphoguanylyl-(3΄-5΄) guanosine (pGpG) by specific photodiesterases (PDEs), whose activities are associated with EAL or HD-GYP specific domains (Liang 2015). Given the role played by c-di-GMP in integrating environmental inputs and controlling the motile–sessile transition in both directions, it seems highly likely that c-di-GMP signalling is important in these mixed-species biofilms colonising cooling water systems. Several methods have been developed to quantify c-di-GMP levels (Schleheck et al. 2009; Rybtke et al. 2012), and these can be used to follow changes in biofilm c-di-GMP levels. Studies with a range of single-species biofilms have established the importance of intra- and interspecies cell-to-cell communication systems, QS, in controlling biofilm development (see the reviews Papenfort and Bassler 2016; Wolska et al. 2016; Whiteley, Diggle and Greenberg 2017). QS relies on the production, secretion, accumulation and population-wide detection of signal molecules, called autoinducers. When a sufficient number of bacteria is present and autoinducer concentrations reach a threshold level, the bacteria start to sense their critical mass and respond by repressing or activating target genes (Burmølle et al. 2014; Papenfort and Bassler 2016; Wolska et al. 2016). Although these systems seem to play no clear role in cell attachment and initial biofilm developmental stages, they are essential for further biofilm development and also regulate biofilm cell dispersal (Wolska et al. 2016). In general, the N-acyl homoserine lactone (AHL)-based systems impact biofilms composed of Gram-negative species including the model P. aeruginosa biofilm system (de Kievit 2009; Papenfort and Bassler 2016), while peptide-based QS systems regulate biofilm formation in Staphylococcus aureus and other Gram-positive populations (Parsek and Greenberg 2005; Suntharalingam and Cvitkovitch 2005; Novick and Gelsinger 2008). Quorum sensing research has led to important advances in the understanding of the genetics, genomics, biochemistry and signal diversity of QS (Whiteley, Diggle and Greenberg 2017), but under laboratory cultures and with growth conditions very different to those found in the natural environment. Despite this, in vitro systems have provided fundamental knowledge of the role of QS molecules in modulating the composition and function of natural multispecies biofilms, where their levels play a similar role in formation of microbial complex natural communities seen in stromatolites and microbial mats. Here, AHL levels vary with the diurnal cycle driven by pH changes as a reflection of community metabolism and photosynthesis activity (Decho et al. 2009). The role of AHL-mediated QS in the formation and assembly of microbial granules has been demonstrated in membrane bioreactors (Yeon et al. 2009) and sequencing batch reactors (Tan et al. 2014; Tan et al. 2015). Despite these findings, it is still unclear how such interactions can be achieved and coordinated among phylogenetically very different populations in complex biofilm communities. Working in natural microbial habitats is challenging and requires integration of a comprehensive understanding of QS action derived from laboratory studies together with relevant ecological principles before the role of intercellular communication in natural mixed multispecies biofilms can be clarified. Factors affecting the development of biofilm communities in cooling water systems would not be dissimilar to those experienced by mixed species biofilms in other natural and bioprocess systems. It is therefore likely that QS signalling has an equally important role in biofilm formation in cooling water industrial systems, in mediating cooperative microbial community behaviour. In perspective, the analysis of QS molecules and c-di GMP on biofilm communities grown on purpose artificial removable substrata placed in cooling systems would enable their role to be better understood and may allow the definition of appropriate specific control actions. Health related issues: occurrence of biofilm-associated Legionella pneumophila in cooling water systems Biofilm formation in cooling water systems poses a public health risk associated with the presence there of pathogens. Biofilms can favour the presence, survival and proliferation of thermotolerant pathogenic bacteria, especially Legionella pneumophila, held responsible for about 90% of worldwide cases of Legionnaires' disease (Wéry et al. 2008; Walser et al. 2014; Pereira et al. 2017). This is a severe pneumonia like illness with a case fatality rate of 10%–15% (Walser et al. 2014). As cooling towers are the major sources (Walser et al. 2014; Pereira et al. 2017), surveillance of Legionella in such systems is highly relevant to human health. Public health authorities like the European Working Group for Legionella Infections (EWGLI) and World Health Organization (WHO) have published guidelines aimed at preventing and controlling the risk of Legionella proliferation in cooling towers (Mouchotouri et al. 2010). However, the current approach to monitor and control its presence remains haphazard, with inconsistent approaches to disinfection and unsatisfactory endpoints to evaluate success of control countermeasures (Yu 2008). Monitoring is usually based on colony plate counts of Legionella (Walser et al. 2014), and biocide dosages, mainly chlorine and/or glutaraldehyde, are applied subsequently to control it. The problems of relying on plate counts to quantify this pathogen in cooling towers has been discussed (Yu 2008). Consequently, alternative approaches have been suggested (Collins et al. 2017; Gong et al. 2017). Quantitative real-time polymerase chain assays (qPCR) are a widely accepted alternative to detect Legionella in environmental samples (Yang et al. 2010; Kao et al. 2013; Collins et al. 2017), and its use in cooling water has been recommended as a valuable tool for timely facilitating control and public health protection (Collins et al. 2017). A combination of mip (Molecular Inversion Probe), SBT (Sequence-Based Typing) and FAFLP (Fluorescence Amplified Fragment Length Polymorphism) methods have also been proposed (Gong et al. 2017). Long-term studies conducted on the bulk water of cooling towers (Wery et al. 2008; Pereira et al. 2017) have demonstrated that the structure and species richness of microbial communities associated with Legionella species can be affected in these systems by environmental and/or operational conditions (Wery et al. 2008; Pereira et al. 2017). The distinct temporal changes of the microbial communities and the substantial variation in the abundance of L. pneumophila highlight the need for continuous monitoring of the cooling towers to prevent outbreaks of Legionellosis. However, because of its ecology, reducing the risk related to Legionella remains a challenge. Its ability to exist in biofilms in association with protozoa complicate its monitoring and control. Although the literature, reviewed by Declerck (2010), has focused on the survival and replication of L. pneumophila in cultured biofilms, little is known so far about the mechanisms and factors affecting its life cycle in multispecies biofilms colonising anthropogenic systems like cooling towers. Many questions remain to be answered, because of the lack of reliable data from studies using pilot-scale or on-site experiments and naturally occurring biofilm communities. The main challenge should be to elucidate whether Legionella can survive and replicate outside a protozoan host in environmental biofilms. It is already known that Legionella spp. have evolved a capability to replicate intracellularly in 14 species of biofilm-associated free-living amoebae (Molmeret et al. 2005; Declarck 2010). On the other hand, evidence exists of adhesion of L. pneumophila in pre-established biofilms as a secondary coloniser (Declerck 2010). Data from some studies have demonstrated that Legionella is able to replicate and thrive in the biofilm matrix (Vervaeren et al. 2006; Dechlerck et al. 2009), because it has the capacity to obtain nutrients either directly from other living microbes, like algae and heterotrophic bacteria, and/or indirectly from decaying organic matter (Declerck 2010). Under laboratory conditions, L. pneumophila showed it could grow on extracellular exudates from the cyanobacterium Fisherella sp. (Tison et al. 1980) and the green algae Scenedesmus spp. and Chlorella spp. (Hume and Hann 1984). Necrotrophic growth of L. pneumophila has also been shown (Temmerman et al. 2006). It is clearly important to understand the mechanisms regulating interactions between L. pneumophila and populations in pre-established biofilms. The discovery of intracellular signalling molecules Legionella autoinducer-1 (LAI-1) (Spirig et al. 2008) and AHKs (Abdel-Nour et al. 2013) suggests some involvement of QS mechanisms in interactions between L. pneumophila and biofilm primary colonising populations. BIOFILM MONITORING IN COOLING WATER SYSTEMS The operational and environmental issues related to biofilm development in these systems tend to be addressed separately though it is desirable to adopt more innovative and holistic approaches, taking account of all fouling factors with the primary aim of preventing and/or reducing cell adhesion and biofilm formation in addition to minimising their impact on the recipient water bodies, where cooling water is discharged via blow-down (Venugopalau et al. 2012). Traditional methods of monitoring cooling water systems Microbial monitoring is an integral part of any cooling water treatment program, and it is essential to determine the effectiveness of any antifouling and/or anti-MIC treatments, and to establish the most cost effective level of treatment in terms of energy, water and chemical usage. Conventionally, biofouling and MIC are monitored and diagnosed indirectly, by determining the number of free-living bacteria in bulk water samples by plate-count methods (Flemming 2011). However, attached bacterial numbers can exceed planktonic numbers by three to four logarithm units in water systems (Cloete, Jacobs and Brozel 1998). Moreover, free-living cell number determinations do not provide reliable or robust information about the biofilm site or the extent and the composition of biofilms in cooling system. Although biofilms and planktonic communities from dispersed biofilms may share populations (Di Gregorio et al. 2017), such samples taken from the same systems are notably different (Wang et al. 2013; Di Gregorio et al. 2017). Thus, biofilm surface sampling is mandatory for proper monitoring of biofouling in such systems (Cloete, Jacobs and Brozel 1998; Schaule, Griebe and Flemming 2000; Flemming 2002). Sampling approaches utilised in cooling water systems, consist either of biofilm scraping from defined, representative surface areas or test substrata known as ‘coupons’, located in situ. Coupons have been used to monitor MIC values (Videla and Herrera 2005) by evaluating the surface corrosion rate and by enumerating the sessile bacteria. Viable cell counts (‘colony-forming units,’ cfu) are used to quantify microbes on the substrata, but with the drawback of estimating only a fraction of the biofilm community, as the percentage of cultivable organisms there is usually less than 1% of the total number (Rompre´ et al. 2002). A modified Robbins device (Ruseska et al. 1982) can be used. It tests surfaces exposed to the flowing bulk fluid, for given periods and data analysed in the laboratory. Its main disadvantage is the lag between the time-consuming investigations and availability of theresults. Online methods to detect biofilms in cooling water systems From the discussion above, it appears clear that, to obtain more accurate data faster, non-destructive monitoring providing online and real time information are necessary for implementing preventative measures against micro-biofouling and MIC. Many online methods have been described, some of which have been applied successfully, mainly for detecting the kinetics of material deposition and changes of biofilm layer thickness. These have been reviewed (Flemming 2011) and include methods based on measurements of thermal or mechanical variations induced by fouling (Fillaudeau 2003; Pavanello et al. 2011), or with DTM (differential turbidity measurement) devices (Klahre and Flemming 2000), rotoscope device, detecting changes in light absorption in response to deposit formation (Cloete and Maluleke 2005) and systems measuring the friction resistance airing from biofilm roughness. However, none can discriminate between biotic and abiotic fouling, and in most cases, they cannot detect thin biofilm layers (Pavanello et al. 2011). It would be better to utilise early warning systems, which allow biofilm detection at its initial stage of development, before it becomes a complex, multi-stratified and EPS-enclosed structure, much more difficult to remove. Thus, electrochemical sensors, including the ALVIM device (Pavanello et al. 2011) and BIoGEORGE sensors (Bruijs et al. 2001) have been developed, which exploit natural cathodic depolarisation induced by biofilm growth on alloys exposed to natural, aerated waters. These can provide information on biofilm development, measuring cathodic currents of samples polarised at a fixed potential, generating a signal when the biofilm exceeds a predetermined threshold in its surface area (Pavanello et al. 2011). In full-scale cooling water systems, these devices have given rapid and accurate information on formation and activity of biofilms, even at early stages of their surface colonisation, allowing an optimal, antimicrobial dosing regimen to be implemented that keeps biofilm development under control. Besides electrochemical sensors, optical techniques show promise for monitoring online biofilm development (Fischer, Wahl and Friedrichs 2012; Fischer, Triggs and Krauss 2016). The current state of monitoring techniques based on optical sensors has been reviewed (Fischer, Triggs and Krauss 2016), and the increasing number of biofilm monitoring systems based on the detection of changes in light properties discussed (Fischer, Triggs and Krauss 2016). These exploit interactions between light irradiation and biofilms including absorption/transmission, reflection, fluorescence and bioluminescence. In particular, methods based on fluorescence are especially because of their high sensitivity and rapid response time (Fischer, Wahl and Friedrichs 2012). Biofilm monitoring systems based on detection of fluorescing molecules have also been detailed. These include amino and nucleic acids, NAD(P)H, ATP and pyridoxine (Wolf, Crespo and Reis 2002; Fischer, Wahl and Friedrichs 2012). Online systems able to discriminate in situ biological deposits from chemical fouling by measuring simultaneously fluorescence, light refraction, transmission and scattering, in real time, have also been described (Strathmann et al. 2013). Several challenges still need to be overcome to improve such monitoring systems, for example in miniaturising the sensors using microfabrication technology or functionality of the sensor surfaces (Fischer, Triggs and Krauss 2016). Monitoring systems able to detect the compounds responsible for biofilm adhesion and development including AHLs and c-di-GMP and/or the EPS biopolymers or cell appendages, responsible for the initial contact with the colonisable surface would be particularly attractive. BIOFOULING CONTROL STRATEGIES Current practice to limit biofilm growth in cooling water systems The most common countermeasure adopted to control biofilm development in cooling water systems is to use oxidising (mainly chlorine, ozone, hydrogen peroxide) and/or non-oxidising (principally amines, aldehydes, isothiazolone) biocides (see Table 2) often combined with synthetic dispersants or enzymes for enhancing biocide activity (Cloete, Jacobs and Brozel 1998; Bott 2009). Their mode of action depends on which biocide is used (Russell 2003; Bridier et al. 2011), but their target sites are essentially cell wall components, cytoplasmic membranes, functional and structural proteins, RNA, DNA and other cytoplasmic components (Cloete, Jacobs and Brozel 1998). Their use is predicated on the view that disinfection, by killing microbial cells, will solve the biofouling problem (Flemming 2011). Table 2. Mainly chemical antifouling treatment methods commonly used in cooling systems (JEA 2005; Ludensky 2005; Rajagopal et al. 2012). Biocide type  Form  Recommended maximum concentration  Advantages  Disadvantages  Oxidising biocides              Cl2  Gas  0.5 mg/L  Economical, effectiveness  Toxic gas Safety concerns Costly equipment  NaOCl  Liquid  N/A  Economical, effectiveness  Low activity, limited stability  Calcium hypochlorite  Solid  N/A  Economical, effectiveness  Adds calcium to the system  NaOCl + NaBr  Liquid  N/A  Effective, easily retrofitted to most chlorination systems  Requires feeding two chemicals  Bromine Chloride  Liquid  N/A  Most economical form of bromine  Feeder cost, safety and handling concern  Stabilised bromine     0.2 mg/L  Good stability, less toxic  Higher cost, less effective on algae and at high organic load  Ozone  Gas  N/A  Effective against spore-formers and fungi  Very reactive and volatile, corrosive, rapidly lost, low solubility, safety concerns  Hydrogen peroxide  Liquid  N/A  Degrades to water and oxygen  Slower acting, needs higher residual  Non-oxidising biocides                 Target           Glutaraldehyde  Bacteria Algae Fungi  N/A  High efficacy in various applications  Inhalation toxicity  Thiocyanates  Bacteria  N/A  Low cost  Low solubility  Isothiazolone  Bacteria Algae Fungi  N/A  Persistent broad spectrum  Irritation, Skin sensitisation  Quaternary ammonium compounds  Bacteria Algae Mollusks  N/A  Broad spectrum, Fast acting  Not effective vs. fungi, Foam possible  Biocide type  Form  Recommended maximum concentration  Advantages  Disadvantages  Oxidising biocides              Cl2  Gas  0.5 mg/L  Economical, effectiveness  Toxic gas Safety concerns Costly equipment  NaOCl  Liquid  N/A  Economical, effectiveness  Low activity, limited stability  Calcium hypochlorite  Solid  N/A  Economical, effectiveness  Adds calcium to the system  NaOCl + NaBr  Liquid  N/A  Effective, easily retrofitted to most chlorination systems  Requires feeding two chemicals  Bromine Chloride  Liquid  N/A  Most economical form of bromine  Feeder cost, safety and handling concern  Stabilised bromine     0.2 mg/L  Good stability, less toxic  Higher cost, less effective on algae and at high organic load  Ozone  Gas  N/A  Effective against spore-formers and fungi  Very reactive and volatile, corrosive, rapidly lost, low solubility, safety concerns  Hydrogen peroxide  Liquid  N/A  Degrades to water and oxygen  Slower acting, needs higher residual  Non-oxidising biocides                 Target           Glutaraldehyde  Bacteria Algae Fungi  N/A  High efficacy in various applications  Inhalation toxicity  Thiocyanates  Bacteria  N/A  Low cost  Low solubility  Isothiazolone  Bacteria Algae Fungi  N/A  Persistent broad spectrum  Irritation, Skin sensitisation  Quaternary ammonium compounds  Bacteria Algae Mollusks  N/A  Broad spectrum, Fast acting  Not effective vs. fungi, Foam possible  View Large Table 2. Mainly chemical antifouling treatment methods commonly used in cooling systems (JEA 2005; Ludensky 2005; Rajagopal et al. 2012). Biocide type  Form  Recommended maximum concentration  Advantages  Disadvantages  Oxidising biocides              Cl2  Gas  0.5 mg/L  Economical, effectiveness  Toxic gas Safety concerns Costly equipment  NaOCl  Liquid  N/A  Economical, effectiveness  Low activity, limited stability  Calcium hypochlorite  Solid  N/A  Economical, effectiveness  Adds calcium to the system  NaOCl + NaBr  Liquid  N/A  Effective, easily retrofitted to most chlorination systems  Requires feeding two chemicals  Bromine Chloride  Liquid  N/A  Most economical form of bromine  Feeder cost, safety and handling concern  Stabilised bromine     0.2 mg/L  Good stability, less toxic  Higher cost, less effective on algae and at high organic load  Ozone  Gas  N/A  Effective against spore-formers and fungi  Very reactive and volatile, corrosive, rapidly lost, low solubility, safety concerns  Hydrogen peroxide  Liquid  N/A  Degrades to water and oxygen  Slower acting, needs higher residual  Non-oxidising biocides                 Target           Glutaraldehyde  Bacteria Algae Fungi  N/A  High efficacy in various applications  Inhalation toxicity  Thiocyanates  Bacteria  N/A  Low cost  Low solubility  Isothiazolone  Bacteria Algae Fungi  N/A  Persistent broad spectrum  Irritation, Skin sensitisation  Quaternary ammonium compounds  Bacteria Algae Mollusks  N/A  Broad spectrum, Fast acting  Not effective vs. fungi, Foam possible  Biocide type  Form  Recommended maximum concentration  Advantages  Disadvantages  Oxidising biocides              Cl2  Gas  0.5 mg/L  Economical, effectiveness  Toxic gas Safety concerns Costly equipment  NaOCl  Liquid  N/A  Economical, effectiveness  Low activity, limited stability  Calcium hypochlorite  Solid  N/A  Economical, effectiveness  Adds calcium to the system  NaOCl + NaBr  Liquid  N/A  Effective, easily retrofitted to most chlorination systems  Requires feeding two chemicals  Bromine Chloride  Liquid  N/A  Most economical form of bromine  Feeder cost, safety and handling concern  Stabilised bromine     0.2 mg/L  Good stability, less toxic  Higher cost, less effective on algae and at high organic load  Ozone  Gas  N/A  Effective against spore-formers and fungi  Very reactive and volatile, corrosive, rapidly lost, low solubility, safety concerns  Hydrogen peroxide  Liquid  N/A  Degrades to water and oxygen  Slower acting, needs higher residual  Non-oxidising biocides                 Target           Glutaraldehyde  Bacteria Algae Fungi  N/A  High efficacy in various applications  Inhalation toxicity  Thiocyanates  Bacteria  N/A  Low cost  Low solubility  Isothiazolone  Bacteria Algae Fungi  N/A  Persistent broad spectrum  Irritation, Skin sensitisation  Quaternary ammonium compounds  Bacteria Algae Mollusks  N/A  Broad spectrum, Fast acting  Not effective vs. fungi, Foam possible  View Large However, biofilm cells display a higher tolerance to disinfectants than their planktonic counterparts. Their increased resistance is multi-factorial (Heinzel 1998; Bridier et al. 2011; Pal et al. 2015) resulting from phenotypic adaptation, gene transfers and mutations (Kelly, Vespermann and Bolton 2009; Hannan et al. 2010). Increased resistance is also intimately related to their tree-dimensional structures (Bridier et al. 2011), with the key role most likely played by the EPS matrix. This compact structure may hamper biocide efficacy by limiting their penetration to the extent where microbial cells are not exposed to them (Cloete, Jacobs and Brozel 1998; Flemming and Ridgway 2009; Bridier et al. 2011; Kundukad et al. 2016). Optimising the breakdown of this matrix is therefore essential to improve the disinfection process, by disrupting the EPS matrix and exposing microbial cells to the biocide (Cloete, Jacobs and Brozel 1998). Dispersants and emulsifiers are also commonly used in combination with biocides in cooling water systems. Their possession of both hydrophilic and hydrophobic functional groups enable them to penetrate the complex the EPS matrix and to pre-condition the biofilm surface (Cloete, Jacobs and Brozel 1998). Sulphonates, sulphates and quaternary ammonium compounds represent the most commonly used surfactants in industrial systems (Cloete, Jacobs and Brozel 1998). ‘Green’ bio-dispersants, mainly polyglucosides, characterised by their high biodegradability, lack of potential bioaccumulation, non-toxicity and non-carcinogenicity have also been proposed for cooling water systems (Di Pippo et al. 2017). Similarly, the use of enzyme-based detergents, mainly proteases and polysaccharide hydrolysing enzymes (Meyer 2003), can also enhance the cleaning process (Bridier et al. 2011), exploiting their activities against key EPS matrix components. Commercial enzyme formulations containing mixtures of enzymes with different substrate specificities are available, although it is important to elucidate the biofilm matrix composition first so that the appropriate enzymes, proteases, cellulases, polysaccharide depolymerases, DNAse, can be applied (Bridier et al. 2011). Indeed, the biofilm matrix composition will vary depending on different abiotic conditions (i.e. pH, temperature, pressure and shear forces) and on biofilm community diversity (Neu 1994; Di Pippo et al. 2009). Because biofilms in cooling water systems are complex microbial communities (Wang et al. 2013; Di Gregorio et al. 2017), their EPS matrix composition will reflect the populations present there (Flemming, Neu and Wozniak 2007), and this may change in response to environmental factors, such as irradiance in phototrophic biofilms, where EPS composition is closely related to photosynthesis diurnal fluctuations (Staats et al. 2000; Otero &Vincenzini 2003; Stal and Defarge 2005). For many years, chlorine was the biocide used in almost all industries, being relatively cheap, largely available and easy to apply. However, its detrimental effect on the quality of the water discharged into the recipient environment severely restricts its use. Furthermore, chlorine can form carcinogenic compounds like chloromethanes in contact with organic material in natural environments (Bott 2009). Ozone has also been used to sterilise cooling water. However, it too has a number of limitations. Ozone decomposes rapidly in water, its half-life time in pure water is a few hours but in waters used for cooling purpose, the half-life is reduced to minutes by its oxidation of any organic matter present. Its rate of decomposition also depends on the water pH, being higher at increased pH values. Moreover, ozone reacts with natural organic substances to produce low molecular weight oxygenated byproducts that generally are more biodegradable than their precursors. These promote biological growth and further limit the disinfection efficacy of ozone (Cloete, Jacobs and Brozel 1998). Dechlorination before disposal can be an alternative to the discharge of chlorinated water. Since techniques for dechlorination constitute additional operating costs, efforts should be directed to finding more efficient, economic and environmentally friendly biocides (Bott 2009). Future perspectives for biofilm control The need to manage biofouling in industrial systems beyond the application of one-shot solutions in order to prevent and/or limit biofilm growth has been already emphasised (Flemming and Ridgway 2009; Flemming 2011). One of the most effective and convenient methods to minimise biofilm development is to focus on the initial developmental step of cell adhesion by using low-fouling surfaces, not readily prone to microbial colonisation. It is possible now to treat surfaces of cooling water systems with paints or multi-layer coatings at different key locations, e.g. intake conduits, pipes or condenser waterboxes. Many innovative and developing technologies come from the marine fields, where biofouling on ship hulls is a serious problem and is usually controlled by hull coatings releasing at controlled rates antimicrobial compounds that inhibit the growth of benthic microbes (Ma et al. 2017). Organotin- and metal-based coatings have been extremely successful in biofouling prevention and are widely used in the antifouling paints of ships (Howell and Behrends 2010; Ten Haller-Tjabbes and Walmsley 2010). However, their banning, because of their toxic effects on the marine ecosystem, and the potential development of antibiotic resistance among strains of the fouling bacteria, have necessitated searches for alternative, sustainable and environmentally safe antifouling approaches. Advances in nanotechnology and polymer science meet the need for using ‘green’ technologies to develop non-biocidal, non-fouling coatings for the maritime industry. An example is the fabrication of amphiphilic surfaces displaying both hydrophobic and hydrophilic domains to avoid microbial attachment, foul release (FR) systems, consisting of advanced composite silicon polymers and hydrogel nanolayers that weaken foulant interfacial bond. These FR properties have been combined with microencapsulated hydrolytic enzymes (e.g. serin proteases) capable of preventing bioadhesion to effectively replace traditional biocidal paints (Callow and Callow 2011; Ciriminna, Bright and Pagliaro 2015). In this context, Ma et al. (2017) have synthesised novel coatings by incorporating butenolide derived from the marine bacteria Streptomyces spp. into biodegradable poly(ε-caprolactone)-based polyurethane. Apart from seeking ‘green’ fouling resistant coatings, other bio-inspired antifouling, long lasting solutions have sought to mimic the surface topographies of certain marine fauna (shark, pilot whale) and aquatic plants (lotus leaf) (Nir and Reches 2016). Their unique surface roughness and wettability protect these marine organisms from bio-adhesion, and these properties have been reproduced using soft litography on polydimethylsiloxane, and by polyelectrolyte layer-by-layer spray coating. The lotus leaf superhydrophobic and self-cleaning properties have been reproduced by thermal deposition of paraffin and fluorinated waxes on a range of surfaces (e.g. copper, glass, and silicon) that then exhibited durable resistance to biofilm formation and development. Furthermore, Kreder et al. (2016) have designed a new naturally derived antifouling solution, the ‘slippery liquid infused porous surface’ (SLIPS), derived from Nepenthes carnivorous plant. It resists wetting by oil, water and even blood. Moreover, SLIPS has proved effective in preventing the growth of Pseudomonas aeruginosa, Escherichia coli and Staphylococcus aureus. SLIPS also exhibits great durability under extreme environmental conditions including high temperatures, extreme pH values and UV radiation. The interest in mimicking some of the naturally evolved antifouling strategies exhibited by aquatic organisms has also led Sathe et al. (2017) to exploit reactive oxygen species, ROS, used in some algae against biofouling. ROS production has been achieved with fabrication of a ZnO photocatalytic nanocoating on fishing nets. The authors compared biofilm communities grown in mesocosms upon light activation, on ZnO nanorods and antifouling (AF, copper) coated nets and control uncoated nets, with high throughput DNA sequencing. Improved performance was achieved with the nanostructured (ZnO) nets over the AF coated net, with microbial abundances significantly lower with the former. Furthermore, there was a preferential removal of the pathogenic biofilm members with the AF coated nets. The authors concluded that sunlight-responsive antifouling ZnO nanorods coating is more efficient at mitigating biofouling than commercial biocidal paints, and they emphasise the scalability and low-cost potential of their approach as an example of solar-assisted, environmentally friendly antifouling technologies (Sathe et al. 2017). Other innovative approaches have been developed, based on fundamental understanding of the foulant adhesion strategies leading to manufacture of less specific antifouling coatings. Libraries of peptide anchors, including 3,4-dihydoxy-L-phenyalanine (DOPA), a common constituent of adhesive proteins in marine organisms, were designed and conjugated to a range of polymers, especially saccharides, showing the capability of adhering to different surfaces and thus conferring resistance to non-specific interaction (Nir and Reches 2016). Further development of this bio-molecular mimetic approach led to the polymerisation of DOPA into sticky coatings to then be cast as adhesive-activated layers on silicon surfaces. DOPA-based tripeptides have also been developed that exhibit self-assembly properties into antifouling films, thin transparent coatings of 3 nm in thickness, on range of surfaces, preventing protein adsorption and thus biofilm formation (Nir and Reches 2016). The understanding of the in vivo mechanisms involved in biofilm initial adhesion and development led to the search for QS inhibitors or quenchers as natural antifouling compounds (Jha et al. 2013; Nir and Reches 2016). One approach was to design structural analogues of the AHL QS autoinducers, on the basis that these would exert the same biological function, thus abolishing cell-to-cell communication. Indeed, a range of lactone derivatives and furanones have now been explored as quorum quenchers with some success, indicating it might be possible with them to alter microbial biofilm morphology and functioning (Wu et al. 2004). Jha et al. (2013) have described a QS inhibitor 2-dodecanoyloxyethanesulfonate, a compound extracted from the red alga Asparagopsis taxiformis. Exploitation of natural substances isolated from a broad range of biological sources, including terrestrial plants, algae, corals and microbes shows promise in biofouling prevention and mitigation, as these compounds exhibit a compatibility with biological systems and a higher specificity than heavy metals (Chen and Qian 2017; Le Norcy et al. 2017; Ma et al. 2017; Dahms and Dobretsov 2017; Wang et al. 2017). A wealth of reports exists on their biological and antimicrobial activities in vitro. However, progress in applying them as effective antifouling agents has yet to be pursued, especially in terms of their cost effective mass production, biosafety and antifouling action. Problems still to be solved satisfactorily are the incorporation of these antifouling compounds into suitable polymers and their compatibility and controlled release from new generation coatings (Ma et al. 2017). Furthermore, the potential use of natural product-based antifouling coatings in industrial cooling water systems must be tested on-site, or, at least, on multispecies biofilms grown in systems that mimic the real conditions, to verify their applicability on treated surfaces, their antifouling effects and lifetime. CONCLUSIONS A thorough insight in the microbial community organisational structure, with a major attention to microbial key players, is necessary to encourage the development and the application of sensitive and effective biofouling control measures. Unfortunately, even though many aspects of the ecology of biofilms in natural habitats and their formation in medical fields have been disclosed, only scant information is available on those in cooling water systems. A critical evaluation of the available literature here highlights the research questions urgently needing answers and deserving further investigation. The scarce evidences from long-term studies performed on multi-species biofilms growing in cooling industrial systems and the lack of data on biofilm formation processes in such systems have prevented the elucidation of the key molecular and ecophysiological details of their initiation and development. This situation has clearly limited the development of reliable and robust early-warning monitoring approaches. The need for better exploitation of novel, sustainable and environmentally safe antifouling control strategies as alternatives to toxic biocides, e.g. chlorine, commonly used in cooling water systems has also been discussed. ACKNOWLEDGEMENTS The Authors wish to thank Prof. Robert Seviour for the critical review of the English version and Dr Elena Romano from the Centre of Advanced Microscopy ‘P. Albertano’ (CAM), Department of Biology, University of Rome ‘Tor Vergata’, for her skillful assistance in the use of the facility. Conflict of interest. None declared. 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TI - Biofilm growth and control in cooling water industrial systems
JF - FEMS Microbiology Ecology
DO - 10.1093/femsec/fiy044
DA - 2018-05-01
UR - https://www.deepdyve.com/lp/oxford-university-press/biofilm-growth-and-control-in-cooling-water-industrial-systems-rNfHY3fJAY
SP - fiy044
VL - 94
IS - 5
DP - DeepDyve
ER -