The genus Tenacibaculum encompasses several species pathogenic for marine ﬁsh. Tenacibaculum dicentrarchi and “Tenacibaculum ﬁnnmarkense” (Quotation marks denote species that have not been validly named.) were retrieved from skin lesions of farmed ﬁsh such as European sea bass or Atlantic salmon. They cause a condition referred to as tenacibaculosis and severe outbreaks and important ﬁsh losses have been reported in Spanish, Norwegian, and Chilean marine farms. We report here the draft genomes of the T. dicentrarchi and “T. ﬁnnmarkense” type strains. These genomes were compared with draft genomes from ﬁeld isolates retrieved from Chile and Norway and with previously published Tenacibaculum genomes. We used Average Nucleotide Identity and core genome-based phylogeny as a proxy index for species boundary delineation. This work highlights evolution of closely related ﬁsh-pathogenic species and suggests that homologous recombination likely contributes to genome evolution. It also corrects the species afﬁliation of strain AYD7486TD claimed by Grothusen et al. (2016). Key words: Tenacibaculum, tenacibaculosis, genomes, ﬁsh pathogens, virulence, evolution. Introduction those, several species of the genus Tenacibaculum are respon- The rapid development of intensive aquaculture has been as- sible for diseases collectively designated tenacibaculosis sociated with a dramatic increase in outbreaks of infectious (Avendano-Herrera et al. 2006; Suzuki 2015). diseases (FAO 2016; Bayliss et al. 2017). The rapid interna- Tenacibaculum dicentrarchi and “Tenacibaculum tional spread of pathogens through the trade of ﬁsh and eggs ﬁnnmarkense” are two among those ﬁsh-associated, recently or as a response to environmental changes has been docu- described species. The former was ﬁrst isolated from mented (Brynildsrud et al. 2014; Rahmati-Holasoo et al. European sea bass (Dicentrarchus labrax)in Spain (Pineiro- 2016). In this context, the success and sustainability of aqua- Vidal et al. 2012) and recently also identiﬁed from Atlantic culture largely depend on the control of pathogens. Among salmon (Salmo salar) in Chile (Avendano-Herrera et al. 2016) The Author(s) 2018. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/), which permits non- commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact firstname.lastname@example.org 452 Genome Biol. Evol. 10(2):452–457. doi:10.1093/gbe/evy020 Advance Access publication January 19, 2018 Downloaded from https://academic.oup.com/gbe/article-abstract/10/2/452/4817510 by Ed 'DeepDyve' Gillespie user on 16 March 2018 Evolution of Fish-Pathogenic Species GBE and Norway (Olsen et al. 2017) and from red conger eel Sequencing reads were assembled using Velvet (Zerbino and (Genypterus chilensis)in Chile (Irgang et al. 2017). Birney 2008)or SPAdes (Bankevich et al. 2012). Genome an- “Tenacibaculum ﬁnnmarkense” was isolated from notation, including manual curation, and genome compari- Atlantic salmon with ulcerative disease in Norway son including core genome computation were performed (Sma ˚ ge et al. 2016). using the MicroScope platform (Medigue et al. 2017 and Identiﬁcation of the causative agent of tenacibaculosis was references therein). ﬁrst based on the isolation of bacteria from tissues of diseased ﬁsh and their characterization by phenotypic, biochemical, and serological methods (Pineiro-Vidal, Carballas et al. ANI and Phylogenetic Reconstruction 2008; Pineiro-Vidal, Riaza et al. 2008). The use of 16 S ANIs analyses were performed using the ANIm method de- rDNA sequencing improved the identiﬁcation reliability scribed by Richter and Rossello-Mora (2009) and imple- (Cepeda et al. 2003; Fringuelli et al. 2012). However, these mented in the Python module Pyani (https://github.com/ methods usually cannot differentiate closely related bacterial widdowquinn/pyani). Digital DNA–DNA hybridization was species. MLST was developed (Habib et al. 2014) and used to performed using the GGDC website (http://ggdc.dsmz.de/) demonstrate the presence of T. dicentrarchi in Chile and Formula 2 (Auch et al. 2010). Logistic regression was (Avendano-Herrera et al. 2016) and to reveal the variety of used for reporting the probabilities that DDH is70% and Tenacibaculum spp. in a number of sea-farmed ﬁsh species in thus accounting for bacteria belonging to the same species. Norway (Olsen et al. 2017). Pairwise alignments were computed using the MUMer soft- In this study, we present seven draft genomes of ware (Kurtz et al. 2004). For phylogenetic reconstruction, Tenacibaculum strains, including the T. dicentrarchi (USC T T comparison of the gene content between strains was done 3509 )and “T. ﬁnnmarkense”(HFJ )type strains,as well as by pairwise proteome similarity search using BlastP ﬁve ﬁeld isolates from Chile and Norway selected on the basis Bidirectional Best Hit and the MicroScope default parameters of available MLST data (Olsen et al. 2017). Comparison has (i.e., >80% protein identity, >80% coverage). A set of 895 been performed with available Tenacibaculum genomes from groups of orthologous proteins was retained and multiple Genbank, including strain AYD7486TD originally described as alignments on individual orthologous proteins were per- T. dicentrarchi (Grothusen et al. 2016). We used Average formed using MUSCLE (Edgar 2004) implemented in the Nucleotide Identity (ANI) to delineate species boundaries msa R package (Bioconductor). The resulting alignments and core genome analysis to infer phylogenetic relationships were manually checked and concatenated for tree recon- between these strains. We also correct the species afﬁliation struction using UGENE and PhyML with default parameters of strain AYD7486TD. (Okonechnikov et al. 2012). Tree rendering was achieved us- ing the Figtree software (http://tree.bio.ed.ac.uk/software/ﬁg- Materials and Methods tree/). The neighbor-net analysis in the Splits Tree 4 software (http://splitstree.org/; Huson and Bryant 2006) provided a phy- Bacterial Strains logenetic network representing possible evolutionary relation- The T. dicentrarchi type strain USC 3509 (Pine ~ iro-Vidal et al. ships between the concatenated sequences of core genome 2012) was obtained from Dr Y. Santos (University of Santiago genes. Minimal recombination breakpoints were identi- de Compostela, Spain) and the “T. ﬁnnmarkense”strain HFJ ﬁed using the four-gamete test (Hudson and Kaplan (Sma ˚ ge et al. 2016) was obtained from Dr H. Duesund 1985). Putative recombination events were indicated as (Cermaq Group AS, Bergen, Norway). Strains TNO006, pairwise homoplasy index (PHI; Bruen et al. 2006)calcu- TNO010, and TNO020 were isolated from skin ulcers of latedby SplitsTree 4. Atlantic salmon in Norway whereas strain TNO021 was iso- lated from mouth ulcer of a corkwing-wrasse (Symphodus Results and Discussion melops) alsoinNorway (Habib et al. 2014; Olsen et al. 2017). Strain TdChD05 was retrieved from external lesion of General Genome Features an Atlantic salmon in Chile (Avendan ~o-Herrera et al. 2016). A summary of the genomes analyzed in this study is presented All strains were routinely grown on marine agar 2216 (Difco) in supplementary table 1, Supplementary Material online. and in the corresponding broth at 170 rpm and 15 C Strikingly, the sizes of the genomes reported here are the (TNO006) or 22 C (all other strains). smallest among those available to date for the genus Tenacibaculum (e.g., T. maritimum:3.4Mb, T. soleae: Genome Sequencing and Annotation 3.0 Mb, T. ovolyticum: 4.1 Mb). The average genome size is Genomic DNA was extracted with the Wizard Genomic DNA 2.7 Mb and 2.9 Mb for T. dicentrarchi and “T. ﬁnnmarkense,” Puriﬁcation Kit (PROMEGA). All strains were sequenced with respectively; at 2.4 Mb, strain TNO020 has the smallest ge- Illumina (HiSeq 2x100 pair-end reads with 300 bp insert size). nome. All strains studied are devoid of plasmid. Genome Biol. Evol. 10(2):452–457 doi:10.1093/gbe/evy020 Advance Access publication January 19, 2018 453 Downloaded from https://academic.oup.com/gbe/article-abstract/10/2/452/4817510 by Ed 'DeepDyve' Gillespie user on 16 March 2018 Bridel et al. GBE ANI Delineates T. dicentrarchi and “T. ﬁnnmarkense”and “T. ﬁnnmarkense” strains in two connected subclusters as Allocates Strain AY7486TD to “T. ﬁnnmarkense” previously observed in the MLST data set of Olsen et al. (2017). Whatever the group of strains considered (i.e., ANI was reported to be an accurate and practical method for clades I and III strains, clades I, II, and III strains as well species delineation and a 95–96% identity was proposed as as clades I, II, III, and IV strains), the PHI test P-value is 0.0, the threshold (Rodriguez-R and Konstantinidis 2014). ANI indicating signiﬁcant evidence of recombination. In addi- comparisons were computed using T. ovolyticum (Suzuki tion, the high number of recombination breakpoints et al. 2001) as an outgroup and the results were plotted as found in T. dicentrarchi and “T. ﬁnnmarkense”genomes a heatmap (supplementary ﬁg. 1A and 1B, Supplementary (10 per kilobase in average) is another clue suggesting Material online). Strains TdChD05 from Chile and TNO021 recombination events in these species. from Norway, both previously allocated to the species T. dicentrarchi (Pineiro-Vidal et al. 2012; Olsen et al. 2017; Avendano-Herrera et al. 2016), indeed form a highly cohesive T Comparative Genomics Highlights Intricate Relationships group with T. dicentrarchi USC 3509 (98% ANI and 88% between T. dicentrarchi and “T. finnmarkense” alignment coverage). In contrast, strain AY7486TD, also orig- inally described as T. dicentrarchi (Grothusen et al. 2016), The average number of predicted CDS for T. dicentrarchi and displays an ANI value of only 93% with the type strain of “T. ﬁnnmarkense” strains is 2,381 and 2,536, respectively, this species and consequently does not fall within the T. dicen- which is in good agreement with the observed genome sizes. trarchi cluster. Instead, strain AYD7486TD forms a cluster with The core genome is composed of 2,013 and 1,947 CDS for strains TNO006, TNO010 and “T. ﬁnnmarkense”HFJ (96% T. dicentrarchi and “T. ﬁnnmarkense,” respectively (supple- ANI and 85% alignment coverage, above the species delin- mentary ﬁg. 2A and B, Supplementary Material online). These eation threshold). ANI values delineate two subclusters, one small gene sets, about half those of Tenacibaculum agarivor- grouping strains TNO010 and AYD7486TD (99% ANI) and ans HZ1 (Xu et al. 2017)and Tenacibaculum jejuense KCTC the other grouping strain TNO006 and “T. ﬁnnmarkense” 22618 (Ficko-Blean 2017), seem related to a deﬁcient HFJ (98% ANI). Supplementary ﬁgure 1, Supplementary biopolymer-degrading ability of T. dicentrarchi and Material online, also shows that although T. dicentrarchi “T. ﬁnnmarkense.” Indeed, these genomes lack the pathways and “T. ﬁnnmarkense” are distinct species they obviously dis- encoding for the degradation of marine carbohydrates (e.g., play signiﬁcant proximity in terms of sequences identity (93– sulfatase, glycoside hydrolase, polysaccharide lyase) identiﬁed 94% ANI) and fraction of shared genomes (77–88%). Strain in the environmental species T. agarivorans and T. jejuense,in TNO020 does not belong to any of the previously deﬁned line with a restricted ecological niche (i.e., ﬁsh tissues) and an clusters (88–89% ANI; 55–68% alignment coverage) and exclusive protein-based predicted regimen for these patho- therefore likely belongs to a yet undescribed Tenacibaculum genic species. Moreover, the presence of insertion sequences species as previously suggested (Habib et al. 2014; Olsen et al. or their scars as well as genes remnants in T. dicentrarchi, 2017). The same conclusions (supplementary ﬁg. 1C, “T. ﬁnnmarkense” and strain TNO020 argues for genome Supplementary Material online) were drawn using genome- reduction trends in contrast to the horizontal transfer genes to-genome distance calculator (Auch et al. 2010). As in T. jejuense and T. agarivorans. These ﬁndings support the expected, T. ovolyticum DSM 18103 behaves as an outgroup expected small genome size of bacterial pathogens compared displaying lower sequence identity (85%) and poor alignment with their nonpathogenic relatives (Weinert and Welch 2017). coverage (17–34%) with all other strains studied. Using 895 The core genome of the seven strains belonging to both core genome-encoding protein sequences, we constructed a T. dicentrarchi and “T. ﬁnnmarkense” is composed of 1,818 phylogenetic tree from the concatenation of each individual CDS (supplementary ﬁg. 2C, Supplementary Material online), alignment (ﬁg. 1). Bootstrap values strongly support the divi- a value close to those computed for each species. Each strain sion between T. dicentrarchi and “T. ﬁnnmarkense”and the has 180 speciﬁc genes essentially composed of prophages core genome-based phylogenetic tree perfectly matches remnants, restriction/modiﬁcation systems, toxin/antitoxin the ANI dendogram. Furthermore, a correlation between systems and transposases encoding genes or their scars as theMLSTclades deﬁned by Olsen et al. (2017)and the clus- well as genes required for the biosynthesis of exopolysacchar- ters observed in ﬁgure 1 is obvious: “T. ﬁnnmarkense”HFJ ides that likely account for the minor intraspecies genome size and strain TNO006 belong to clade III, strains TNO010 and differences previously mentioned. These strain-speciﬁc genes, AYD7486TD to clade I, all three T. dicentrarchi strains to clade representing the accessory genome, do not seem linked to II and strain TNO020 to clade IV. Using Splits Tree analysis, a bacterial pathogenicity as no bona ﬁde toxin or virulence reticulated network structure between the four clades, indic- factor-encoding genes have been identiﬁed in this gene ative of within and between species recombination events pool. Therefore, virulence-encoding genes likely belong to (ﬁg. 2), is observed. The dense network joining clade I and the core genome common to both T. dicentrarchi and clade III is in good agreement with the grouping of “T. ﬁnnmarkense.” Among those, peptidases containing a 454 Genome Biol. Evol. 10(2):452–457 doi:10.1093/gbe/evy020 Advance Access publication January 19, 2018 Downloaded from https://academic.oup.com/gbe/article-abstract/10/2/452/4817510 by Ed 'DeepDyve' Gillespie user on 16 March 2018 Evolution of Fish-Pathogenic Species GBE FIG.1.—Core genome phylogeny. Phylogenetic tree inferred by PhyML with boostraping (100 replicates) using the concatenation of the 895 aligned orthologous genes. The MLST clades I–IV deﬁned in Olsen et al. (2017) are reported. FIG.2.—Detection of recombination. Reticulate evolutionary relationship between concatenated sequences of the 895 core genome genes visualized by the Splits Tree neighbor-net analysis. The clades deﬁned in Olsen et al. (2017) are reported. carboxy-terminal protein domain (TIGR04183), predicted to evolution for some virulence-linked functions in ﬁsh- be required for T9SS-mediated secretion and cell surface ex- pathogenic Tenacibaculum species. posure (Veith et al. 2013), were identiﬁed. These peptidases (i.e., TFINN_2500013, TFINN_140038,and TFINN_60057 T Conclusion from “T. ﬁnnmarkense”HFJ and their orthologs) are likely involved in the breakdown of proteinaceous compounds and Since the pioneering work of Wakabayashi and col. on T. the destruction of host tissues. The presence of a M9 family maritimum in the eighties (Wakabayashi et al. 1986), many protease-encoding gene (TFINN_140038 and orthologs), sim- other Tenacibaculum species have been described. Some of ilar to the 120 kDa collagenase of Clostridium perfringens them are important ﬁsh pathogens and an unexpected diver- (Matsushita et al. 1994) but different from the M43 family sity at different levels (e.g., genetic, ﬁsh host, geographical) collagenase (encoded by MARIT_1085) identiﬁed in T. mariti- has been reported (Habib et al. 2014; Olsen et al. 2017). mum (Perez-Pascual et al. 2017), suggests convergent Tenacibaculum dicentrarchi strains were previously identiﬁed Genome Biol. Evol. 10(2):452–457 doi:10.1093/gbe/evy020 Advance Access publication January 19, 2018 455 Downloaded from https://academic.oup.com/gbe/article-abstract/10/2/452/4817510 by Ed 'DeepDyve' Gillespie user on 16 March 2018 Bridel et al. GBE from several farmed ﬁsh species in Spain, Norway and Chile, computational resources: The INRA MIGALE bioinformatics whereas “T. ﬁnnmarkense” strains were exclusively isolated in platform (http://migale.jouy.inra.fr), the LABGeM, and the Norway so far (Olsen et al. 2017). Thanks to genomes com- National Infrastructure “France Genomique” funded as part parison, we were able to correct the afﬁliation of strain of the Investissement d’avenir program managed by Agence AYD7486TD which actually belongs to the species “T. Nationale pour la Recherche (contract ANR-10-INBS-09). A.- ﬁnnmarkense” rather than to T. dicentrarchi as previously H. acknowledges Grant FONDECYT 1150695 and the claimed (Grothusen et al. 2016). Importantly, this result dem- CONICYT/FONDAP/15110027 from the Comision Nacional onstrates that “T. ﬁnnmarkense” is also present in Chilean de Investigacion Cientıﬁca y Tecnologica (CONICYT, Chile). ﬁsh farms. Our data set suggests that T. dicentrarchi strains The authors are very grateful to Sophie Pasek and Mathilde form a cohesive group whereas “T. ﬁnnmarkense” strains are Carpentier for fruitful discussion. split into two subclusters. Similar subclusters, referred to as genomovars, were reported in Flavobacterium columnare, Literature Cited another ﬁsh pathogen of the family Flavobacteriaceae with Auch AF, Klenk H-P, Go ¨ ker M. 2010. Standard operating procedure for a broad host range. Correlations between genomovars, ﬁsh calculating genome-to-genome distances based on high-scoring seg- hosts and virulence have been suggested (Evenhuis and ment pairs. Stand Genomic Sci. 2(1):142–148. LaFrentz 2016; Olivares-Fuster et al. 2007). Hence, the ~ Avendano-Herrera R, et al. 2016. Isolation, characterization and virulence potential of Tenacibaculum dicentrarchi in salmonid cultures in Chile. same type of genomic heterogeneity observed in “T. Transbound Emerg Dis. 63(2):121–126. ﬁnnmarkense” may account for speciﬁc traits such as host ~ ~ Avendano-Herrera R, Toranzo AE, Magarinos B. 2006. Tenacibaculosis speciﬁcity or level of virulence. Strikingly, the virulence factors infectioninmarine ﬁsh caused by Tenacibaculum maritimum:a re- described in the closely related species T. maritimum (i.e., a view. Dis Aquat Organ. 71(3):255–266. sphingomyelinase, a ceramidase, a chondroitin AC lyase, a Bankevich A, et al. 2012. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol. sialidase and a M43 family collagenase; Perez-Pascual et al. 19(5):455–477. 2017) have not been identiﬁed in any of the genomes de- Bayliss SC, et al. 2017. The promise of whole genome pathogen sequenc- scribed in the present study. In full agreement with this ob- ing for the molecular epidemiology of emerging aquaculture patho- servation, a parallel evolution of pathogenicity in the species gens. Front Microbiol. 8:121. encompassed in the genus Tenacibaculum has been proposed Bruen TC, Philippe H, Bryant D. 2006. A simple and robust statistical test for detecting the presence of recombination. Genetics (Habib et al. 2014). However, the grouping of T. dicentrarchi 172(4):2665–2681. and “T. ﬁnnmarkense” aswellas T. soleae and T. ovolyticum Brynildsrud O, et al. 2014. Microevolution of Renibacterium salmonina- (Habib et al. 2014; Olsen et al. 2017; Sma ˚ ge et al. 2016)in a rum: evidence for intercontinental dissemination associated with ﬁsh single clade exclusively encompassing ﬁsh-associated bacteria movements. ISME J. 8(4):746–756. suggests evolution of these four species from a pathogenic an- Cepeda C, Garcıa-Marquez S, Santos Y. 2003. Detection of Flexibacter maritimus in ﬁsh tissue using nested PCR ampliﬁcation. J Fish Dis. cestor. In addition, our data support recombination as an im- 26(2):65–70. portant force shaping genome evolution of these ﬁsh pathogens Edgar RC. 2004. MUSCLE: multiple sequence alignment with high accu- as previously observed in other members of the family racy and high throughput. Nucleic Acids Res. 32(5):1792–1797. Flavobacteriaceae (Nicolas et al. 2008; Vos and Didelot 2009). Evenhuis JP, LaFrentz BR. 2016. Virulence of Flavobacterium columnare The genome sequences reported here should therefore facilitate genomovars in rainbow trout Oncorhynchus mykiss.Dis Aquat Organ. 120(3):217–224. future epidemiological studies and provide new insights into FAO. 2016. The State of World Fisheries and Aquaculture 2016. Available pathogenicity and niche adaptation of emerging ﬁsh pathogens. from: http://www.fao.org/3/a-i5555e.pdf. Ficko-Blean E, et al. 2017. Carrageenan catabolism is conferred by a com- plex regulon in marine heterotrophic bacteria. Nat Commun Supplementary Material (forthcoming) Supplementary data areavailableat Genome Biology and Fringuelli E, et al. 2012. Development of a quantitative real-time PCR for Evolution online. the detection of Tenacibaculum maritimum and its application to ﬁeld samples. J Fish Dis. 35(8):579–590. Grothusen H, et al. 2016. First complete genome sequence of Acknowledgments Tenacibaculum dicentrarchi, an emerging bacterial pathogen of sal- monids. Genome Announc. 4(1):e01756–15. This study was funded by the EU EMIDA ERA-NET project Habib C, et al. 2014. Multilocus sequence analysis of the marine bacterial “Control Flavobacteriaceae Infections in European Fish genus Tenacibaculum suggests parallel evolution of ﬁsh pathogenicity and endemic colonization of aquaculture systems. Appl Environ farms” and by the Agence Nationale pour la Recherche (con- Microbiol. 80(17):5503–5514. tract ANR-14-CE19-0020). This work has beneﬁted from the Hudson RR, Kaplan NL. 1985. Statistical properties of the number of re- facilities and expertise of the high-throughput sequencing combination events in the history of a sample of DNA sequences. platform of I2BC (Centre de Recherche de Gif; http://www. Genetics. 111(1):147–164. i2bc.paris-saclay.fr/spip.php? article399&lang¼en). We also Huson DH, Bryant D. 2006. Application of phylogenetic networks in evo- lutionary studies. Mol Biol Evol. 23(2):254–267. wish to thank the following structures for providing 456 Genome Biol. Evol. 10(2):452–457 doi:10.1093/gbe/evy020 Advance Access publication January 19, 2018 Downloaded from https://academic.oup.com/gbe/article-abstract/10/2/452/4817510 by Ed 'DeepDyve' Gillespie user on 16 March 2018 Evolution of Fish-Pathogenic Species GBE Irgang R, et al. 2017. First identiﬁcation and characterization of Iran: clinical, histopathological and molecular study. J Fish Dis. Tenacibaculum dicentrarchiisolated from Chilean red conger eel 39(10):1153–1163. (Genypterus chilensis, Guichenot 1848). J Fish Dis. 40(12):1915–1920. Richter M, Rossello-Mora R. 2009. Shifting the genomic gold standard for Kurtz S, et al. 2004. Versatile and open software for comparing large the prokaryotic species deﬁnition. Proc Natl Acad Sci U S A. genomes. Genome Biol. 5(2):R12. 106(45):19126–19131. Matsushita O, Yoshihara K, Katayama S, Minami J, Okabe A. 1994. Rodriguez-R LM, Konstantinidis KT. 2014. Bypassing cultivation to identify Puriﬁcation and characterization of Clostridium perfringens 120-kilo- bacterial species. Microbe 9(3):111–118. dalton collagenase and nucleotide sequence of the corresponding Sma ˚ ge SB, et al. 2016. Tenacibaculum ﬁnnmarkense sp. nov., a ﬁsh gene. J Bacteriol. 176(1):149–156. pathogenic bacterium of the family Flavobacteriaceae isolated Medigue C, et al. 2017. MicroScope-an integrated resource for commu- from Atlantic salmon. Antonie Van Leeuwenhoek. nity expertise of gene functions and comparative analysis of microbial 109(2):273–285. genomic and metabolic data. Brief Bioinformatics bbx113, https://doi. Suzuki M. 2015. Tenacibaculum. In: Whitman WB, Rainey F, K€ ampfer P, org/10.1093/bib/bbx113. Trujillo M, Chun J, DeVos P, Hedlund B, Dedysh S, editors. Bergey’s Nicolas P, et al. 2008. Population structure of the ﬁsh-pathogenic bacte- manual of systematics of archaea and bacteria. Chichester (United rium Flavobacterium psychrophilum. Appl Environ Microbiol. 74(12): Kingdom): John Wiley & Sons, Ltd. p. 1–7. Available from: http:// 3702–3709. doi.wiley.com/10.1002/9781118960608.gbm00345 (accessed Okonechnikov K, Golosova O, Fursov M. 2012. Unipro UGENE: a uniﬁed 28.08.17). bioinformatics toolkit. Bioinformatics 28(8):1166–1167. Suzuki M, Nakagawa Y, Harayama S, Yamamoto S. 2001. Olivares-Fuster O, et al. 2007. Host-speciﬁc association between Phylogenetic analysis and taxonomic study of marine Flavobacterium columnare genomovars and ﬁsh species. Syst Appl Cytophaga-like bacteria: proposal for Tenacibaculum gen. nov. Microbiol. 30(8):624–633. with Tenacibaculum maritimum comb.nov.and Tenacibaculum Olsen AB, et al. 2017. Multilocus sequence analysis reveals extensive ge- ovolyticum comb. nov., and description of Tenacibaculum meso- netic variety within Tenacibaculum spp. associated with ulcers in sea- philum sp.nov.and Tenacibaculum amylolyticum sp. nov. Int J farmed ﬁsh in Norway. Vet Microbiol. 205:39–45. Syst Evol Microbiol. 51(5):1639–1652. Olsen AB, et al. 2011. Tenacibaculum sp. associated with winter ulcers in Veith PD, et al. 2013. Protein substrates of a novel secretion system sea-reared Atlantic salmon Salmo salar. Dis Aquat Organ. are numerous in the Bacteroidetes phylum and have in common a 94(3):189–199. cleavable C-terminal secretion signal, extensive post-translational Perez-Pascual D, et al. 2017. The complete genome sequence of the ﬁsh modiﬁcation, and cell-surface attachment. J Proteome Res. pathogen Tenacibaculum maritimum provides insights into virulence 12(10):4449–4461. mechanisms. Front Microbiol. 8:1542. Vos M, Didelot X. 2009. A comparison of homologous recombination Pineiro-Vidal M, Carballas CG, Gomez-Barreiro O, Riaza A, Santos Y. rates in bacteria and archaea. ISME J. 3(2):199–208. 2008. Tenacibaculum soleae sp. nov., isolated from diseased sole Wakabayashi H, Hikida M, Masumura K. 1986. Flexibacter maritimus sp. (Solea senegalensis Kaup). Int J Syst Evol Microbiol. 58(Pt 4):881–885. nov., a pathogen of marine ﬁshes. Int J Syst Evol Microbiol. Pineiro-Vidal M, Gijon D, Zarza C, Santos Y. 2012. Tenacibaculum dicen- 36(3):396–398. trarchi sp. nov., a marine bacterium of the family Flavobacteriaceae Weinert LA, Welch JJ. 2017. Why might bacterial pathogens have small isolated from European sea bass. Int J Syst Evol Microbiol. 62(Pt genomes? Trends Ecol Evol. 32(12):936–947. 2):425–429. Xu Z-X, Yu P, Mu D-S, Liu Y, Du Z-J. 2017. Tenacibaculum agarivorans sp. Pin ~eiro-Vidal M, Riaza A, Santos Y. 2008. Tenacibaculum discolor sp. nov. nov., an agar-degrading bacterium isolated from marine alga Porphyra and Tenacibaculum gallaicum sp. nov., isolated from sole (Solea sen- yezoensis Ueda. Int J Syst Evol Microbiol. 67(12):5139–5143. egalensis)and turbot (Psetta maxima) culture systems. Int J Syst Evol Zerbino DR, Birney E. 2008. Velvet: algorithms for de novo short read Microbiol. 58(Pt 1):21–25. assembly using de Bruijn graphs. Genome Res. 18(5):821–829. Rahmati-Holasoo H, et al. 2016. First detection of koi herpesvirus from koi, Cyprinus carpio L. experiencing mass mortalities in Associate editor:Howard Ochman Genome Biol. Evol. 10(2):452–457 doi:10.1093/gbe/evy020 Advance Access publication January 19, 2018 457 Downloaded from https://academic.oup.com/gbe/article-abstract/10/2/452/4817510 by Ed 'DeepDyve' Gillespie user on 16 March 2018
Genome Biology and Evolution – Oxford University Press
Published: Feb 1, 2018
It’s your single place to instantly
discover and read the research
that matters to you.
Enjoy affordable access to
over 18 million articles from more than
15,000 peer-reviewed journals.
All for just $49/month
Query the DeepDyve database, plus search all of PubMed and Google Scholar seamlessly
Save any article or search result from DeepDyve, PubMed, and Google Scholar... all in one place.
Get unlimited, online access to over 18 million full-text articles from more than 15,000 scientific journals.
Read from thousands of the leading scholarly journals from SpringerNature, Elsevier, Wiley-Blackwell, Oxford University Press and more.
All the latest content is available, no embargo periods.
“Hi guys, I cannot tell you how much I love this resource. Incredible. I really believe you've hit the nail on the head with this site in regards to solving the research-purchase issue.”Daniel C.
“Whoa! It’s like Spotify but for academic articles.”@Phil_Robichaud
“I must say, @deepdyve is a fabulous solution to the independent researcher's problem of #access to #information.”@deepthiw
“My last article couldn't be possible without the platform @deepdyve that makes journal papers cheaper.”@JoseServera