The pan-genome of Splendidus clade species in the family Vibrionaceae: Insights into evolution, adaptation, and pathogenicity.
Journal
Environmental microbiology
ISSN: 1462-2920
Titre abrégé: Environ Microbiol
Pays: England
ID NLM: 100883692
Informations de publication
Date de publication:
10 2022
10 2022
Historique:
received:
05
07
2022
accepted:
13
09
2022
pubmed:
16
9
2022
medline:
20
10
2022
entrez:
15
9
2022
Statut:
ppublish
Résumé
The Splendidus clade is the largest clade in Vibrionaceae, and its members are often related to mortality of marine animals with huge economic losses. The molecular bases of their pathogenicity and virulence, however, remain largely unknown. In particular, the complete genome sequences of the Splendidus clade species are rarely registered, which is one of the obstacles to predict core and/or unique genes responsible for their adaptation and pathogenicity, and to perform a fine scale meta-transcriptome during bacterial infection to their hosts. In this study, we obtained the complete genomes of all type strains in the Splendidus clade and revealed that (1) different genome sizes (4.4-5.9 Mb) with V. lentus the biggest and most of them had several big plasmids, likely because of the different features on mobilome elements; (2) the Splendidus clade consists of 19 species except V. cortegadensis, and 3 sub-clades (SC) were defined with the 15 most closely related members as SC1; (3) different carbohydrate degradation preferences may be the result of environmental adaptation; and (4) a broad prediction of virulence factors (VFs) revealed core and species unique VF genes.
Identifiants
pubmed: 36106979
doi: 10.1111/1462-2920.16209
doi:
Substances chimiques
Carbohydrates
0
Virulence Factors
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
4587-4606Informations de copyright
© 2022 Society for Applied Microbiology and John Wiley & Sons Ltd.
Références
Anonymous. (2001) Notification that new names and new combinations have appeared in volume 51, part 1, of the IJSEM. International Journal of Systematic and Evolutionary Microbiology, 51, 269.
Aramaki, T., Blanc-Mathieu, R., Endo, H., Ohkubo, K., Kanehisa, M., Goto, S. et al. (2020) KofamKOALA: KEGG Ortholog assignment based on profile HMM and adaptive score threshold. Bioinformatics, 36, 2251-2252.
Baumann, P., Baumann, L., Bang, S. & Woolkalis, M. (1980) Reevaluation of the taxonomy of Vibrio, Beneckea, and Photobacterium: abolition of the genus Beneckea. Current Microbiology, 4, 127-132.
Baumann, P., Baumann, L., & Mandel, M. (1971) Taxonomy of marine bacteria: the genus Beneckea. Journal of Bacteriology, 107, 68-294.
Beaz-Hidalgo, R., Diéguez, A.L., Cleenwerck, I., Balboa, S., Doce, A., de Vos, P. et al. (2010) Vibrio celticus sp. nov., a new Vibrio species belonging to the Splendidus clade with pathogenic potential for clams. Systematic and Applied Microbiology, 33, 311-315.
Beaz-Hidalgo, R., Doce, A., Pascual, J., Toranzo, A.E. & Romalde, J.L. (2009) Vibrio gallaecicus sp. nov. isolated from cultured clams in north-western Spain. Systematic and Applied Microbiology, 32, 111-117.
Bertelli, C., Laird, M.R., Williams, K.P., Lau, B.Y., Hoad, G., Winsor, G.L. et al. (2017) IslandViewer 4: expanded prediction of genomic islands for larger-scale datasets. Nucleic Acids Research, 45, W30-W35.
Beijerinck, N. W. (1900) On different forms of hereditary variation in microbes. Proc Acad Sci, 3, 35-365.
Binesse, J., Delsert, C., Saulnier, D., Champomier-Vergès, M.-C., Zagorec, M., Munier-Lehmann, H. et al. (2008) Metalloprotease Vsm is the major determinant of toxicity for extracellular products of Vibrio splendidus. Applied and Environmental Microbiology, 74, 7108-7117.
Bramhachari, P.V. & Dubey, S.K. (2006) Isolation and characterization of exopolysaccharide produced by Vibrio harveyi strain VB23. Letters in Applied Microbiology, 43, 571-577.
Bruto, M., Labreuche, Y., James, A., Piel, D., Chenivesse, S., Petton, B. et al. (2018) Ancestral gene acquisition as the key to virulence potential in environmental Vibrio populations. The ISME Journal, 12, 2954-2966.
Chen, L., Zheng, D., Liu, B., Yang, J. & Jin, Q. (2016) VFDB 2016: hierarchical and refined dataset for big data analysis-10 years on. Nucleic Acids Research, 44, D694-D697.
Craig, L., Pique, M.E. & Tainer, J.A. (2004) Type IV pilus structure and bacterial pathogenicity. Nature Reviews. Microbiology, 2, 363-378.
de Kievit, T.R. & Iglewski, B.H. (2000) Bacterial quorum sensing in pathogenic relationships. Infection and Immunity, 68, 4839-4849.
Defoirdt, T., Boon, N., Sorgeloos, P., Verstraete, W. & Bossier, P. (2008) Quorum sensing and quorum quenching in Vibrio harveyi: lessons learned from in vivo work. The ISME Journal, 2, 19-26.
Defoirdt, T., Bossier, P., Sorgeloos, P. & Verstraete, W. (2005) The impact of mutations in the quorum sensing systems of Aeromonas hydrophila, Vibrio anguillarum and Vibrio harveyi on their virulence towards gnotobiotically cultured Artemia franciscana. Environmental Microbiology, 7, 1239-1247.
Diéguez, A.L., Beaz-Hidalgo, R., Cleenwerck, I., Balboa, S., de Vos, P. & Romalde, J.L. (2011) Vibrio atlanticus sp. nov. and Vibrio artabrorum sp. nov., isolated from the clams Ruditapes philippinarum and Ruditapes decussatus. International Journal of Systematic and Evolutionary Microbiology, 61, 2406-2411.
Dobrindt, U., Hochhut, B., Hentschel, U. & Hacker, J. (2004) Genomic islands in pathogenic and environmental microorganisms. Nature Reviews. Microbiology, 2, 414-424.
Dubert, J., Barja, J.L. & Romalde, J.L. (2017) New insights into pathogenic Vibrios affecting bivalves in hatcheries: present and future prospects. Frontiers in Microbiology, 8, 762.
Edgar, R.C. (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research, 32, 1792-1797.
Enos-Berlage, J.L. & McCarter, L.L. (2000) Relation of capsular polysaccharide production and colonial cell organization to colony morphology in Vibrio parahaemolyticus. Journal of Bacteriology, 182, 5513-5520.
Eren, A.M., Esen, Ö.C., Quince, C., Vineis, J.H., Morrison, H.G., Sogin, M.L. et al. (2015) Anvi'o: an advanced analysis and visualization platform for 'omics data. PeerJ, 3, e1319.
Faury, N., Saulnier, D., Thompson, F.L., Gay, M., Swings, J. & Le Roux, F. (2004) Vibrio crassostreae sp. nov., isolated from the haemolymph of oysters (Crassostrea gigas). International Journal of Systematic and Evolutionary Microbiology, 54, 2137-2140.
Floyd, K.A., Lee, C.K., Xian, W., Nametalla, M., Valentine, A., Crair, B. et al. (2020) c-di-GMP modulates type IV MSHA pilus retraction and surface attachment in Vibrio cholerae. Nature Communications, 11, 1549.
Frans, I., Michiels, C.W., Bossier, P., Willems, K.A., Lievens, B. & Rediers, H. (2011) Vibrio anguillarum as a fish pathogen: virulence factors, diagnosis and prevention. Journal of Fish Diseases, 34, 643-661.
Frost, L.S., Leplae, R., Summers, A.O. & Toussaint, A. (2005) Mobile genetic elements: the agents of open source evolution. Nature Reviews. Microbiology, 3, 722-732.
Galperin, M.Y., Wolf, Y.I., Makarova, K.S., Vera Alvarez, R., Landsman, D. & Koonin, E.V. (2021) COG database update: focus on microbial diversity, model organisms, and widespread pathogens. Nucleic Acids Research, 49, D274-D281.
Giovannoni, S.J., Cameron Thrash, J. & Temperton, B. (2014) Implications of streamlining theory for microbial ecology. The ISME Journal, 8, 1553-1565.
Giovannoni, S.J., Tripp, H.J., Givan, S., Podar, M., Vergin, K.L., Baptista, D. et al. (2005) Genome streamlining in a cosmopolitan oceanic bacterium. Science (80-), 309, 1242-1245.
Gomez-Gil, B., Thompson, C.C., Matsumura, Y., Sawabe, T., Iida, T., Christen, R. et al. (2014) The famlily Vibrionaceae. In: The Prokaryotes. Berlin, Heidelberg: Springer Berlin Heidelberg, pp. 659-747.
Green, E.R. & Mecsas, J. (2016) Bacterial secretion systems: an overview. Microbiology Spectrum, 4, 13.
Gu, Z., Eils, R. & Schlesner, M. (2016) Complex heatmaps reveal patterns and correlations in multidimensional genomic data. Bioinformatics, 32, 2847-2849.
Haiko, J. & Westerlund-Wikström, B. (2013) The role of the bacterial flagellum in qdhesion and virulence. Biology (Basel), 2, 1242-1267.
Hedlund, B.P. & Staley, J.T. (2001) Vibrio cyclotrophicus sp. nov., a polycyclic aromatic hydrocarbon (PAH)-degrading marine bacterium. International Journal of Systematic and Evolutionary Microbiology, 51, 61-66.
Hehemann, J.-H., Arevalo, P., Datta, M.S., Yu, X., Corzett, C.H., Henschel, A. et al. (2016) Adaptive radiation by waves of gene transfer leads to fine-scale resource partitioning in marine microbes. Nature Communications, 7, 12860.
Hira, J., Bentdal, S., Devold, H., Stensvåg, K. & Landfald, B. (2019) Vibrio echinoideorum sp. nov., isolated from an epidermal lesion on the test of a green sea urchin (Strongylocentrotus droebachiensis). International Journal of Systematic and Evolutionary Microbiology, 69, 2277-2282.
Huang, J., Ma, J., Shang, K., Hu, X., Liang, Y., Li, D. et al. (2016) Evolution and diversity of the antimicrobial resistance associated mobilome in Streptococcus suis: a probable mobile genetic elements reservoir for other Streptococci. Frontiers in Cellular and Infection Microbiology, 6, 118.
Hunt, D.E., David, L.A., Gevers, D., Preheim, S.P., Alm, E.J. & Polz, M.F. (2008) Resource partitioning and sympatric differentiation among closely related bacterioplankton. Science (80-), 320, 1081-1085.
Hyatt, D., Chen, G.-L., LoCascio, P.F., Land, M.L., Larimer, F.W. & Hauser, L.J. (2010) Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinformatics, 11, 119.
Jiang, C., Tanaka, M., Nishikawa, S., Mino, S., Romalde, J.L., Thompson, F.L. et al. (2022) Vibrio clade 3.0: new Vibrionaceae evolutionary units using genome-based approach. Current Microbiology, 79, 1-15.
Johnson, T.L., Fong, J.C., Rule, C., Rogers, A., Yildiz, F.H. & Sandkvist, M. (2014) The type II secretion system delivers matrix proteins for biofilm formation by Vibrio cholerae. Journal of Bacteriology, 196, 4245-4252.
Kajitani, R., Yoshimura, D., Ogura, Y., Gotoh, Y., Hayashi, T. & Itoh, T. (2020) Platanus_B: an accurate de novo assembler for bacterial genomes using an iterative error-removal process. DNA Research, 27, dsaa014.
Kauffman, K.M., Chang, W.K., Brown, J.M., Hussain, F.A., Yang, J., Polz, M.F. et al. (2022) Resolving the structure of phage-bacteria interactions in the context of natural diversity. Nature Communications, 13, 372.
Kehlet-Delgado, H., Häse, C.C. & Mueller, R.S. (2020) Comparative genomic analysis of Vibrios yields insights into genes associated with virulence towards C. gigas larvae. BMC Genomics, 21, 599.
Kim, D., Baik, K.S., Hwang, Y.S., Choi, J.-S., Kwon, J. & Seong, C.N. (2013) Vibrio hemicentroti sp. nov., an alginate lyase-producing bacterium, isolated from the gut microflora of sea urchin (Hemicentrotus pulcherrimus). International Journal of Systematic and Evolutionary Microbiology, 63, 3697-3703.
Kolmogorov, M., Yuan, J., Lin, Y. & Pevzner, P.A. (2019) Assembly of long, error-prone reads using repeat graphs. Nature Biotechnology, 37, 540-546.
Koren, S., Walenz, B.P., Berlin, K., Miller, J.R., Bergman, N.H. & Phillippy, A.M. (2017) Canu: scalable and accurate long-read assembly via adaptive k-mer weighting and repeat separation. Genome Research, 27, 722-736.
Kumar, S., Stecher, G., Li, M., Knyaz, C. & Tamura, K. (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Molecular Biology and Evolution, 35, 1547-1549.
Lasa, A., Diéguez, A.L. & Romalde, J.L. (2013) Vibrio toranzoniae sp. nov., a new member of the Splendidus clade in the genus Vibrio. Systematic and Applied Microbiology, 36, 96-100.
Lasa, A., Diéguez, A.L. & Romalde, J.L. (2014) Vibrio cortegadensis sp. nov., isolated from clams. Antonie Van Leeuwenhoek, 105, 335-341.
Lasa, A., Gibas, C.J. & Romalde, J.L. (2017) Comparative genomic analysis of two Vibrio toranzoniae strains with different virulence capacity reveals clues on its pathogenicity for fish. Frontiers in Microbiology, 8, 86.
Le Roux, F., Goubet, A., Thompson, F.L., Faury, N., Gay, M., Swings, J. et al. (2005) Vibrio gigantis sp. nov., isolated from the haemolymph of cultured oysters (Crassostrea gigas). International Journal of Systematic and Evolutionary Microbiology, 55, 2251-2255.
Le Roux, F., Zouine, M., Chakroun, N., Binesse, J., Saulnier, D., Bouchier, C. et al. (2009) Genome sequence of Vibrio splendidus: an abundant planctonic marine species with a large genotypic diversity. Environmental Microbiology, 11, 1959-1970.
Lee, I., Ouk Kim, Y., Park, S.-C. & Chun, J. (2016) OrthoANI: an improved algorithm and software for calculating average nucleotide identity. International Journal of Systematic and Evolutionary Microbiology, 66, 1100-1103.
Lee, K.-J., Kim, J.-A., Hwang, W., Park, S.-J. & Lee, K.-H. (2013) Role of capsular polysaccharide (CPS) in biofilm formation and regulation of CPS production by quorum-sensing in Vibrio vulnificus. Molecular Microbiology, 90, 841-857.
Lemire, A., Goudenège, D., Versigny, T., Petton, B., Calteau, A., Labreuche, Y. et al. (2015) Populations, not clones, are the unit of vibrio pathogenesis in naturally infected oysters. The ISME Journal, 9, 1523-1531.
Li, C., Pan, D., Li, M., Wang, Y., Song, L., Yu, D. et al. (2021) Aerobactin-mediated iron acquisition enhances biofilm formation, oxidative stress resistance, and virulence of Yersinia pseudotuberculosis. Frontiers in Microbiology, 12, 699913.
Li, J., Lim, M.S., Li, S., Brock, M., Pique, M.E., Woods, V.L. et al. (2008) Vibrio cholerae toxin-coregulated pilus structure analyzed by hydrogen/deuterium exchange mass spectrometry. Structure, 16, 137-148.
Li, Y. & Ma, Q. (2017) Iron acquisition strategies of Vibrio anguillarum. Frontiers in Cellular and Infection Microbiology, 7, 342.
Liang, W., Zhang, C., Liu, N., Zhang, W., Han, Q. & Li, C. (2016) Cloning and characterization of Vshppd, a gene inducing haemolysis and immune response of Apostichopus japonicus. Aquaculture, 464, 246-252.
Liang, W., Zhang, W. & Li, C. (2022) Vibrio splendidus virulence to Apostichopus japonicus is mediated by hppD through glutamate metabolism and flagellum assembly. Virulence, 13, 458-470.
Liu, B., Zheng, D., Jin, Q., Chen, L. & Yang, J. (2019) VFDB 2019: a comparative pathogenomic platform with an interactive web interface. Nucleic Acids Research, 47, D687-D692.
Liu, R., Chen, H., Zhang, R., Zhou, Z., Hou, Z., Gao, D. et al. (2016) Comparative transcriptome analysis of Vibrio splendidus JZ6 reveals the mechanism of its pathogenicity at low temperatures. Applied and Environmental Microbiology, 82, 2050-2061.
Lucena, T., Carmen Macián, M., Arahal, D.R., Rodrigo-Torres, L. & Pujalte, M.J. (2017) Whole genome sequences reveal Vibrio hemicentroti Kim et al. 2013 as a later heterotypic synonym of Vibrio splendidus (Beijerinck 1900) Baumann et al. 1981. International Journal of Systematic and Evolutionary Microbiology, 67, 1669-1671.
Luo, H., Thompson, L.R., Stingl, U. & Hughes, A.L. (2015) Selection maintains low genomic GC content in marine SAR11 lineages. Molecular Biology and Evolution, 32, 2738-2748.
Macián, M.C., Ludwig, W., Aznar, R., Grimont, P.A., Schleifer, K.H., Garay, E. et al. (2001) Vibrio lentus sp. nov., isolated from Mediterranean oysters. International Journal of Systematic and Evolutionary Microbiology, 51, 1449-1456.
Matilla, M.A. & Krell, T. (2018) The effect of bacterial chemotaxis on host infection and pathogenicity. FEMS Microbiology Reviews, 42, fux052.
Meier-Kolthoff, J.P., Auch, A.F., Klenk, H.-P. & Göker, M. (2013) Genome sequence-based species delimitation with confidence intervals and improved distance functions. BMC Bioinformatics, 14, 60.
Milton, D.L. (2006) Quorum sensing in vibrios: complexity for diversification. International Journal of Medical Microbiology, 296, 61-71.
Morais, V., Dee, V. & Suárez, N. (2018) Purification of capsular polysaccharides of Streptococcus pneumoniae: traditional and new methods. Frontiers in Bioengineering and Biotechnology, 6, 145.
Muralidharan, J. & Jayachandran, S. (2003) Physicochemical analyses of the exopolysaccharides produced by a marine biofouling bacterium, Vibrio alginolyticus. Process Biochemistry, 38, 841-847.
Nasfi, H., Travers, M.A., de Lorgeril, J., Habib, C., Sannie, T., Sorieul, L. et al. (2015) A European epidemiological survey of Vibrio splendidus clade shows unexplored diversity and massive exchange of virulence factors. World Journal of Microbiology and Biotechnology, 31, 461-475.
Nei, M. & Kumar, S. (2000) Molecular evolution and phylogenetics. New York: Oxford University Press.
Oyanedel, D., Labreuche, Y., Bruto, M., Amraoui, H., Robino, E., Haffner, P. et al. (2020) Vibrio splendidus O-antigen structure: a trade-off between virulence to oysters and resistance to grazers. Environmental Microbiology, 22, 4264-4278.
Pacinelli, E., Wang, L. & Reeves, P.R. (2002) Relationship of Yersinia pseudotuberculosis O antigens IA, IIA, and IVB: the IIA gene cluster was derived from that of IVB. Infection and Immunity, 70, 3271-3276.
Parks, D.H., Imelfort, M., Skennerton, C.T., Hugenholtz, P. & Tyson, G.W. (2015) CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes. Genome Research, 25, 1043-1055.
Parte, A.C., Sardà Carbasse, J., Meier-Kolthoff, J.P., Reimer, L.C. & Göker, M. (2020) List of prokaryotic names with standing in nomenclature (LPSN) moves to the DSMZ. International Journal of Systematic and Evolutionary Microbiology, 70, 5607-5612.
Payne, S.M., Mey, A.R. & Wyckoff, E.E. (2016) Vibrio iron transport: evolutionary adaptation to life in multiple environments. Microbiology and Molecular Biology Reviews, 80, 69-90.
Pérez-Cataluña, A., Lucena, T., Tarazona, E., Arahal, D.R., Macián, M.C. & Pujalte, M.J. (2016) An MLSA approach for the taxonomic update of the Splendidus clade, a lineage containing several fish and shellfish pathogenic Vibrio spp. Systematic and Applied Microbiology, 39, 361-369.
Poli, A., Romano, I., Mastascusa, V., Buono, L., Orlando, P., Nicolaus, B. et al. (2018) Vibrio coralliirubri sp. nov., a new species isolated from mucus of red coral (Corallium rubrum) collected at Procida Island, Italy. Antonie Van Leeuwenhoek, 111, 1105-1115.
Pritchard, L., Glover, R.H., Humphris, S., Elphinstone, J.G. & Toth, I.K. (2016) Genomics and taxonomy in diagnostics for food security: soft-rotting enterobacterial plant pathogens. Analytical Methods, 8, 12-24.
Rasmussen-Ivey, C.R., Figueras, M.J., McGarey, D. & Liles, M.R. (2016) Virulence factors of Aeromonas hydrophila: in the wake of reclassification. Frontiers in Microbiology, 7, 1337.
Rodriguez-R, L.M. & Konstantinidis, K.T. (2016) The enveomics collection: a toolbox for specialized analyses of microbial genomes and metagenomes. PeerJ Preprints, 4, e1900v1.
Romalde, J.L., Dieguez, A.L., Lasa, A. & Balboa, S. (2014) New Vibrio species associated to molluscan microbiota: a review. Frontiers in Microbiology, 4, 413.
Rubio, T., Oyanedel, D., Labreuche, Y., Toulza, E., Luo, X., Bruto, M. et al. (2019) Species-specific mechanisms of cytotoxicity toward immune cells determine the successful outcome of Vibrio infections. Proceedings of the National Academy of Sciences, 116, 14238-14247.
Sandkvist, M. (2001) Type II secretion and pathogenesis. Infection and Immunity, 69, 3523-3535.
Sarkar, P., Issac, P.K., Raju, S.V., Elumalai, P., Arshad, A. & Arockiaraj, J. (2021) Pathogenic bacterial toxins and virulence influences in cultivable fish. Aquaculture Research, 52, 2361-2376.
Saulnier, D., De Decker, S., Haffner, P., Cobret, L., Robert, M. & Garcia, C. (2010) A large-scale epidemiological study to identify bacteria pathogenic to pacific oyster Crassostrea gigas and correlation between virulence and metalloprotease-like activity. Microbial Ecology, 59, 787-798.
Sawabe, T., Kita-Tsukamoto, K. & Thompson, F.L. (2007) Inferring the evolutionary history of vibrios by means of multilocus sequence analysis. Journal of Bacteriology, 189, 7932-7936.
Sawabe, T., Koizumi, S., Fukui, Y., Nakagawa, S., Ivanova, E.P., Kita-Tsukamoto, K. et al. (2009) Mutation is the main driving force in the diversification of the Vibrio splendidus clade. Microbes and Environments, 24, 281-285.
Sawabe, T., Ogura, Y., Matsumura, Y., Feng, G., Amin, A.R., Mino, S. et al. (2013) Updating the Vibrio clades defined by multilocus sequence phylogeny: proposal of eight new clades, and the description of Vibrio tritonius sp. nov. Frontiers in Microbiology, 4, 414.
Schultz-Hauser, G., Köster, W., Schwarz, H. & Braun, V. (1992) Iron(III) hydroxamate transport in Escherichia coli K-12: FhuB-mediated membrane association of the FhuC protein and negative complementation of fhuC mutants. Journal of Bacteriology, 174, 2305-2311.
Shin, S.-H. (2021) Regulation of iron-uptake systems in Vibrio vulnificus, a ferrophilic bacterium. Medical Biological Science and Engineering, 4, 69-82.
Sikora, A.E. (2013) Proteins secreted via the type II secretion system: smart strategies of Vibrio cholerae to maintain fitness in different ecological niches. PLoS Pathogens, 9, e1003126.
Song, Y.C., Jin, S., Louie, H., Ng, D., Lau, R., Zhang, Y. et al. (2004) FlaC, a protein of Campylobacter jejuni TGH9011 (ATCC43431) secreted through the flagellar apparatus, binds epithelial cells and influences cell invasion. Molecular Microbiology, 53, 541-553.
Stothard, P. & Wishart, D.S. (2005) Circular genome visualization and exploration using CGView. Bioinformatics, 21, 537-539.
Sun, J., Li, X., Qiu, Y., Xue, X., Zhang, M., Yang, W. et al. (2022) Quorum sensing regulates transcription of the pilin gene mshA1 of MSHA pilus in Vibrio parahaemolyticus. Gene, 807, 145961.
Tait, K., Hutchison, Z., Thompson, F.L. & Munn, C.B. (2010) Quorum sensing signal production and inhibition by coral-associated vibrios. Environmental Microbiology Reports, 2, 145-150.
Tanizawa, Y., Fujisawa, T. & Nakamura, Y. (2018) DFAST: a flexible prokaryotic genome annotation pipeline for faster genome publication. Bioinformatics, 34, 1037-1039.
Terashima, H., Kojima, S. & Homma, M. (2008) Chapter 2 flagellar motility in bacteria: structure and function of flagellar motor. International Review of Cell and Molecular Biology, 270, 39-85.
Thompson, F.L., Hoste, B., Vandemeulebroecke, K. & Swings, J. (2001) Genomic diversity amongst Vibrio isolates from different sources determined by fluorescent amplified fragment length polymorphism. Systematic and Applied Microbiology, 24, 520-538.
Thompson, F.L., Iida, T. & Swings, J. (2004) Biodiversity of Vibrios. Microbiology and Molecular Biology Reviews, 68, 403-431.
Thompson, F.L., Thompson, C.C., Hoste, B., Vandemeulebroecke, K., Gullian, M. & Swings, J. (2003) Vibrio fortis sp. nov. and Vibrio hepatarius sp. nov., isolated from aquatic animals and the marine environment. International Journal of Systematic and Evolutionary Microbiology, 53, 1495-1501.
Thompson, F.L., Thompson, C.C., Li, Y., Gomez-Gil, B., Vandenberghe, J., Hoste, B. et al. (2003) Vibrio kanaloae sp. nov., Vibrio pomeroyi sp. nov. and Vibrio chagasii sp. nov., from sea water and marine animals. International Journal of Systematic and Evolutionary Microbiology, 53, 753-759.
Thompson, F.L., Thompson, C.C. & Swings, J. (2003) Vibrio tasmaniensis sp. nov., isolated from Atlantic Salmon (Salmo salar L.). Systematic and Applied Microbiology, 26, 65-69.
Thompson, J.R., Pacocha, S., Pharino, C., Klepac-Ceraj, V., Hunt, D.E., Benoit, J. et al. (2005) Genotypic diversity within a natural coastal bacterioplankton population. Science (80-), 307, 1311-1313.
Vale, F.F., Lehours, P. & Yamaoka, Y. (2022) Editorial: the role of mobile genetic elements in bacterial evolution and their adaptability. Frontiers in Microbiology, 13, 849667.
Van Dongen, S. & Abreu-Goodger, C. (2012) Using MCL to extract clusters from networks. Methods in Molecular Biology, 804, 281-295.
Vaser, R., Sović, I., Nagarajan, N. & Šikić, M. (2017) Fast and accurate de novo genome assembly from long uncorrected reads. Genome Research, 27, 737-746.
Walker, B.J., Abeel, T., Shea, T., Priest, M., Abouelliel, A., Sakthikumar, S. et al. (2014) Pilon: an integrated tool for comprehensive microbial variant detection and genome assembly improvement. PLoS One, 9, e112963.
Watnick, P.I., Fullner, K.J. & Kolter, R. (1999) A role for the mannose-sensitive hemagglutinin in biofilm formation by Vibrio cholerae El Tor. Journal of Bacteriology, 181, 3606-3609.
Whitehead, N.A., Barnard, A.M.L., Slater, H., Simpson, N.J.L. & Salmond, G.P.C. (2001) Quorum-sensing in gram-negative bacteria. FEMS Microbiology Reviews, 25, 365-404.
Wick, R.R., Judd, L.M., Gorrie, C.L. & Holt, K.E. (2017) Unicycler: resolving bacterial genome assemblies from short and long sequencing reads. PLoS Computational Biology, 13, e1005595.
Winzer, K. & Williams, P. (2001) Quorum sensing and the regulation of virulence gene expression in pathogenic bacteria. International Journal of Medical Microbiology, 291, 131-143.
Yang, Q., Han, Y. & Zhang, X.-H. (2011) Detection of quorum sensing signal molecules in the family Vibrionaceae. Journal of Applied Microbiology, 110, 1438-1448.
Zampini, M., Canesi, L., Betti, M., Ciacci, C., Tarsi, R., Gallo, G. et al. (2003) Role for mannose-sensitive hemagglutinin in promoting interactions between Vibrio cholerae El Tor and mussel hemolymph. Applied and Environmental Microbiology, 69, 5711-5715.
Zhang, C., Liang, W., Zhang, W. & Li, C. (2016) Characterization of a metalloprotease involved in Vibrio splendidus infection in the sea cucumber, Apostichopus japonicus. Microbial Pathogenesis, 101, 96-103.
Zhang, N.-X., Zhang, D.-C. & Qiao, N.-H. (2019) Vibrio profundi sp. nov., isolated from a deep-sea seamount. Antonie Van Leeuwenhoek, 112, 1603-1610.
Zhang, W. & Li, C. (2021) Virulence mechanisms of vibrios belonging to the Splendidus clade as aquaculture pathogens, from case studies and genome data. Reviews in Aquaculture, 13, 2004-2026.
Zhang, X.H., He, X. & Austin, B. (2020) Vibrio harveyi: a serious pathogen of fish and invertebrates in mariculture. Marine Life Science & Technology, 2, 231-245.
Zhao, Z., Liu, J., Deng, Y., Huang, W., Ren, C., Call, D.R. et al. (2018) The Vibrio alginolyticus T3SS effectors, Val1686 and Val1680, induce cell rounding, apoptosis and lysis of fish epithelial cells. Virulence, 9, 318-330.