The widespread presence of a family of fish virulence plasmids in Vibrio vulnificus stresses its relevance as a zoonotic pathogen linked to fish farms

Literature cited

• Oliver JD. The biology of Vibrio vulnificus. Microbiol Spectr. 2015 Jun 25;3(3):3.
   Web of Science ®Google Scholar
• Baker-Austin C, Trinanes J, Gonzalez-Escalona N, et al. Non-cholera vibrios: the microbial barometer of climate change. Trends Microbiol. 2017;25:76–84.
   PubMed Web of Science ®Google Scholar
• Ceccarelli D, Amaro C, Romalde JL, et al. Vibrio species. In: Michael P. Doyle, Francisco Diez-Gonzalez, Colin Hill, editors. Food microbiology. Washington, DC: ASM Press; 2019. p. 347–388.
   Google Scholar
• Amaro C, Fouz B, Sanjuán E, et al. Vibriosis. In: Patrick T K Woo, Jo-Ann Leong, Kurt Buchmann, editors. Climate change and infectious fish diseases. Wallingford: CABI; 2020. p. 182–210.
   Google Scholar
• Horseman MA, Surani S. A comprehensive review of Vibrio vulnificus: An important cause of severe sepsis and skin and soft-tissue infection. Int J Infect Dis. 2011;15:e157–66.
   PubMed Web of Science ®Google Scholar
• Dalsgaard A, Frimodt-Møller N, Bruun B, et al. Clinical manifestations and molecular epidemiology of Vibrio vulnificus infections in Denmark. Eur J Clin Microbiol Infect Dis. 1996;15(3):227–232.
   Web of Science ®Google Scholar
• Veenstra J, Rietra PJGM, Coster JM, et al. Human Vibrio vulnificus infections and environmental isolates in the Netherlands. Aquac Res. 1993 Jan;24(1):119–122.
   Google Scholar
• Tison DL, Nishibuchi M, Greenwood JD, et al. Vibrio vulnificus biogroup 2: new biogroup pathogenic for eels. Appl Environ Microbiol. 1982 Sep;44(3):640–646.
   PubMed Web of Science ®Google Scholar
• Bisharat N, Agmon V, Finkelstein R, et al. Clinical, epidemiological, and microbiological features of Vibrio vulnificus biogroup 3 causing outbreaks of wound infection and bacteraemia in Israel. Lancet. 1999 Oct;354(9188):1421–1424.
   Web of Science ®Google Scholar
• Amaro C, Biosca EG. Vibrio vulnificus biotype 2, pathogenic for eels, is also an opportunistic pathogen for humans. Appl Environ Microbiol. 1996 Apr;62(4):1454–1457.
   PubMed Web of Science ®Google Scholar
• Roig FJ, González-Candelas F, Sanjuán E, et al. Phylogeny of Vibrio vulnificus from the analysis of the core-genome: implications for intra-species taxonomy. Front Microbiol. 2018 Jan 5;8(JAN):1–13.
   Google Scholar
• Pajuelo D, Lee C-T, Roig FJ, et al. Novel host-specific iron acquisition system in the zoonotic pathogen Vibrio vulnificus. Environ Microbiol. 2015 Jun 1;17(6):2076–2089.
   Web of Science ®Google Scholar
• Hernández-Cabanyero C, Lee C, Tolosa-Enguis V, et al. Adaptation to host in Vibrio vulnificus, a zoonotic pathogen that causes septicemia in fish and humans. Environ Microbiol. 2019 Aug 11;21(8):3118–3139.
   Web of Science ®Google Scholar
• Te LC, Pajuelo D, Llorens A, et al. MARTX of Vibrio vulnificus biotype 2 is a virulence and survival factor. Environ Microbiol. 2013;15(2):419–432.
   Web of Science ®Google Scholar
• Jeong HG, Satchell KJF. Additive function of Vibrio vulnificus MARTXVv and VvhA cytolysins promotes rapid growth and epithelial tissue necrosis during intestinal infection. PLoS Pathog. 2012;8(3).
   Web of Science ®Google Scholar
• Roig FJ, Amaro C. Plasmid diversity in Vibrio vulnificus biotypes. Microbiology. 2009;155(2):489–497.
   Web of Science ®Google Scholar
• Efimov V, Danin-Poleg Y, Green SJ, et al. Draft genome sequence of the pathogenic bacterium Vibrio vulnificus V252 biotype 1, isolated in Israel. Genome Announc. 2015 Oct 29;3(5).
   Google Scholar
• Danin-Poleg Y, Raz N, Roig FJ, et al. Draft genome sequence of environmental bacterium Vibrio vulnificus CladeA-yb158. Genome Announc. 2015 Aug 27;3(4).
   Google Scholar
• Carmona-Salido H, Fouz B, Sanjuán E, et al. Draft genome sequences of Vibrio vulnificus strains recovered from moribund tilapia. Microbiol Resour Announc. 2021 Jun 3;10(22).
   Web of Science ®Google Scholar
• Hor L-I, Goo C-T, Wan L. Isolation and characterization of Vibrio vulnificus inhabiting the marine environment of the southwestern area of Taiwan. J Biomed Sci. 1995 Oct;2(4):384–389.
   Google Scholar
• Sanjuán E, Amaro C. Multiplex PCR assay for detection of Vibrio vulnificus biotype 2 and simultaneous discrimination of serovar E strains. Appl Environ Microbiol. 2007 Mar 15;73(6):2029–2032.
   Web of Science ®Google Scholar
• Roig FJ, Sanjuán E, Llorens A, et al. Pilf polymorphism-based PCR to distinguish Vibrio vulnificus strains potentially dangerous to public health. Appl Environ Microbiol. 2010 Mar 1;76(5):1328–1333.
   Web of Science ®Google Scholar
• Fouz B, Larsen JL, Amaro C. Vibrio vulnificus serovar A: an emerging pathogen in European anguilliculture. J Fish Dis. 2006 May;29(5):285–291.
   Web of Science ®Google Scholar
• Amaro C, Biosca EG, Fouz B, et al. Evidence that water transmits Vibrio vulnificus biotype 2 infections to eels. Appl Environ Microbiol. 1995;61(3):1133–1137.
   Web of Science ®Google Scholar
• Reed LJ, Muench H. A simple method of estimating fifty per cent endpoints. Am J Epidemiol. 1938 May 1;27(3):493–497.
   Google Scholar
• Fouz B, Alcaide E, Barrera R, et al. Susceptibility of Nile tilapia (oreochromis niloticus) to vibriosis due to Vibrio vulnificus biotype 2 (serovar E). Aquaculture. 2002 Sep 23;212(1–4):21–30.
   Web of Science ®Google Scholar
• Ewels P, Magnusson M, Lundin S, et al. MultiQC: summarize analysis results for multiple tools and samples in a single report. Bioinformatics. 2016 Oct 1;32(19):3047–3048.
   PubMed Web of Science ®Google Scholar
• Schmieder R, Edwards R. Quality control and preprocessing of metagenomic datasets. Bioinformatics. 2011 Mar 15;27(6):863–864.
   PubMed Web of Science ®Google Scholar
• De Coster W, D’Hert S, Schultz DT, et al. Nanopack: visualizing and processing long-read sequencing data. Berger B, editor. Bioinformatics. 2018 Aug 1;34(15):2666–2669.
   PubMed Web of Science ®Google Scholar
• Bankevich A, Nurk S, Antipov D, et al. SPAdes: A new genome assembly algorithm and its applications to single-Cell sequencing. J Comput Biol. 2012 May;19(5):455–477.
   PubMed Web of Science ®Google Scholar
• Wick RR, Judd LM, Gorrie CL, et al. Unicycler: resolving bacterial genome assemblies from short and long sequencing reads. Phillippy AM, editor. PLoS Comput Biol. 2017 Jun 8;13(6):e1005595.
   PubMed Web of Science ®Google Scholar
• Gurevich A, Saveliev V, Vyahhi N, et al. QUAST: quality assessment tool for genome assemblies. Bioinformatics. 2013 Apr 15;29(8):1072–1075.
   PubMed Web of Science ®Google Scholar
• Seemann T. Prokka: rapid prokaryotic genome annotation. Bioinformatics. 2014 Jul 15;30(14):2068–2069.
   PubMed Web of Science ®Google Scholar
• Lechner M, Findeiß S, Steiner L, et al. Proteinortho: detection of (Co-)orthologs in large-scale analysis. BMC Bioinformatics. 2011 Dec 28;12(1):124.
   PubMed Web of Science ®Google Scholar
• Roig FJ, González-Candelas F, Amaro C. Domain organization and evolution of multifunctional autoprocessing repeats-in-toxin (MARTX) toxin in Vibrio vulnificus. Appl Environ Microbiol. 2011 Jan 15;77(2):657–668.
   Web of Science ®Google Scholar
• Couvin D, Bernheim A, Toffano-Nioche C, et al. CRISPRCasfinder, an update of CRISRFinder, includes a portable version, enhanced performance and integrates search for Cas proteins. Nucleic Acids Res. 2018 Jul 2;46(W1):W246–51.
   PubMed Web of Science ®Google Scholar
• Biswas A, Gagnon JN, Brouns SJJ, et al. CRISPRTarget: bioinformatic prediction and analysis of crRNA targets. RNA Biol. 2013;10(5):817–827.
   PubMed Web of Science ®Google Scholar
• Sullivan MJ, Petty NK, Beatson SA. Easyfig: a genome comparison visualizer. Bioinformatics. 2011 Apr;27(7):1009–1010.
   PubMed Web of Science ®Google Scholar
• Moura A, Soares M, Pereira C, et al. INTEGRALL: a database and search engine for integrons, integrases and gene cassettes. Bioinformatics. 2009;25(8):1096–1098.
   PubMed Web of Science ®Google Scholar
• Arndt D, Grant JR, Marcu A, et al. PHASTER: a better, faster version of the PHAST phage search tool. Nucleic Acids Res. 2016 Jul 8;44(W1):W16–21.
   PubMed Web of Science ®Google Scholar
• Katoh K, Standley DM. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol. 2013 Apr 1;30(4):772–780.
   PubMed Web of Science ®Google Scholar
• Borowiec ML. AMAS: a fast tool for alignment manipulation and computing of summary statistics. PeerJ. 2016 Jan 28;4:e1660.
   PubMed Web of Science ®Google Scholar
• Nguyen L-T, Schmidt HA, von Haeseler A, et al. IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol Biol Evol. 2015 Jan;32(1):268–274.
   PubMed Web of Science ®Google Scholar
• Kalyaanamoorthy S, Minh BQ, Wong TKF, et al. Modelfinder: fast model selection for accurate phylogenetic estimates. Nat Methods. 2017:587–589.
   Web of Science ®Google Scholar
• Hoang DT, Chernomor O, von Haeseler A, et al. UFBoot2: improving the ultrafast bootstrap approximation. Mol Biol Evol. 2018 Feb 1;35(2):518–522.
   PubMed Web of Science ®Google Scholar
• Letunic I, Bork P. Interactive tree Of life (iTOL) v4: recent updates and new developments. Nucleic Acids Res. 2019 Jul 2;47(W1):W256–9.
   PubMed Web of Science ®Google Scholar
• Tamura K. Estimation of the number of nucleotide substitutions when there are strong transition-transversion and G + C-content biases. Mol Biol Evol. 1992 Jul;9(4):678–687.
   PubMed Web of Science ®Google Scholar
• Kumar S, Stecher G, Li M, et al. MEGA x: Molecular evolutionary genetics analysis across computing platforms. Battistuzzi FU, editor. Mol Biol Evol. 2018 Jun 1;35(6):1547–1549.
   PubMed Web of Science ®Google Scholar
• Lee C-T, Amaro C, Wu K-M, et al. A common virulence plasmid in biotype 2 Vibrio vulnificus and its dissemination aided by a conjugal plasmid. J Bacteriol. 2008 Mar 1;190(5):1638–1648.
   Web of Science ®Google Scholar
• Kim BS. The modes of action of MARTX toxin effector domains. Toxins (Basel. 2018 Dec 2;10(12):507.
   Web of Science ®Google Scholar
• Murciano C, Lee C-T, Fernández-Bravo A, et al. MARTX toxin in the zoonotic serovar of Vibrio vulnificus triggers an early cytokine storm in mice. Front Cell Infect Microbiol. 2017 Jul 20;7(JUL):332.
   Web of Science ®Google Scholar
• Makarova KS, Wolf YI, Alkhnbashi OS, et al. An updated evolutionary classification of CRISPR-Cas systems. Nat Rev Microbiol. 2015 Nov 1;13(11):722–736.
   PubMed Web of Science ®Google Scholar
• Makarova KS, Haft DH, Barrangou R, et al. Evolution and classification of the CRISPR–Cas systems. Nat Rev Microbiol. 2011 Jun 9;9(6):467–477.
   PubMed Web of Science ®Google Scholar
• Chung HY, Kim YT, Kim S, et al. Complete genome sequence of Vibrio vulnificus FORC-017 isolated from a patient with a hemorrhagic rash after consuming raw dotted gizzard shad. Gut Pathog. 2016 Jun 20;8(1):1–6.
   Web of Science ®Google Scholar
• Valiente E, Jiménez N, Merino S, et al. Vibrio vulnificus biotype 2 serovar E gne but not galE is essential for lipopolysaccharide biosynthesis and virulence. Infect Immun. 2008 Apr;76(4):1628–1638.
   Web of Science ®Google Scholar
• Kim BS, Satchell KJF. MARTX effector cross kingdom activation by Golgi-associated ADP-ribosylation factors. Cell Microbiol. 2016 Aug 1;18(8):1078–1093.
   Web of Science ®Google Scholar
• Kwak JS, Jeong HG, Satchell KJF. Vibrio vulnificus rtxA1 gene recombination generates toxin variants with altered potency during intestinal infection. Proc Natl Acad Sci U S A. 2011 Jan 25;108(4):1645–1650.
   Web of Science ®Google Scholar
• Ford MJ. Molecular evolution of transferrin: evidence for positive selection in salmonids. Mol Biol Evol. 2001 Apr 1;18(4):639–647.
   Web of Science ®Google Scholar