CoChat
Sign Up
Cited by 68Vibrio bacteria research studiesGenomics and Phylogenetic StudiesEnterobacteriaceae and Cronobacter Research

Pyrosequencing-based comparative genome analysis of Vibrio vulnificus environmental isolates

Open access
Morrison, Shatavia S., Williams, Tiffany, Cain, Aurora, Froelich, Brett, Taylor, Casey, Baker-Austin, Craig, Verner-Jeffreys, David, Hartnell, Rachel +2 more·2012·PLoS ONE
DOI 10.1371/journal.pone.0037553PMC PMC3360785
Open this paper in CoChat — free accountOpen PDF

Abstract

Between 1996 and 2006, the US Centers for Disease Control reported that the only category of food-borne infections increasing in frequency were those caused by members of the genus Vibrio. The gram-negative bacterium Vibrio vulnificus is a ubiquitous inhabitant of estuarine waters, and is the number one cause of seafood-related deaths in the US. Many V. vulnificus isolates have been studied, and it has been shown that two genetically distinct subtypes, distinguished by 16S rDNA and other gene polymorphisms, are associated predominantly with either environmental or clinical isolation. While local genetic differences between the subtypes have been probed, only the genomes of clinical isolates have so far been completely sequenced. In order to better understand V. vulnificus as an agent of disease and to identify the molecular components of its virulence mechanisms, we have completed whole genome shotgun sequencing of three diverse environmental genotypes using a pyrosequencing approach. V. vulnificus strain JY1305 was sequenced to a depth of 33×, and strains E64MW and JY1701 were sequenced to lesser depth, covering approximately 99.9% of each genome. We have performed a comparative analysis of these sequences against the previously published sequences of three V. vulnificus clinical isolates. We find that the genome of V. vulnificus is dynamic, with 1.27% of genes in the C-genotype genomes not found in the E- genotype genomes. We identified key genes that differentiate between the genomes of the clinical and environmental genotypes. 167 genes were found to be specifically associated with environmental genotypes and 278 genes with clinical genotypes. Genes specific to the clinical strains include components of sialic acid catabolism, mannitol fermentation, and a component of a Type IV secretory pathway VirB4, as well as several other genes with potential significance for human virulence. Genes specific to environmental strains included several that may have implications for the balance between self-preservation under stress and nutritional competence.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1371/journal.pone.0037553

Cites

1 of 1 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • The ary gene is associated with virulence of clinical strains by providing sulfur within the host, thus providing an immune evasion approach.

    “The ary gene has been demonstrated to be associated with virulence of clinical strains by providing a pathogen with sulfur within the host, thus providing an immune evasion approach (Morrison et al., 2012).”

    From <i>Vibrio vulnificus</i>in aquariums is a novel threat to marine mammals and public health (2018) · cites this paper as Morrison et al., 2012

    The Results and Discussion section, under “Arylsulfatases” (page unavailable), reports that an arylsulfatase gene cluster distinguishes clinical C-genotype from environmental E-genotype strains and that the enzymes release sulfate. It suggests the cluster may aid survival in the sulfur-limited human gut, but does not demonstrate that it causes virulence or describe immune evasion. (LLM, conf=0.89)

    Experimental — accuracy not yet measured

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

Flagged first, then by citations

Research works printed but not linked: 74

  1. [1]Jones MK Oliver JD 2009 Vibrio vulnificus: disease and pathogenesis. Infect Immun 77 1723 1733 19255188 PMC2681776
  2. [2]Oliver JD 2006 Vibrio vulnificus. Belkin S Colwell RR Oceans and Health: Pathogens in the Marine Environment New York Springer Science 253 276
  3. [3]Merkel SM Alexander S Oliver JD Huet-Hudson YM 2001 Essential role for estrogen in protection against Vibrio vulnificus induced endotoxic shock. Infect Immun 69 6119 6122 11553550 PMC98741
  4. [4]Varki A 1993 Biological roles of oligosaccharides: all of the theories are correct. Glycobiology 3 97 130 8490246 PMC7108619
  5. [5]Starks AM Schoeb TR Tamplin ML Parveen S Doyle TJ 2000 Pathogenesis of infection by clinical and environmental strains of Vibrio vulnificus in iron-dextran-treated mice. Infect Immun 68 5785 5793 10992486 PMC101538
  6. [6]Aznar R Ludwig W Amann RI Schleifer KH 1994 Sequence determination of rRNA genes of pathogenic Vibrio species and whole-cell identification of Vibrio vulnificus with rRNA-targeted oligonucleotide probes. Int J Syst Bacteriol 44 330 337 8186099
  7. [7]Nilsson WB Paranjype RN DePaola A Strom MS 2003 Sequence polymorphism of the 16S rRNA gene of Vibrio vulnificus is a possible indicator of strain virulence. J Clin Microbiol 41 442 446 12517889 PMC149629
  8. [8]Gutacker M Conza N Benagli C Pedroli A Bernasconi MV 2003 Population genetics of Vibrio vulnificus: identification of two divisions and a distinct eel-pathogenic clone. Appl Environ Microbiol 69 3203 3212 12788717 PMC161503
  9. [9]Okura M Osawa R Iguchi A Takagi M Arakawa E 2004 PCR-based identification of pandemic group Vibrio parahaemolyticus with a novel group-specific primer pair. Microbiol Immunol 48 787 790 15502414
  10. [10]Warner JM Oliver JD 1998 Randomly amplified polymorphic DNA analysis of starved and viable but nonculturable Vibrio vulnificus cells. Appl Environ Microbiol 64 3025 3028 9687468 PMC106810
  11. [11]Rosche TM Yano Y Oliver JD 2005 A rapid and simple PCR analysis indicates there are two subgroups of Vibrio vulnificus which correlate with clinical or environmental isolation. Microbiol Immunol 49 381 389 15840964
  12. [12]Warner E Oliver JD 2008 Population structures of two genotypes of Vibrio vulnificus in oysters (Crassostrea virginica) and seawater. Appl Environ Microbiol 74 80 85 17993556 PMC2223226
  13. [13]Baker-Austin C Gore A Oliver JD Rangdale R McArthur JV 2010 Rapid in situ detection of virulent Vibrio vulnificus strains in raw oyster matrices using real-time PCR. Environmental Microbiology Reports 2 76 80 23766001
  14. [14]Cohen AL Oliver JD DePaola A Feil EJ Boyd EF 2007 Emergence of a virulent clade of Vibrio vulnificus and correlation with the presence of a 33-kilobase genomic island. Appl Environ Microbiol 73 5553 5565 17616611 PMC2042058
  15. [15]Chen CY Wu KM Chang YC Chang CH Tsai HC 2003 Comparative genome analysis of Vibrio vulnificus, a marine pathogen. Genome Res 13 2577 2587 14656965 PMC403799
  16. [16]Kim YR Lee SE Kim CM Kim SY Shin EK 2003 Characterization and pathogenic significance of Vibrio vulnificus antigens preferentially expressed in septicemic patients. Infect Immun 71 5461 5471 14500463 PMC201039
  17. [17]Park JH Cho YJ Chun J Seok YJ Lee JK 2011 Complete genome sequence of Vibrio vulnificus MO6-24/O. J Bacteriol 193 2062 2063 21317338 PMC3133017
  18. [18]Gulig PA de Crecy-Lagard V Wright AC Walts B Telonis-Scott M 2010 SOLiD sequencing of four Vibrio vulnificus genomes enables comparative genomic analysis and identification of candidate clade-specific virulence genes. BMC Genomics 11 512 20863407 PMC3091676
  19. [19]Chevreux B Wetter T Suhai S 1999 Genome Sequence Assembly Using Trace Signals and Additional Sequence Information. 45 56 In Proceedings of German Conference on Bioinformatics
  20. [20]Li J Jiang J Leung F 2011 6–10× pyrosequencing is a practical approach for whole prokaryote genome studies. Gene 494 1 57 64 22192914
  21. [21]Stothard P Wishart DS Circular genome visualization and exploration using CGView. Bioinformatics 21 537 539 15479716
  22. [22]Kim HU Kim SY Jeong H Kim TY Kim JJ 2011 Integrative genome-scale metabolic analysis of Vibrio vulnificus for drug targeting and discovery. Mol Syst Biol 7 460 21245845 PMC3049409
  23. [23]Darling AE Mau B Perna NT progressiveMauve: multiple genome alignment with gene gain, loss and rearrangement. PLoS One 5 e11147 PMC2892488 20593022
  24. [24]Senoh M Miyoshi S Okamoto K Fouz B Amaro C 2005 The cytotoxin-hemolysin genes of human and eel pathogenic Vibrio vulnificus strains: comparison of nucleotide sequences and application to the genetic grouping. Microbiol Immunol 2005 513 519 15965298
  25. [25]Drake SL Whitney B Levine JF DePaola A Jaykus LA 2010 Correlation of mannitol fermentation with virulence-associated genotypic characteristics in Vibrio vulnificus isolates from oysters and water samples in the Gulf of Mexico. Foodborne Pathog Dis 7 97 101 19785540
  26. [26]Kachlany SC Planet PJ DeSalle R Fine DH Figurski DH 2001 Genes for tight adherence of Actinobacillus actinomycetemcomitans: from plaque to plague to pond scum. Trends Microbiol 9 429 437 11553455
  27. [27]Rosche TM Binder EA Oliver JD 2010 Vibrio vulnificus genome suggest two distinct ecotypes. Environmental Microbiology Reports 2 128 132 23766007
  28. [28]Ashburner M Ball CA Blake JA Botstein D Butler H 2000 Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat Genet 25 25 29 10802651 PMC3037419
  29. [29]Harris MA Clark J Ireland A Lomax J Ashburner M 2004 The Gene Ontology (GO) database and informatics resource. Nucleic Acids Res 32 D258 261 14681407 PMC308770
  30. [30]Bauer S Gagneur J Robinson PN 2010 GOing Bayesian: model-based gene set analysis of genome-scale data. Nucleic Acids Res 38 3523 3532 20172960 PMC2887944
  31. [31]Cain AA Kosara R Gibas CJ 2012 GenoSets: Visual Analytic Methods for Comparative Genomics PLoS One in review PMC3463605 23056299
  32. [32]King T Ishihama A Kori A Ferenci T 2004 A regulatory trade-off as a source of strain variation in the species Escherichia coli. J Bacteriol 186 5614 5620 15317765 PMC516835
  33. [33]Ferenci T 2005 Maintaining a healthy SPANC balance through regulatory and mutational adaptation. Mol Microbiol 57 1 8 15948944
  34. [34]Dryselius R Kurokawa K Iida T 2007 Vibrionaceae, a versatile bacterial family with evoluntionarily conserved variability. Research in Microbiology 158 479 486 17590316
  35. [36]Orikoshi H Nakayama S Hanato C Miyamoto K Tsujibo H 2005 Role of the N-terminal polycystic kidney disease domain in chitin degradation by chitinase A from a marine bacterium, Alteromonas sp. strain O-7. J Appl Microbiol 99 551 557 16108796
  36. [37]Grimes DJ Johnson CN Dillon KS Flowers AR Noriea NF 3rd 2009 What genomic sequence information has revealed about Vibrio ecology in the ocean–a review. Microb Ecol 58 447 460 19727929
  37. [38]Meibom KL Blokesch M Dolganov NA Wu CY Schoolnik GK 2005 Chitin induces natural competence in Vibrio cholerae. Science 310 1824 1827 16357262
  38. [39]Hülsmann A Rosche TM Kong I -S Hassan HM Beam DM Oliver JD 2003 RpoS-Dependent Stress Response and Exoenzyme Production in Vibrio vulnificus. Appl Environ Microbiol 69 6114 6120 14532069 PMC201245
  39. [40]Bogard R Oliver JD 2007 Role of Iron in Human Serum Resistance of the Clinical and Environmental Vibrio vulnificus genotypes. Appl Environ Microbiol 73 7501 7505 17933938 PMC2168077
  40. [44]Hoffman JA Badger JL Zhang Y Huang SH Kim KS 2000 Escherichia coli K1 aslA contributes to invasion of brain microvascular endothelial cells in vitro and in vivo. Infect Immun 68 5062 5067 10948126 PMC101739
  41. [45]Smith AJ Greenman J Embery G 1997 Detection and possible biological role of chondroitinase and heparitinase enzymes produced by Porphyromonas gingivalis W50. J Periodontal Res 32 1 8 9085237
  42. [46]Kim DE Kim KH Bae YJ Lee JH Jang YH 2005 Purification and characterization of the recombinant arylsulfatase cloned from Pseudoalteromonas carrageenovora. Protein Expr Purif 39 107 115 15596366
  43. [47]Sperandio V Torres AG Jarvis B Nataro JP Kaper JB 2003 Bacteria-host communication: the language of hormones. Proc Natl Acad Sci U S A 100 8951 8956 12847292 PMC166419
  44. [48]Angata T Varki A 2002 Chemical diversity in the sialic acids and related alpha-keto acids: an evolutionary perspective. Chem Rev 102 439 469 11841250
  45. [49]Wiggins R Hicks SJ Soothill PW Millar MR Corfield AP 2001 Mucinases and sialidases: their role in the pathogenesis of sexually transmitted infections in the female genital tract. Sex Transm Infect 77 402 408 11714935 PMC1744407
  46. [50]Jeong HG Oh MH Kim BS Lee MY Han HJ 2009 The Capability of Catabolic Utilization of N-Acetylneuraminic Acid, a Sialic Acid, Is Essential for Vibrio vulnificus pathogenesis. Infection and Immunity 77 3209 3217 19487477 PMC2715665
  47. [51]Vimr ER Troy FA 1985 Identification of an inducible catabolic system for sialic acids (nan) in Escherichia coli. J Bacteriol 164 845 853 3902799 PMC214328
  48. [52]Almagro-Moreno S Boyd EF 2009 Insights into the evolution of sialic acid catabolism among bacteria. BMC Evolutionary Biology 9 118 19470179 PMC2693436
  49. [53]Lubin JB Boyd EF 2010 Ability of catabolize sialic acid is present predominately in clinical isolates of Vibrio vulnificus. Proceedings of Vibrio 2010 conference
  50. [54]Murray JW Delumeau O Lewis RJ 2005 Structure of nonheme globin in environmental stress signaling. PNAS 48 17320 17325 PMC1297668 16301540
  51. [55]Been M Francke C Siezen R Abee T 2011 Novel sB regulation modules of Gram-positive bacteria involve the use of complex hybrid histidine kinases. Microbiology 157 3 12 21051490
  52. [56]Pané-Farré J Lewis RJ Stülke J 2005 The RsbRST Stress Module in Bacteria: A Signalling System That May Interact with Different Output Modules. J Mol Microbiol Biotechnol 9 65 76 16319496
  53. [57]Nakhamchik A Wilde C Rowe-Magnus DA 2008 Cyclic-di-GMP regulates extracellular polysaccharide production, biofilm formation, and rugose colony development by Vibrio vulnificus. Appl Environ Microbiol 74 4199 4209 18487410 PMC2446529
  54. [58]Yildiz FH Visick KL 2009 Vibrio biofilms: so much the same yet so different. Trends Microbiol 17 109 118 19231189 PMC2729562
  55. [59]Sommerfeldt N Possling A Becker G Pesavento C Tschowri N 2009 Gene expression patterns and differential input into curli fimbriae regulation of all GGDEF/EAL domain proteins in Escherichia coli. Microbiology 155 1318 1331 19332833
  56. [60]Clegg S Hughes KT 2002 FimZ is a molecular link between sticking and swimming in Salmonella enterica serovar Typhimurium. J Bacteriol 184 1209 1213 11807085 PMC134799
  57. [61]Cascales E Christie PJ 2003 The versatile bacterial type IV secretion systems. Nat Rev Microbiol 1 137 149 15035043 PMC3873781
  58. [62]Grohmann E Muth G Espinosa M 2003 Conjugative plasmid transfer in gram-positive bacteria. Microbiol Mol Biol Rev 67 277 301 12794193 PMC156469
  59. [63]Christie PJ Atmakuri K Krishnamoorthy V Jakubowski S Cascales E 2005 Biogenesis, architecture, and function of bacterial type IV secretion systems. Annu Rev Microbiol 59 451 485 16153176 PMC3872966
  60. [64]Ward DV Draper O Zupan JR Zambryski PC 2002 Peptide linkage mapping of the Agrobacterium tumefaciens vir-encoded type IV secretion system reveals protein subassemblies. Proc Natl Acad Sci U S A 99 11493 11500 12177441 PMC123284
  61. [65]Christie PJ Vogel JP 2000 Bacterial type IV secretion: conjugation systems adapted to deliver effector molecules to host cells. Trends Microbiol 8 354 360 10920394 PMC4847720
  62. [66]Mao F Dam P Chou J Olman V Xu Y 2009 DOOR: a database for prokaryotic operons. Nucleic Acids Res 37 D459 463 18988623 PMC2686520
  63. [67]Margulies M Egholm M Altman WE Attiya S Bader JS 2005 Genome sequencing in microfabricated high-density picolitre reactors. Nature 437 376 380 16056220 PMC1464427
  64. [68]Kurtz S Phillippy A Delcher A Smoot M Shumway M 2004 Versatile and open software for comparing large genomes. Genome Biology 5 R12 14759262 PMC395750
  65. [69]Koressaar T Remm M 2007 Enhancements and modifications of primer design program Primer3. Bioinformatics 23 1289 1291 17379693
  66. [70]Salzberg SL Delcher AL Kasif S White O 1998 Microbial gene identification using interpolated Markov models. Nucleic Acids Res 26 544 548 9421513 PMC147303
  67. [71]Lukashin AV Borodovsky M 1998 GeneMark.hmm: new solutions for gene finding. Nucleic Acids Res 26 1107 1115 9461475 PMC147337
  68. [72]Lowe TM Eddy SR 1997 tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res 25 955 964 9023104 PMC146525
  69. [73]Lagesen K Hallin P Rodland EA Staerfeldt HH Rognes T 2007 RNAmmer: consistent and rapid annotation of ribosomal RNA genes. Nucleic Acids Res 35 3100 3108 17452365 PMC1888812
  70. [74]Li L Stoeckert CJ Jr Roos DS 2003 OrthoMCL: identification of ortholog groups for eukaryotic genomes. Genome Res 13 2178 2189 12952885 PMC403725
  71. [75]Suzuki H Lefebure T Hubisz MJ Bitar PP Lang P 2011 Comparative genomic analysis of the Streptococcus dysgalactiae species group: gene content, molecular adaptation, and promoter evolution. Genome Biology and Evolution doi: 10.1093/gbe/evr006 PMC3056289 21282711 · DOI
  72. [76]Hasan NA Grim CJ Haley BJ Chun J Alam M 2010 Comparative genomics of clinical and environmental Vibrio mimicus. Proc Natl Acad Sci USA 107 49 21134 21139 21078967 PMC3000290
  73. [77]Thompson JD Higgins DG Gibson TJ 1994 CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22 22 4673 4680 7984417 PMC308517
  74. [78]Guindon S Gascuel 2003 A Simple, Fast, and Accurate Algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology 52 5 696 704 14530136

Cited by

Sorted by citations

Authors
Morrison, S. S., Williams, T., Cain, A., Froelich, B., Taylor, C., Baker-Austin, C., Verner-Jeffreys, D., Hartnell, R., Oliver, J. D., & Gibas, C. J.
Affiliations
  • University of North Carolina at Charlotte (US)
  • Centre for Environment, Fisheries and Aquaculture Science (GB)
Corresponding author
Gibas, Cynthia J.
ORCID
Venue
PLoS ONE
Publisher
Public Library of Science (PLoS)
Published
2012-05-25
Volume
7
Issue
5
Pages
e37553
ISSN
1932-6203 (ISSN-L)
DOI
10.1371/journal.pone.0037553
PMC
PMC3360785
OpenAlex
W2019820906
Cited by
68
References
1
Citations by year
2026: 1 · 2025: 1 · 2024: 2 · 2023: 3 · 2022: 2 · 2021: 2 · 2020: 1 · 2019: 3 · 2018: 4 · 2017: 5 · 2016: 1 · 2015: 11 · 2014: 13 · 2013: 14 · 2012: 5
FWCI
8.78
Type
journal article
Language
en
Open access
Licence
Locations
  • PLoS ONE (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • UEA Digital Repository (University of East Anglia) (acceptedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • Figshare (submittedVersion, cc-by)
Funders
  • U.S. Department of Education
  • U.S. Department of Agriculture (2009-03571)
  • Virginia Commonwealth University
  • Centre for Environment, Fisheries and Aquaculture Science
  • Biotechnology and Biological Sciences Research Council (BBS/E/T/000PR6193)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Endocrinology › Vibrio bacteria research studies
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Phylogenetic Studies
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Endocrinology › Enterobacteriaceae and Cronobacter Research
Keywords
Vibrio vulnificus, environmental isolates, clinical isolates, comparative genomics, whole genome sequencing, virulence genes, sialic acid catabolism, mannitol fermentation, type IV secretion system, VirB4, gene content variation, seafood-borne infection, estuarine bacteria
MeSH terms
Chromosome Mapping, Genes, Bacterial, Genotype, Phylogeny, Genome, Bacterial, Sequence Analysis, DNA, Seafood, Gene Order, Vibrio vulnificus, Molecular Sequence Annotation

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review