1887

Abstract

A Gram-stain-negative, rod-shaped bacterial strain, designated IRLE0018 (=NRRL B-65642=NCTC 14661), was isolated from a cyanobacterial bloom along the Indian River Lagoon (IRL), a large and highly biodiverse estuary in eastern Florida (USA). The results of phylogenetic, biochemical, and phenotypic analyses indicate that this isolate is distinct from species of the genus with validly published names and is the closest relative to the emergent human pathogen, . Here, we present the complete genome sequence of strain IRLE0018 (4 535 135 bp). On the basis of the established average nucleotide identity (ANI) values for the determination of different species (ANI <95 %), strain IRLE0018, with an ANI of approximately 92 % compared with its closest relative, , represents a novel species within the genus . To our knowledge, this represents the first time this species has been described. The results of genomic analyses of IRLE0018 indicate the presence of antibiotic resistance genes and several known virulence factors, however, its pathogenicity profile (e.g. survival in serum, phagocytosis avoidance) reveals limited virulence potential of this species in contrast to .

Funding
This study was supported by the:
  • Burroughs Wellcome Fund (Award 1021977)
    • Principle Award Recipient: Almagro-MorenoSalvador
  • National Science Foundation (Award 2045671)
    • Principle Award Recipient: Almagro-MorenoSalvador
Loading

Article metrics loading...

/content/journal/ijsem/10.1099/ijsem.0.005675
2023-02-06
2024-05-02
Loading full text...

Full text loading...

References

  1. Reen FJ, Almagro-Moreno S, Ussery D, Boyd EF. The genomic code: inferring Vibrionaceae niche specialization. Nat Rev Microbiol 2006; 4:697–704 [View Article] [PubMed]
    [Google Scholar]
  2. Vezzulli L, Colwell RR, Pruzzo C. Ocean warming and spread of pathogenic vibrios in the aquatic environment. Microb Ecol 2013; 65:817–825 [View Article] [PubMed]
    [Google Scholar]
  3. Colwell RR. Global climate and infectious disease: the cholera paradigm. Science 1996; 274:2025–2031 [View Article] [PubMed]
    [Google Scholar]
  4. Almagro-Moreno S, Taylor RK. Cholera: environmental reservoirs and impact on disease ransmissiont. Microbiol Spectr 2013; 1:OH-0003-2012 [View Article]
    [Google Scholar]
  5. Sakib SN, Reddi G, Almagro-Moreno S. Environmental role of pathogenic traits in Vibrio cholerae. J Bacteriol 2018; 200:e00795–17 [View Article] [PubMed]
    [Google Scholar]
  6. Gulig PA, Bourdage KL, Starks AM. Molecular pathogenesis of Vibrio vulnificus. J Microbiol 2005; 43 Spec No:118–131
    [Google Scholar]
  7. Oliver JD. Vibrio vulnificus: death on the half shell. a personal journey with the pathogen and its ecology. Microb Ecol 2013; 65:793–799 [View Article]
    [Google Scholar]
  8. Phillips KE, Satchell KJF. Vibrio vulnificus: from oyster colonist to human pathogen. PLoS Pathog 2017; 13:e1006053 [View Article]
    [Google Scholar]
  9. Han D, Yu F, Tang H, Ren C, Wu C et al. Spreading of pandemic Vibrio parahaemolyticus O3:K6 and its serovariants: a re-analysis of strains isolated from multiple studies. Front Cell Infect Microbiol 2017; 7:188 [View Article]
    [Google Scholar]
  10. Li L, Meng H, Gu D, Li Y, Jia M. Molecular mechanisms of Vibrio parahaemolyticus pathogenesis. Microbiol Res 2019; 222:43–51 [View Article]
    [Google Scholar]
  11. López-Pérez M, Jayakumar JM, Grant T-A, Zaragoza-Solas A, Cabello-Yeves PJ et al. Ecological diversification reveals routes of pathogen emergence in endemic Vibrio vulnificus populations. Proc Natl Acad Sci U S A 2021; 118:40 [View Article] [PubMed]
    [Google Scholar]
  12. Reddi G, Pruss K, Cottingham KL, Taylor RK, Almagro-Moreno S. Catabolism of mucus components influences motility of Vibrio cholerae in the presence of environmental reservoirs. PLoS One 2018; 13:e0201383 [View Article]
    [Google Scholar]
  13. Groubert TN, Oliver JD. Interaction of Vibrio vulnificus and the Eastern Oyster, Crassostrea virginica. J Food Prot 1994; 57:224–228 [View Article]
    [Google Scholar]
  14. Islam MS, Mahmuda S, Morshed MG, Bakht HBM, Khan MNH et al. Role of cyanobacteria in the persistence of Vibrio cholerae O139 in saline microcosms. Can J Microbiol 2004; 50:127–131 [View Article]
    [Google Scholar]
  15. Warner E, Oliver JD. Population structures of two genotypes of Vibrio vulnificus in oysters (Crassostrea virginica) and seawater. Appl Environ Microbiol 2008; 74:80–85 [View Article]
    [Google Scholar]
  16. Huq A, Haley BJ, Taviani E, Chen A, Hasan NA et al. Detection, isolation, and identification of Vibrio cholerae from the environment. Curr Protoc Microbiol 2012; Chapter 6:Unit6A.5 [View Article]
    [Google Scholar]
  17. Schuster BM, Tyzik AL, Donner RA, Striplin MJ, Almagro-Moreno S et al. Ecology and genetic structure of a northern temperate Vibrio cholerae population related to toxigenic isolates. Appl Environ Microbiol 2011; 77:7568–7575 [View Article]
    [Google Scholar]
  18. Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 2014; 30:2114–2120 [View Article] [PubMed]
    [Google Scholar]
  19. Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M et al. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 2012; 19:455–477 [View Article] [PubMed]
    [Google Scholar]
  20. Pritchard L, Glover RH, Humphris S, Elphinstone JG, Toth IK. Genomics and taxonomy in diagnostics for food security: soft-rotting enterobacterial plant pathogens. Anal Methods 2016; 8:12–24 [View Article]
    [Google Scholar]
  21. Segata N, Börnigen D, Morgan XC, Huttenhower C. PhyloPhlAn is a new method for improved phylogenetic and taxonomic placement of microbes. Nat Commun 2013; 4:2304 [View Article] [PubMed]
    [Google Scholar]
  22. Nguyen L-T, Schmidt HA, von Haeseler A, Minh BQ. IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol Biol Evol 2015; 32:268–274 [View Article] [PubMed]
    [Google Scholar]
  23. Hoang DT, Chernomor O, von Haeseler A, Minh BQ, Vinh LS. UFBoot2: improving the ultrafast bootstrap approximation. Mol Biol Evol 2018; 35:518–522 [View Article]
    [Google Scholar]
  24. Lydon KA, Kinsey T, Le C, Gulig PA, Jones JL. Biochemical and virulence characterization of Vibrio vulnificus isolates from clinical and environmental sources. Front Cell Infect Microbiol 2021; 11:637019 [View Article]
    [Google Scholar]
  25. DePaola C a. A. Bacteriological analytical manual chapter 9. vibrio 2004
    [Google Scholar]
  26. Orata FD, Xu Y, Gladney LM, Rishishwar L, Case RJ et al. Characterization of clinical and environmental isolates of Vibrio cidicii sp. nov., a close relative of Vibrio navarrensis. Int J Syst Evol Microbiol 2016; 66:4148–4155 [View Article] [PubMed]
    [Google Scholar]
  27. Farmer J. J III JM, Brenner FW, Cameron DN, Birkhead KM. Bergey’s Manual® of Systematic Bacteriology–Volume Two: The Proteobacteria, Part B: The Gammaproteobacteria, ed. N.R.K. Don J. Brenner, James T. Staley (Chairman), George M. Garrity, David R. Boone (Vice Chairman), Paul Vos, Michael Goodfellow, Fred A. Rainey, Karl-Heinz Schleifer. Vol. 2 New York, NY: Springer; 2005
    [Google Scholar]
  28. Huang Y, Niu B, Gao Y, Fu L, Li W. CD-HIT Suite: a web server for clustering and comparing biological sequences. Bioinformatics 2010; 26:680–682 [View Article] [PubMed]
    [Google Scholar]
  29. Overbeek R, Begley T, Butler RM, Choudhuri JV, Chuang H-Y et al. The subsystems approach to genome annotation and its use in the project to annotate 1000 genomes. Nucleic Acids Res 2005; 33:5691–5702 [View Article] [PubMed]
    [Google Scholar]
  30. Grondin JM, Tamura K, Déjean G, Abbott DW, Brumer H. Polysaccharide utilization loci: fueling microbial communities. J Bacteriol 2017; 199:15 [View Article]
    [Google Scholar]
  31. Durica-Mitic S, Göpel Y, Görke B. Carbohydrate utilization in bacteria: making the most out of sugars with the help of small regulatory RNAs. Microbiol Spectr 2018; 6: [View Article]
    [Google Scholar]
  32. Almagro-Moreno S, Boyd EF. Sialic acid catabolism confers a competitive advantage to pathogenic Vibrio cholerae in the mouse intestine. Infect Immun 2009; 77:3807–3816 [View Article]
    [Google Scholar]
  33. Lubin J-B, Kingston JJ, Chowdhury N, Boyd EF. Sialic acid catabolism and transport gene clusters are lineage specific in Vibrio vulnificus. Appl Environ Microbiol 2012; 78:3407–3415 [View Article]
    [Google Scholar]
  34. Christgen SL, Becker DF. Role of Proline in Pathogen and Host Interactions. Antioxid Redox Signal 2019; 30:683–709 [View Article] [PubMed]
    [Google Scholar]
  35. Lubin J-B, Lewis WG, Gilbert NM, Weimer CM, Almagro-Moreno S et al. Host-like carbohydrates promote bloodstream survival of Vibrio vulnificus in vivo. Infect Immun 2015; 83:3126–3136 [View Article]
    [Google Scholar]
  36. Bochner BR, Gadzinski P, Panomitros E. Phenotype microarrays for high-throughput phenotypic testing and assay of gene function. Genome Res 2001; 11:1246–1255 [View Article] [PubMed]
    [Google Scholar]
  37. Dong Y, Li S, Zhao D, Liu J, Ma S et al. IolR, a negative regulator of the myo-inositol metabolic pathway, inhibits cell autoaggregation and biofilm formation by downregulating RpmA in Aeromonas hydrophila. NPJ Biofilms Microbiomes 2020; 6:22 [View Article]
    [Google Scholar]
  38. Lewis JA, Horswill AR, Schwem BE, Escalante-Semerena JC. The tricarballylate utilization (tcuRABC) genes of Salmonella enterica serovar Typhimurium LT2. J Bacteriol 2004; 186:1629–1637 [View Article]
    [Google Scholar]
  39. Vanhove AS, Hang S, Vijayakumar V, Wong AC, Asara JM et al. Vibrio cholerae ensures function of host proteins required for virulence through consumption of luminal methionine sulfoxide. PLoS Pathog 2017; 13:e1006428 [View Article]
    [Google Scholar]
  40. Bender RA. Regulation of the histidine utilization (Hut) system in bacteria. Microbiol Mol Biol Rev 2012; 76:565–584 [View Article]
    [Google Scholar]
  41. Lakin SM, Dean C, Noyes NR, Dettenwanger A, Ross AS et al. MEGARes: an antimicrobial resistance database for high throughput sequencing. Nucleic Acids Res 2017; 45:D574–D580 [View Article] [PubMed]
    [Google Scholar]
  42. Chen L, Zheng D, Liu B, Yang J, Jin Q. VFDB 2016: hierarchical and refined dataset for big data analysis--10 years on. Nucleic Acids Res 2016; 44:D694–7 [View Article] [PubMed]
    [Google Scholar]
  43. Shaw KS, Rosenberg Goldstein RE, He X, Jacobs JM, Crump BC et al. Antimicrobial susceptibility of Vibrio vulnificus and Vibrio parahaemolyticus recovered from recreational and commercial areas of Chesapeake Bay and Maryland Coastal Bays. PLoS One 2014; 9:e89616 [View Article]
    [Google Scholar]
  44. Baker-Austin C, McArthur JV, Lindell AH, Wright MS, Tuckfield RC et al. Multi-site analysis reveals widespread antibiotic resistance in the marine pathogen Vibrio vulnificus. Microb Ecol 2009; 57:151–159 [View Article]
    [Google Scholar]
  45. Kreger A, DeChatelet L, Shirley P. Interaction of Vibrio vulnificus with human polymorphonuclear leukocytes: association of virulence with resistance to phagocytosis. J Infect Dis 1981; 144:244–248 [View Article]
    [Google Scholar]
  46. Campos MA, Vargas MA, Regueiro V, Llompart CM, Albertí S et al. Capsule polysaccharide mediates bacterial resistance to antimicrobial peptides. Infect Immun 2004; 72:7107–7114 [View Article]
    [Google Scholar]
  47. Pettis GS, Mukerji AS. Structure, function, and regulation of the essential virulence factor capsular polysaccharide of Vibrio vulnificus. Int J Mol Sci 2020; 21:E3259 [View Article]
    [Google Scholar]
  48. Kim H, Ayrapetyan M, Oliver JD. Survival of Vibrio vulnificus genotypes in male and female serum, and production of siderophores in human serum and seawater. Foodborne Pathog Dis 2014; 11:119–125 [View Article]
    [Google Scholar]
  49. Williams T, Ayrapetyan M, Ryan H, Oliver J. Serum Survival of Vibrio vulnificus: Role of Genotype, Capsule, Complement, Clinical Origin, and in Situ Incubation. Pathogens 2014; 3:822–832 [View Article]
    [Google Scholar]
  50. Severi E, Randle G, Kivlin P, Whitfield K, Young R et al. Sialic acid transport in Haemophilus influenzae is essential for lipopolysaccharide sialylation and serum resistance and is dependent on a novel tripartite ATP-independent periplasmic transporter. Mol Microbiol 2005; 58:1173–1185 [View Article]
    [Google Scholar]
  51. Kashimoto T, Ueno S, Hanajima M, Hayashi H, Akeda Y et al. Vibrio vulnificus induces macrophage apoptosis in vitro and in vivo. Infect Immun 2003; 71:533–535 [View Article]
    [Google Scholar]
  52. Kashimoto T, Ueno S, Hayashi H, Hanajima M, Yoshioka K et al. Depletion of lymphocytes, but not neutrophils, via apoptosis in a murine model of Vibrio vulnificus infection. J Med Microbiol 2005; 54:15–22 [View Article]
    [Google Scholar]
  53. Lo H-R, Lin J-H, Chen Y-H, Chen C-L, Shao C-P et al. RTX toxin enhances the survival of Vibrio vulnificus during infection by protecting the organism from phagocytosis. J Infect Dis 2011; 203:1866–1874 [View Article]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/ijsem/10.1099/ijsem.0.005675
Loading
/content/journal/ijsem/10.1099/ijsem.0.005675
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error