1887

INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY logo

Volume 72, Issue 9

sp. nov., a novel member of the Cholerae clade Open Access

Abstract

A number of bacteria with close resemblance to have been isolated over the years by the Centres for Disease Control and Prevention (CDC), which could not be assigned a proper taxonomic designation on the basis of the results from preliminary identification methods. Nine such isolates have been found to share 16S rRNA gene identity exceeding 99 % with yet DNA–DNA hybridization (60.4–62.1 %) and average nucleotide identity values (94.4–95.1 %) were below the species cut-off, indicating a potentially novel species. Phylogenetic analysis of core genomes places this group of isolates in a monophyletic clade, within the ‘Cholerae clade’, but distinct from any other species. Extensive phenotypic characterization reveals unique biochemical properties that distinguish this novel species from . Comparative genomic analysis reveals a unique set of siderophore genes, indicating that iron acquisition strategies could be vital for the divergence of the novel species from a common ancestor with . On the basis of the genetic, phylogenetic and phenotypic differences observed, we propose that these isolates represent a novel species of the genus , for which the name sp. nov. is proposed. Strain 2521-89 (= DSM 112461=CCUG 75318), isolated from lake water, is the type strain.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): Cholerae clade , novel species , Vibrio , Vibrio cholerae and Vibriosis
Funding
This study was supported by the:
  • Alberta Innovates - Technology Futures
    • Principle Award Recipient: MohammadTarequl Islam
© 2022 The Authors
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License.
Loading

Article metrics loading...

/content/journal/ijsem/10.1099/ijsem.0.005571
2022-09-28
2024-05-02
Loading full text...

Full text loading...

/deliver/fulltext/ijsem/72/9/ijsem005571.html?itemId=/content/journal/ijsem/10.1099/ijsem.0.005571&mimeType=html&fmt=ahah

References

  1. Baker-Austin C, Trinanes J, Gonzalez-Escalona N, Martinez-Urtaza J. Non-cholera Vibrios: the microbial barometer of climate change. Trends Microbiol 2017; 25:76–84 [View Article]
     [Google Scholar]
  2. Lipp EK, Huq A, Colwell RR. Effects of global climate on infectious disease: the cholera model. Clin Microbiol Rev 2002; 15:757–770 [View Article]
     [Google Scholar]
  3. Boyd EF, Carpenter MR, Chowdhury N, Cohen AL, Haines-Menges BL et al. Post-genomic analysis of members of the family Vibrionaceae. Microbiol Spectr 2015; 3: [View Article]
     [Google Scholar]
  4. Kaper JB, Morris JG, Levine MM. Cholera. Clin Microbiol Rev 1995; 8:48–86 [View Article]
     [Google Scholar]
  5. Colwell RR. Infectious disease and environment: cholera as a paradigm for waterborne disease. Int Microbiol 2004; 7:285–289
     [Google Scholar]
  6. Islam MT, Nasreen T, Kirchberger PC, Liang KYH, Orata FD et al. Population analysis of Vibrio cholerae in aquatic reservoirs reveals a novel sister species (Vibrio paracholerae sp. nov.) with a history of association with humans. Appl Environ Microbiol 2021; 87:00422–21 [View Article]
     [Google Scholar]
  7. Kirchberger PC, Orata FD, Nasreen T, Kauffman KM, Tarr CL et al. Culture-independent tracking of Vibrio cholerae lineages reveals complex spatiotemporal dynamics in a natural population. Environ Microbiol 2020; 22:4244–4256 [View Article]
     [Google Scholar]
  8. Kirchberger PC, Turnsek M, Hunt DE, Haley BJ, Colwell RR et al. Vibrio metoecus sp. nov., a close relative of Vibrio cholerae isolated from coastal brackish ponds and clinical specimens. Int J Syst Evol Microbiol 2014; 64:3208–3214 [View Article]
     [Google Scholar]
  9. Haley BJ, Grim CJ, Hasan NA, Choi S-Y, Chun J et al. Comparative genomic analysis reveals evidence of two novel Vibrio species closely related to V. cholerae. BMC Microbiol 2010; 10:154 [View Article]
     [Google Scholar]
  10. Hasan NA, Grim CJ, Haley BJ, Chun J, Alam M et al. Comparative genomics of clinical and environmental Vibrio mimicus. Proc Natl Acad Sci 2010; 107:21134–21139 [View Article]
     [Google Scholar]
  11. Baker-Austin C, Oliver JD, Alam M, Ali A, Waldor MK et al. Vibrio spp. infections. Nat Rev Dis Primers 2018; 4:8 [View Article]
     [Google Scholar]
  12. Colwell RR. Infectious disease and environment: cholera as a paradigm for waterborne disease. Int Microbiol 2004; 7:285–289
     [Google Scholar]
  13. Huq A, Small EB, West PA, Huq MI, Rahman R et al. Ecological relationships between Vibrio cholerae and planktonic crustacean copepods. Appl Environ Microbiol 1983; 45:275–283 [View Article]
     [Google Scholar]
  14. Islam MT, Liang K, Im MS, Winkjer J, Busby S et al. Draft genome sequences of nine Vibrio sp. isolates from across the United States closely related to Vibrio cholerae. Microbiol Resour Announc 2018; 7:21 [View Article]
     [Google Scholar]
  15. Orata FD, Kirchberger PC, Méheust R, Barlow EJ, Tarr CL et al. The dynamics of genetic interactions between Vibrio metoecus and Vibrio cholerae, two close relatives co-occurring in the environment. Genome Biol Evol 2015; 7:2941–2954 [View Article]
     [Google Scholar]
  16. Dorman MJ, Kane L, Domman D, Turnbull JD, Cormie C et al. The history, genome and biology of NCTC 30: a non-pandemic Vibrio cholerae isolate from world war one. Proc Biol Sci 2019; 286:20182025 [View Article]
     [Google Scholar]
  17. Liang K, Orata FD, Winkjer NS, Rowe LA, Tarr CL et al. Complete genome sequence of Vibrio sp. strain 2521-89, a close relative of Vibrio cholerae isolated from lake water in New Mexico, USA. Genome Announc 2017; 5:e00905-17 [View Article]
     [Google Scholar]
  18. Liang K, Islam MT, Hussain N, Winkjer NS, Im MS et al. Draft genome sequences of Eight Vibrio sp. clinical isolates from across the United States that form a basal sister clade to Vibrio cholerae. Microbiol Resour Announc 2019; 8:e01473-18 [View Article]
     [Google Scholar]
  19. Alam M, Hasan NA, Sultana M, Nair GB, Sadique A et al. Diagnostic limitations to accurate diagnosis of cholera. J Clin Microbiol 2010; 48:3918–3922 [View Article]
     [Google Scholar]
  20. Farmer III JJ, Michael Janda J, Brenner FW, Cameron DN, Birkhead KM. Vibrio. In Bergey’s Manual of Systematics of Archaea and Bacteria American Cancer Society; 2015 pp 1–79
     [Google Scholar]
  21. Richter M, Rosselló-Móra R. Shifting the genomic gold standard for the prokaryotic species definition. Proc Natl Acad Sci 2009; 106:19126–19131 [View Article]
     [Google Scholar]
  22. Thompson FL, Gevers D, Thompson CC, Dawyndt P, Naser S et al. Phylogeny and molecular identification of vibrios on the basis of multilocus sequence analysis. Appl Environ Microbiol 2005; 71:5107–5115 [View Article]
     [Google Scholar]
  23. 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]
     [Google Scholar]
  24. Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M et al. Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 2012; 28:1647–1649 [View Article]
     [Google Scholar]
  25. Meier-Kolthoff JP, Auch AF, Klenk HP, Göker M. Genome sequence-based species delimitation with confidence intervals and improved distance functions. BMC Bioinformatics 2013; 14:60 [View Article]
     [Google Scholar]
  26. Aziz RK, Bartels D, Best AA, DeJongh M, Disz T et al. The RAST server: rapid annotations using subsystems technology. BMC Genomics 2008; 9:75 [View Article]
     [Google Scholar]
  27. Chaudhari NM, Gupta VK, Dutta C. BPGA-an ultra-fast pan-genome analysis pipeline. Sci Rep 2016; 6:24373 [View Article]
     [Google Scholar]
  28. Angiuoli SV, Salzberg SL. Mugsy: fast multiple alignment of closely related whole genomes. Bioinformatics 2011; 27:334–342 [View Article]
     [Google Scholar]
  29. Stamatakis A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 2014; 30:1312–1313 [View Article]
     [Google Scholar]
  30. Bueno E, Pinedo V, Cava F. Adaptation of Vibrio cholerae to hypoxic environments. Front Microbiol 2020; 11: [View Article]
     [Google Scholar]
  31. Pu M, Rowe-Magnus DA. A tad pilus promotes the establishment and resistance of Vibrio vulnificus biofilms to mechanical clearance. NPJ Biofilms Microbiomes 2018; 4:10 [View Article]
     [Google Scholar]
  32. Wyckoff EE, Mey AR, Payne SM. Iron acquisition in Vibrio cholerae. Biometals 2007; 20:405–416 [View Article]
     [Google Scholar]
  33. Thode SK, Rojek E, Kozlowski M, Ahmad R, Haugen P. Distribution of siderophore gene systems on a Vibrionaceae phylogeny: database searches, phylogenetic analyses and evolutionary perspectives. PLoS One 2018; 13:1–20 [View Article]
     [Google Scholar]
  34. Oliver JD, Warner RA, Cleland DR. Distribution of Vibrio vulnificus and other lactose-fermenting vibrios in the marine environment. Appl Environ Microbiol 1983; 45:985–998 [View Article]
     [Google Scholar]
  35. Heidelberg JF, Eisen JA, Nelson WC, Clayton RA, Gwinn ML et al. DNA sequence of both chromosomes of the cholera pathogen Vibrio cholerae. Nature 2000; 406:477–483 [View Article]
     [Google Scholar]
  36. Chun J, Grim CJ, Hasan NA, Lee JH, Choi SY et al. Comparative genomics reveals mechanism for short-term and long-term clonal transitions in pandemic Vibrio cholerae. Proc Natl Acad Sci U S A 2009; 106:15442–15447 [View Article]
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/ijsem/10.1099/ijsem.0.005571
Loading
Vibrio tarriae sp. nov., a novel member of the Cholerae clade
Int J Syst Evol Microbiol 72, 005571 (2022); https://doi.org/10.1099/ijsem.0.005571
/content/journal/ijsem/10.1099/ijsem.0.005571
/content/journal/ijsem/10.1099/ijsem.0.005571
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF

Most cited Most Cited RSS feed

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