1887

Microbial Genomics logo

Volume 9, Issue 6

Comparative genomics uncovered differences between clinical and environmental populations of in New Zealand Open Access

Abstract

has been identified as an emerging human pathogen worldwide with cases undergoing a global expansion over recent decades in phase with climate change. New Zealand had remained free of outbreaks until 2019, but different outbreaks have been reported consecutively since then. To provide new insights into the recent emergence of cases associated with outbreak clones over recent years, a comparative genomic study was carried out using a selection of clinical (mostly outbreak) and environmental isolates of obtained in New Zealand between 1973 and 2021. Among 151 isolates of clinical (=60) and environmental (=91) origin, 47 sequence types (STs) were identified, including 31 novel STs. The population of environmental isolates generated 30 novel STs, whereas only 1 novel ST (ST2658) was identified among the population of clinical isolates. The novel clinical ST was a single-locus variant of the pandemic ST36 strain, indicating further evolution of this pandemic strain. The environmental isolates exhibited a significant genetic heterogeneity compared to the clinical isolates. The whole-genome phylogeny separated the population of clinical isolates from their environmental counterparts, clearly indicating their distant genetic relatedness. In addition to differences in ancestral profiles and genetic relatedness, these two groups of isolates exhibited a profound difference in their virulence profiles. While the entire population of clinical isolates harboured the thermostable direct haemolysin () and/or the thermostable-related haemolysin (), only a few isolates of environmental origin possessed the same virulence genes. In contrast to and , adhesin-encoding genes, and MSHA, showed a significantly (<0.001) greater association with the environmental isolates compared to the clinical isolates. The effectors, VopQ, VPA0450 and VopS, which belong to T3SS1, were ubiquitous, being present in each isolate regardless of its origin. The effectors VopC and VopA, which belong to T3SS2, were rarely detected in any of the examined isolates. Our data indicate that the clinical and environmental isolates of from New Zealand differ in their population structures, ancestral profiles, genetic relatedness and virulence profiles. In addition, we identified numerous unique non-synonymous single-nucleotide polymorphisms (nsSNPs) in adhesins and effectors, exclusively associated with the clinical isolates tested, which may suggest a possible role of these mutations in the overall virulence of the clinical isolates.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): non-synonymous mutations , pandemic strains , population genomics , Vibrio parahaemolyticus , virulence and whole-genome sequencing
Funding
This study was supported by the:
  • Ministry of Business, Innovation and Employment (Award CAWX1801)
    • Principle Award Recipient: NotApplicable
© 2023 The Authors
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License.
Loading

Article metrics loading...

/content/journal/mgen/10.1099/mgen.0.001037
2023-06-02
2024-05-13
Loading full text...

Full text loading...

/deliver/fulltext/mgen/9/6/mgen001037.html?itemId=/content/journal/mgen/10.1099/mgen.0.001037&mimeType=html&fmt=ahah

References

  1. Newton A, Kendall M, Vugia DJ, Henao OL, Mahon BE. Increasing rates of Vibriosis in the United States, 1996–2010: review of surveillance data from 2 systems. Clin Infect Dis 2012; 54:S391–S395 [View Article]
     [Google Scholar]
  2. Abanto M, Gavilan RG, Baker-Austin C, Gonzalez-Escalona N, Martinez-Urtaza J. Global expansion of pacific Northwest Vibrio parahaemolyticus sequence type 36. Emerg Infect Dis 2020; 26:323–326 [View Article] [PubMed]
     [Google Scholar]
  3. Marder Mph EP, Griffin PM, Cieslak PR, Dunn J, Hurd S et al. Preliminary incidence and trends of infections with pathogens transmitted commonly through food - foodborne diseases active surveillance network, 10 U.S. sites, 2006-2017. MMWR Morb Mortal Wkly Rep 2018; 67:324–328 [View Article] [PubMed]
     [Google Scholar]
  4. Arakawa E, Murase T, Shimada T, Okitsu T, Yamai S et al. Emergence and prevalence of a novel Vibrio parahaemolyticus O3: K6 clone in Japan. Jap J Infect Dis 1999; 52:246–247
     [Google Scholar]
  5. Martinez-Urtaza J, Simental L, Velasco D, DePaola A, Ishibashi M et al. Pandemic Vibrio parahaemolyticus O3:K6, Europe. Emerg Infect Dis 2005; 11:1319–1320 [View Article] [PubMed]
     [Google Scholar]
  6. Baker-Austin C, Trinanes JA, Salmenlinna S, Löfdahl M, Siitonen A et al. Heat wave-associated Vibriosis, Sweden and Finland, 2014. Emerg Infect Dis 2016; 22:1216–1220 [View Article] [PubMed]
     [Google Scholar]
  7. Martinez-Urtaza J, Trinanes J, Abanto M, Lozano-Leon A, Llovo-Taboada J et al. Epidemic dynamics of Vibrio parahaemolyticus illness in a hotspot of disease emergence, Galicia, Spain. Emerg Infect Dis 2018; 24:852–859 [View Article] [PubMed]
     [Google Scholar]
  8. DePaola A, Kaysner CA, Bowers J, Cook DW. Environmental investigations of Vibrio parahaemolyticus in oysters after outbreaks in Washington, Texas, and New York (1997 and 1998). Appl Environ Microbiol 2000; 66:4649–4654 [View Article] [PubMed]
     [Google Scholar]
  9. Hervio-Heath D, Colwell RR, Derrien A, Robert-Pillot A, Fournier JM et al. Occurrence of pathogenic vibrios in coastal areas of France. J Appl Microbiol 2002; 92:1123–1135 [View Article] [PubMed]
     [Google Scholar]
  10. Alam MJ, Tomochika KI, Miyoshi SI, Shinoda S. Environmental investigation of potentially pathogenic Vibrio parahaemolyticus in the Seto-Inland Sea, Japan. FEMS Microbiol Lett 2002; 208:83–87 [View Article] [PubMed]
     [Google Scholar]
  11. García K, Torres R, Uribe P, Hernández C, Rioseco ML et al. Dynamics of clinical and environmental Vibrio parahaemolyticus strains during Seafood-related summer diarrhea outbreaks in Southern Chile. Appl Environ Microbiol 2009; 75:7482–7487 [View Article]
     [Google Scholar]
  12. Chao G, Jiao X, Zhou X, Wang F, Yang Z et al. Distribution of genes encoding four pathogenicity islands (VPaIs), T6SS, biofilm, and type I pilus in food and clinical strains of Vibrio parahaemolyticus in China. Foodborne Pathog Dis 2010; 7:649–658 [View Article] [PubMed]
     [Google Scholar]
  13. Velazquez-Roman J, León-Sicairos N, Flores-Villaseñor H, Villafaña-Rauda S, Canizalez-Roman A. Association of pandemic Vibrio parahaemolyticus O3:K6 present in the coastal environment of Northwest Mexico with cases of recurrent diarrhea between 2004 and 2010. Appl Environ Microbiol 2012; 78:1794–1803 [View Article] [PubMed]
     [Google Scholar]
  14. Liu M, Yang S, Zheng C, Luo X, Bei W et al. Binding to type I collagen is essential for the infectivity of Vibrio parahaemolyticus to host cells. Cellular Microbiol 2018; 20:e12856 [View Article]
     [Google Scholar]
  15. Liu M, Chen S. A novel adhesive factor contributing to the virulence of Vibrio parahaemolyticus. Sci Rep 2015; 5:14449 [View Article]
     [Google Scholar]
  16. Aagesen AM, Häse CC. Sequence analyses of type IV pili from Vibrio cholerae, Vibrio parahaemolyticus, and Vibrio vulnificus. Microb Ecol 2012; 64:509–524 [View Article] [PubMed]
     [Google Scholar]
  17. Krachler AM, Orth K. Functional characterization of the interaction between bacterial adhesin multivalent adhesion molecule 7 (MAM7) protein and its host cell ligands. J Biol Chem 2011; 286:38939–38947 [View Article] [PubMed]
     [Google Scholar]
  18. O’Boyle N, Houeix B, Kilcoyne M, Joshi L, Boyd A. The MSHA pilus of Vibrio parahaemolyticus has lectin functionality and enables TTSS-mediated pathogenicity. Int J Med Microbiol 2013; 303:563–573 [View Article] [PubMed]
     [Google Scholar]
  19. Krachler AM, Ham H, Orth K. Outer membrane adhesion factor multivalent adhesion molecule 7 initiates host cell binding during infection by gram-negative pathogens. Proc Natl Acad Sci 2011; 108:11614–11619 [View Article] [PubMed]
     [Google Scholar]
  20. Orlova EV. A molecular syringe that kills cells. Nat Struct Mol Biol 2015; 22:357–359 [View Article] [PubMed]
     [Google Scholar]
  21. Sreelatha A, Bennett TL, Zheng H, Jiang QX, Orth K et al. Vibrio effector protein, VopQ, forms a lysosomal gated channel that disrupts host ion homeostasis and autophagic flux. Proc Natl Acad Sci 2013; 110:11559–11564 [View Article] [PubMed]
     [Google Scholar]
  22. Luong P, Kinch LN, Brautigam CA, Grishin NV, Tomchick DR et al. Kinetic and structural insights into the mechanism of AMPylation by VopS Fic domain. J Biol Chem 2010; 285:20155–20163 [View Article] [PubMed]
     [Google Scholar]
  23. Broberg CA, Zhang L, Gonzalez H, Laskowski-Arce MA, Orth K. A Vibrio effector protein is an inositol phosphatase and disrupts host cell membrane integrity. Science 2010; 329:1660–1662 [View Article] [PubMed]
     [Google Scholar]
  24. Wang R, Zhong Y, Gu X, Yuan J, Saeed AF et al. The pathogenesis, detection, and prevention of Vibrio parahaemolyticus. Front Microbiol 2015; 6:144 [View Article]
     [Google Scholar]
  25. Burdette DL, Yarbrough ML, Orvedahl A, Gilpin CJ, Orth K. Vibrio parahaemolyticus orchestrates a multifaceted host cell infection by induction of autophagy, cell rounding, and then cell lysis. Proc Natl Acad Sci 2008; 105:12497–12502 [View Article] [PubMed]
     [Google Scholar]
  26. New Zealand Ministry of Health Communicable disease manual. n.d https://www.health.govt.nz/our-work/diseases-and-conditions/communicable-disease-control-manual/acute-gastroenteritis-and-toxin-related-illnesses
  27. Kirs M, Depaola A, Fyfe R, Jones JL, Krantz J et al. A survey of oysters (Crassostrea gigas) in New Zealand for Vibrio parahaemolyticus and Vibrio vulnificus. Int J Food Microbiol 2011; 147:149–153 [View Article] [PubMed]
     [Google Scholar]
  28. Cruz CD, Hedderley D, Fletcher GC. Long-term study of Vibrio parahaemolyticus prevalence and distribution in New Zealand shellfish. Appl Environ Microbiol 2015; 81:2320–2327 [View Article] [PubMed]
     [Google Scholar]
  29. Nordstrom JL, Vickery MCL, Blackstone GM, Murray SL, DePaola A. Development of a multiplex real-time PCR assay with an internal amplification control for the detection of total and pathogenic Vibrio parahaemolyticus bacteria in oysters. Appl Environ Microbiol 2007; 73:5840–5847 [View Article] [PubMed]
     [Google Scholar]
  30. Coil D, Jospin G, Darling AE. A5-miseq: an updated pipeline to assemble microbial genomes from Illumina MiSeq data. Bioinformatics 2015; 31:587–589 [View Article] [PubMed]
     [Google Scholar]
  31. González-Escalona N, Martinez-Urtaza J, Romero J, Espejo RT, Jaykus LA et al. Determination of molecular phylogenetics of Vibrio parahaemolyticus strains by multilocus sequence typing. J Bacteriol 2008; 190:2831–2840 [View Article] [PubMed]
     [Google Scholar]
  32. Francisco AP, Bugalho M, Ramirez M, Carriço JA. Global optimal eBURST analysis of multilocus typing data using a graphic matroid approach. BMC Bioinformatics 2009; 10:152 [View Article] [PubMed]
     [Google Scholar]
  33. Nascimento M, Sousa A, Ramirez M, Francisco AP, Carriço JA et al. PHYLOViZ 2.0: providing scalable data integration and visualization for multiple phylogenetic inference methods. Bioinformatics 2017; 33:128–129 [View Article] [PubMed]
     [Google Scholar]
  34. Yoshimura D, Kajitani R, Gotoh Y, Katahira K, Okuno M et al. Evaluation of SNP calling methods for closely related bacterial isolates and a novel high-accuracy pipeline: BactSNP. Microb Genom 2019; 5:e000261 [View Article] [PubMed]
     [Google Scholar]
  35. Kurtz S, Phillippy A, Delcher AL, Smoot M, Shumway M et al. Versatile and open software for comparing large genomes. Genome Biol 2004; 5:R12 [View Article] [PubMed]
     [Google Scholar]
  36. Li H, Durbin R. Fast and accurate long-read alignment with Burrows–Wheeler transform. Bioinformatics 2010; 26:589–595 [View Article]
     [Google Scholar]
  37. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J et al. Genome project data processing subgroup. the sequence alignment/map (SAM) format and samtools. Bioinformatics 2009; 25:2078–2079 [View Article]
     [Google Scholar]
  38. Saitou N, Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evolution 1987; 4:406–425
     [Google Scholar]
  39. Felsenstein J. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 1985; 39:783–791 [View Article] [PubMed]
     [Google Scholar]
  40. Tamura K, Nei M, Kumar S. Prospects for inferring very large phylogenies by using the neighbor-joining method. Proc Natl Acad Sci 2004; 101:11030–11035 [View Article] [PubMed]
     [Google Scholar]
  41. Tamura K, Stecher G, Kumar S. MEGA11: molecular evolutionary genetics analysis version 11. Mol Biol Evol 2021; 38:3022–3027 [View Article] [PubMed]
     [Google Scholar]
  42. Benson DA, Cavanaugh M, Clark K, Karsch-Mizrachi I, Lipman DJ et al. GenBank. Nucleic Acids Res 2017; 45:D37–D42 [View Article] [PubMed]
     [Google Scholar]
  43. McWilliam H, Li W, Uludag M, Squizzato S, Park YM et al. Analysis tool web services from the EMBL-EBI. Nucleic Acids Res 2013; 41:W597–600 [View Article] [PubMed]
     [Google Scholar]
  44. 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] [PubMed]
     [Google Scholar]
  45. Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 2004; 32:1792–1797 [View Article] [PubMed]
     [Google Scholar]
  46. Turner JW, Paranjpye RN, Landis ED, Biryukov SV, González-Escalona N et al. Population structure of clinical and environmental Vibrio parahaemolyticus from the Pacific Northwest coast of the United States. PLoS One 2013; 8:e55726 [View Article] [PubMed]
     [Google Scholar]
  47. Baker-Austin C, Jenkins C, Dadzie J, Mestanza O, Delgado E et al. Genomic epidemiology of domestic and travel-associated Vibrio parahaemolyticus infections in the UK, 2008–2018. Food Control 2020; 115:107244 [View Article]
     [Google Scholar]
  48. Banerjee SK, Kearney AK, Nadon CA, Peterson C-L, Tyler K et al. Phenotypic and genotypic characterization of Canadian clinical isolates of Vibrio parahaemolyticus collected from 2000 to 2009. J Clin Microbiol 2014; 52:1081–1088 [View Article]
     [Google Scholar]
  49. Li J, Xue F, Yang Z, Zhang X, Zeng D et al. Vibrio parahaemolyticus strains of pandemic serotypes identified from clinical and environmental samples from Jiangsu, China. Front Microbiol 2016; 7:787 [View Article]
     [Google Scholar]
  50. Ronholm J, Petronella N, Chew Leung C, Pightling AW, Banerjee SK. Genomic features of environmental and clinical Vibrio parahaemolyticus isolates lacking recognized virulence factors are dissimilar. Appl Environ Microbiol 2016; 82:1102–1113 [View Article] [PubMed]
     [Google Scholar]
  51. Xie T, Wu Q, Zhang J, Xu X, Cheng J. Comparison of Vibrio parahaemolyticus isolates from aquatic products and clinical by antibiotic susceptibility, virulence, and molecular characterisation. Food Control 2017; 71:315–321 [View Article]
     [Google Scholar]
  52. Santos L de O, de Lanna CA, Arcanjo AC da C, Bisch PM, von Krüger WMA. Genotypic diversity and pathogenic potential of clinical and environmental Vibrio parahaemolyticus isolates from Brazil. Front Microbiol 2021; 12:602653 [View Article] [PubMed]
     [Google Scholar]
  53. Jones JL, Lüdeke CHM, Bowers JC, Garrett N, Fischer M et al. Biochemical, serological, and virulence characterization of clinical and oyster Vibrio parahaemolyticus isolates. J Clin Microbiol 2012; 50:2343–2352 [View Article] [PubMed]
     [Google Scholar]
  54. Bhoopong P, Palittapongarnpim P, Pomwised R, Kiatkittipong A, Kamruzzaman M et al. Variability of properties of Vibrio parahaemolyticus strains isolated from individual patients. J Clin Microbiol 2007; 45:1544–1550 [View Article]
     [Google Scholar]
  55. Paranjpye R, Hamel OS, Stojanovski A, Liermann M. Genetic diversity of clinical and environmental Vibrio parahaemolyticus strains from the Pacific Northwest. Appl Environ Microbiol 2012; 78:8631–8638 [View Article] [PubMed]
     [Google Scholar]
  56. Fujimoto T, Hamamoto I, Taniguchi K, Chikahira M, Okabe N. Molecular epidemiology of adenovirus type 3 detected from 1994 to 2006 in Hyogo Prefecture, Japan. Jpn J Infect Dis 2008; 61:143–145 [View Article]
     [Google Scholar]
  57. Vidovic S, Aly M, Flemming C, Springthorpe S, Sattar SA. First evidence of genotypes Ad3a16 and Ad3a18 in North America, obtained by genetic analysis of infectious human adenovirus from wastewaters of two urban communities in Canada. Appl Environ Microbiol 2011; 77:4256–4259 [View Article] [PubMed]
     [Google Scholar]
  58. Kisiela DI, Chattopadhyay S, Libby SJ, Karlinsey JE, Fang FC et al. Evolution of Salmonella enterica virulence via point mutations in the Fimbrial Adhesin. PLoS Pathog 2016; 8:e1002733 [View Article]
     [Google Scholar]
  59. Alshalchi S, Hayer SS, An R, Munoz-Aguayo J, Flores-Figueroa C et al. The possible influence of non-synonymous point mutations within the FimA adhesin of non-typhoidal Salmonella (NTS) isolates in the process of host adaptation. Front Microbiol 2017; 8:2030 [View Article] [PubMed]
     [Google Scholar]
  60. Blair JMA, Bavro VN, Ricci V, Modi N, Cacciotto P et al. AcrB drug-binding pocket substitution confers clinically relevant resistance and altered substrate specificity. Proc Natl Acad Sci 2015; 112:3511–3516 [View Article] [PubMed]
     [Google Scholar]
  61. Vidovic S, An R, Rendahl A. Molecular and physiological characterization of fluoroquinolone-highly resistant Salmonella enteritidis strains. Front Microbiol 2019; 10:729 [View Article] [PubMed]
     [Google Scholar]
  62. Nguyen AQ, Shimohata T, Hatayama S, Tentaku A, Kido J et al. Type III secretion effector VopQ of Vibrio parahaemolyticus modulates central carbon metabolism in epithelial cells. mSphere 2020; 5:e00960-19 [View Article] [PubMed]
     [Google Scholar]
  63. Nasu H, Iida T, Sugahara T, Yamaichi Y, Park KS et al. A filamentous phage associated with recent pandemic Vibrio parahaemolyticus O3:K6 strains. J Clin Microbiol 2000; 38:2156–2161
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/mgen/10.1099/mgen.0.001037
Loading
Comparative genomics uncovered differences between clinical and environmental populations of Vibrio parahaemolyticus in New Zealand
M Gen 9, 001037 (2023); https://doi.org/10.1099/mgen.0.001037
/content/journal/mgen/10.1099/mgen.0.001037
/content/journal/mgen/10.1099/mgen.0.001037
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