1887

Microbial Genomics logo

Volume 6, Issue 12

Co-existence of multiple distinct lineages in serotype O4:K12 Open Access

Abstract

is an important cause of foodborne gastroenteritis globally. Thermostable direct haemolysin (TDH) and the TDH-related haemolysin are the two key virulence factors in pathogenicity islands harbour the genes encoding these two haemolysins. The serotyping of is based on the combination of O and K antigens. Frequent recombination has been observed in , including in the genomic regions encoding the O and K antigens. serotype O4:K12 has caused gastroenteritis outbreaks in the USA and Spain. Recently, outbreaks caused by this serotype of have been reported in China. However, the relationships among this serotype of strains isolated in different regions have not been addressed. Here, we investigated the genome variation of the serotype O4:K12 using the whole-genome sequences of 29 isolates. We determined five distinct lineages in this strain collection. We observed frequent recombination among different lineages. In contrast, little recombination was observed within each individual lineage. We showed that the lineage of this serotype of isolated in America was different from those isolated in Asia and identified genes that exclusively existed in the strains isolated in America. Pan-genome analysis showed that strain-specific and cluster-specific genes were mostly located in the genomic islands. Pan-genome analysis also showed that the vast majority of the accessory genes in the O4:K12 serotype of were acquired from within the genus . Hence, we have shown that multiple distinct lineages exist in serotype O4:K12 and have provided more evidence about the gene segregation found in isolated in different continents.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): MLST , pathogenic island , population structure , recombination , V. parahaemolyticus and whole genome sequencing
Funding
This study was supported by the:
  • Ministry of Health, Shenzhen, China (Award SZSM201811071)
    • Principle Award Recipient: Qinghua Hu
  • Ministry of Science and Technology of China (Award 2018ZX10714-002)
    • Principle Award Recipient: Bo Pang
  • Ministry of Science and Technology of China (Award 2015CB554201)
    • Principle Award Recipient: Biao Kan
  • Ministry of Science and Technology of China (Award 2017YFC1200800)
    • Principle Award Recipient: Zhenpeng Li
  • Ministry of Science and Technology of China (Award 2016YFC1200103)
    • Principle Award Recipient: Bo Pang
© 2020 The Authors
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
Loading

Article metrics loading...

/content/journal/mgen/10.1099/mgen.0.000287
2019-10-04
2024-04-19
Loading full text...

Full text loading...

/deliver/fulltext/mgen/6/12/mgen000287.html?itemId=/content/journal/mgen/10.1099/mgen.0.000287&mimeType=html&fmt=ahah

References

  1. Honda T, Abad-Lapuebla MA, Ni YX, Yamamoto K, Miwatani T. Characterization of a new thermostable direct haemolysin produced by a Kanagawa-phenomenon-negative clinical isolate of Vibrio parahaemolyticus . J Gen Microbiol 1991; 137:253–259 [View Article][PubMed]
     [Google Scholar]
  2. Shirai H, Ito H, Hirayama T, Nakamoto Y, Nakabayashi N et al. Molecular epidemiologic evidence for association of thermostable direct hemolysin (tdh) and tdh-related hemolysin of Vibrio parahaemolyticus with gastroenteritis. Infect Immun 1990; 58:3568–3573[PubMed]
     [Google Scholar]
  3. Takeda Y. Thermostable direct hemolysin of Vibrio parahaemolyticus . Pharmacol Ther 1982; 19:123–146 [View Article][PubMed]
     [Google Scholar]
  4. Hurley CC, Quirke A, Reen FJ, Boyd EF. Four genomic islands that mark post-1995 pandemic Vibrio parahaemolyticus isolates. BMC Genomics 2006; 7:104 [View Article][PubMed]
     [Google Scholar]
  5. Park KS, Ono T, Rokuda M, Jang MH, Okada K et al. Functional characterization of two type III secretion systems of Vibrio parahaemolyticus . Infect Immun 2004; 72:6659–6665 [View Article][PubMed]
     [Google Scholar]
  6. Okada N, Iida T, Park K-S, Goto N, Yasunaga T et al. Identification and characterization of a novel type III secretion system in trh-positive Vibrio parahaemolyticus strain TH3996 reveal genetic lineage and diversity of pathogenic machinery beyond the species level. Infect Immun 2009; 77:904–913 [View Article][PubMed]
     [Google Scholar]
  7. Makino K, Oshima K, Kurokawa K, Yokoyama K, Uda T et al. Genome sequence of Vibrio parahaemolyticus: a pathogenic mechanism distinct from that of V cholerae . The Lancet 2003; 361:743–749 [View Article]
     [Google Scholar]
  8. Xu F, Gonzalez-Escalona N, Drees KP, Sebra RP, Cooper VS et al. Parallel evolution of two clades of an Atlantic-endemic pathogenic lineage of Vibrio parahaemolyticus by independent acquisition of related pathogenicity islands. Appl Environ Microbiol 2017; 83:e01168-17 [View Article][PubMed]
     [Google Scholar]
  9. Chen Y, Stine OC, Badger JH, Gil AI, Nair GB et al. Comparative genomic analysis of Vibrio parahaemolyticus: serotype conversion and virulence. BMC Genomics 2011; 12:294 [View Article][PubMed]
     [Google Scholar]
  10. Joseph SW, Colwell RR, Kaper JB. Vibrio parahaemolyticus and related halophilic vibrios. CRC Crit Rev Microbiol 1982; 10:77–124 [View Article]
     [Google Scholar]
  11. Lu X, Zhou H, Du X, Liu S, Xu J et al. Population analysis of clinical and environmental Vibrio parahaemolyticus isolated from eastern provinces in China by removing the recombinant SNPs in the MLST loci. Infect Genet Evol 2016; 45:303–310 [View Article][PubMed]
     [Google Scholar]
  12. Cui Y, Yang X, Didelot X, Guo C, Li D et al. Epidemic clones, oceanic gene pools, and Eco-LD in the free living marine pathogen Vibrio parahaemolyticus . Mol Biol Evol 2015; 32:1396–1410 [View Article][PubMed]
     [Google Scholar]
  13. Daniels NA, MacKinnon L, Bishop R, Altekruse S, Ray B et al. Vibrio parahaemolyticus infections in the United States, 1973-1998. J Infect Dis 2000; 181:1661–1666 [View Article][PubMed]
     [Google Scholar]
  14. Martinez-Urtaza J, Baker-Austin C, Jones JL, Newton AE, Gonzalez-Aviles GD et al. Spread of Pacific Northwest Vibrio parahaemolyticus strain. N Engl J Med 2013; 369:1573–1574 [View Article][PubMed]
     [Google Scholar]
  15. Chowdhury A, Ishibashi M, Thiem VD, Tuyet DTN, Tung TV et al. Emergence and serovar transition of Vibrio parahaemolyticus pandemic strains isolated during a diarrhea outbreak in Vietnam between 1997 and 1999. Microbiol Immunol 2004; 48:319–327 [View Article][PubMed]
     [Google Scholar]
  16. González-Escalona N, Cachicas V, Acevedo C, Rioseco ML, Vergara JA et al. Vibrio parahaemolyticus diarrhea, Chile, 1998 and 2004. Emerg Infect Dis 2005; 11:129–131 [View Article][PubMed]
     [Google Scholar]
  17. Li Y, Xie X, Shi X, Lin Y, Qiu Y et al. Vibrio parahaemolyticus, southern coastal region of China, 2007-2012. Emerg Infect Dis 2014; 20:685–688 [View Article][PubMed]
     [Google Scholar]
  18. 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]
  19. Delcher AL, Salzberg SL, Phillippy AM. Using MUMmer to identify similar regions in large sequence sets. Curr Protoc Bioinformatics 2003; 00:10.3.1–10.310 [View Article]
     [Google Scholar]
  20. Didelot X, Wilson DJ. ClonalFrameML: efficient inference of recombination in whole bacterial genomes. PLoS Comput Biol 2015; 11:e1004041 [View Article][PubMed]
     [Google Scholar]
  21. Stamatakis A. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 2006; 22:2688–2690 [View Article][PubMed]
     [Google Scholar]
  22. Letunic I, Bork P. Interactive tree of life (iTOL) v3: an online tool for the display and annotation of phylogenetic and other trees. Nucleic Acids Res 2016; 44:W242–W245 [View Article][PubMed]
     [Google Scholar]
  23. Seemann T. Prokka: rapid prokaryotic genome annotation. Bioinformatics 2014; 30:2068–2069 [View Article][PubMed]
     [Google Scholar]
  24. Page AJ, Cummins CA, Hunt M, Wong VK, Reuter S et al. Roary: rapid large-scale prokaryote pan genome analysis. Bioinformatics 2015; 31:3691–3693 [View Article][PubMed]
     [Google Scholar]
  25. Zhou Z, Alikhan NF, Sergeant MJ, Luhmann N, Vaz C et al. GrapeTree: visualization of core genomic relationships among 100,000 bacterial pathogens. Genome Res 2018; 28:1395–1404 [View Article]
     [Google Scholar]
  26. Nilsson WB, Turner JW. The thermostable direct hemolysin-related hemolysin (trh) gene of Vibrio parahaemolyticus: sequence variation and implications for detection and function. J Microbiol Methods 2016; 126:1–7 [View Article][PubMed]
     [Google Scholar]
  27. Gonzalez-Escalona N, Strain EA, De Jesús AJ, Jones JL, Depaola A. Genome sequence of the clinical O4:K12 serotype Vibrio parahaemolyticus strain 10329. J Bacteriol 2011; 193:3405–3406 [View Article][PubMed]
     [Google Scholar]
  28. 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]
  29. Martinez-Urtaza J, Powell A, Jansa J, Rey JLC, Montero OP et al. Epidemiological investigation of a foodborne outbreak in Spain associated with U.S. West Coast genotypes of Vibrio parahaemolyticus . Springerplus 2016; 5:87 [View Article][PubMed]
     [Google Scholar]
  30. Yang C, Pei X, Wu Y, Yan L, Yan Y et al. Recent mixing of Vibrio parahaemolyticus populations. Isme J 2019; 15:
     [Google Scholar]
  31. Holt KE, Wertheim H, Zadoks RN, Baker S, Whitehouse CA et al. Genomic analysis of diversity, population structure, virulence, and antimicrobial resistance in Klebsiella pneumoniae, an urgent threat to public health. Proc Natl Acad Sci USA 2015; 112:E3574–E3581 [View Article][PubMed]
     [Google Scholar]
  32. Iguchi T, Kondo S, Hisatsune K. Vibrio parahaemolyticus O serotypes from O1 to O13 all produce R-type lipopolysaccharide: SDS-PAGE and compositional sugar analysis. FEMS Microbiol Lett 1995; 130:287–292 [View Article]
     [Google Scholar]
  33. Ishibashi M, Shimada K, Honda T, Sugiyama T, Miwatani J. Current status of OK serotype combinations of Vibrio parahaemolyticus . Nippon Saikingaku Zasshi 2000; 55:539–541 [View Article]
     [Google Scholar]
  34. Nair GB, Ramamurthy T, Bhattacharya SK, Dutta B, Takeda Y et al. Global dissemination of Vibrio parahaemolyticus serotype O3:K6 and its serovariants. Clin Microbiol Rev 2007; 20:39–48 [View Article][PubMed]
     [Google Scholar]
  35. Guo X, Liu B, Chen M, Wang Y, Wang L et al. Genetic and serological identification of three Vibrio parahaemolyticus strains as candidates for novel provisional O serotypes. Int J Food Microbiol 2017; 245:53–58 [View Article][PubMed]
     [Google Scholar]
  36. Chen M, Guo D, Wong H-C, Zhang X, Liu F et al. Development of O-serogroup specific PCR assay for detection and identification of Vibrio parahaemolyticus . Int J Food Microbiol 2012; 159:122–129 [View Article][PubMed]
     [Google Scholar]
  37. 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 USA 2009; 106:15442–15447 [View Article][PubMed]
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/mgen/10.1099/mgen.0.000287
Loading
Co-existence of multiple distinct lineages in Vibrio parahaemolyticus serotype O4:K12
M Gen 6, e000287 (2020); https://doi.org/10.1099/mgen.0.000287
/content/journal/mgen/10.1099/mgen.0.000287
/content/journal/mgen/10.1099/mgen.0.000287
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF

Supplementary material 2

EXCEL

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