Epidemic clones, oceanic gene pools, and eco-LD in the free living marine pathogen vibrio parahaemolyticus

Molecular Biology and Evolution

Volumn 32, Issue 6, 2015, Pages 1396-1410

  Cui, Yujun ^a,b   Yang, Xianwei ^a,b   Didelot, Xavier ^c   Guo, Chenyi ^a   Li, Dongfang ^b   Yan, Yanfeng ^a   Zhang, Yiquan ^a   Yuan, Yanting ^b   Yang, Huanming ^b   Wang, Jian ^b   Wang, Jun ^b   Song, Yajun ^a   Zhou, Dongsheng ^a   Falush, Daniel ^d   Yang, Ruifu ^a,b  

^a BEIJING INSTITUTE OF MICROBIOLOGY AND EPIDEMIOLOGY   (China)

^b BGI SHENZHEN   (China)

^c IMPERIAL COLLEGE LONDON   (United Kingdom)

^d SWANSEA UNIVERSITY   (United Kingdom)

Author keywords

coalescent theory; molecular epidemiology; population genetics; population structure; whole genome sequencing

Indexed keywords

BACTERIAL DNA; GUANOSINE PHOSPHATE; SEA WATER;

ARTICLE; ASIA; BACTERIAL CHROMOSOME; BACTERIAL GENOME; BACTERIAL STRAIN; BACTERICIDAL ACTIVITY; BACTERIUM ISOLATE; BIOFILM; CHROMOSOME PAINTING; CLONAL EVOLUTION; CLONE; CONTROLLED STUDY; ECOTYPE; EFFECTIVE POPULATION SIZE; ENTAMOEBA COLI; GENE FLOW; GENE FREQUENCY; GENE LOCUS; GENE MUTATION; GENE POOL; GENE SEQUENCE; GENETIC ASSOCIATION; GENETIC DISTANCE; GENETIC VARIABILITY; HELICOBACTER PYLORI; HEREDITY; HOMOLOGOUS RECOMBINATION; MARINE BACTERIUM; MICROBIAL DIVERSITY; MIGRATION; MOLECULAR EPIDEMIOLOGY; NONHUMAN; PANDEMIC; PHYLOGENY; POPULATION SIZE; POPULATION STRUCTURE; QUANTITATIVE TRAIT; SIGNAL TRANSDUCTION; SINGLE NUCLEOTIDE POLYMORPHISM; SPECIES DISTRIBUTION; TYPE VI SECRETION SYSTEM; VIBRIO PARAHAEMOLYTICUS; CLASSIFICATION; DNA SEQUENCE; EPISTASIS; GENETIC RECOMBINATION; GENETICS; ISOLATION AND PURIFICATION; MEXICO; MICROBIOLOGY; PHYLOGEOGRAPHY; POPULATION GENETICS; SEA;

BACTERIA (MICROORGANISMS); VIBRIO PARAHAEMOLYTICUS;

ASIA; BIOFILMS; CHROMOSOMES, BACTERIAL; EPISTASIS, GENETIC; GENE POOL; GENETIC LOCI; GENETICS, POPULATION; GENOME, BACTERIAL; MEXICO; OCEANS AND SEAS; PHYLOGENY; PHYLOGEOGRAPHY; POLYMORPHISM, SINGLE NUCLEOTIDE; RECOMBINATION, GENETIC; SEAWATER; SEQUENCE ANALYSIS, DNA; VIBRIO PARAHAEMOLYTICUS;

EID: 84930728804     PISSN: 07374038     EISSN: 15371719     Source Type: Journal    
DOI: 10.1093/molbev/msv009     Document Type: Article

References (64)

1. Achtman M, Wagner M. 2008. Microbial diversity and the genetic nature of microbial species. Nat Rev Microbiol. 6:431-440.
2. Barrett JC, Fry B, Maller J, Daly MJ. 2005. Haploview: Analysis and visualization of LD and haplotype maps. Bioinformatics 21:263-265.
3. Boucher Y, Cordero OX, Takemura A, Hunt DE, Schliep K, Bapteste E, Lopez P, Tarr CL, Polz MF. 2011. Local mobile gene pools rapidly cross species boundaries to create endemicity within global Vibrio cholerae populations. MBio 2:e00335-10.
4. Castillo-Ramrez S, Harris SR, Holden MT, He M, Parkhill J, Bentley SD, Feil EJ. 2011. The impact of recombination on dN/dS within recently emerged bacterial clones. PLoS Pathog. 7:e1002129.
5. Charlesworth B. 2009. Fundamental concepts in genetics: effective population size and patterns of molecular evolution and variation. Nat Rev Genet. 10:195-205.
6. Charlesworth D. 2006. Balancing selection and its effects on sequences in nearby genome regions. PLoS Genet. 2:e64.
7. Cohan FM, Koeppel AF. 2008. The origins of ecological diversity in prokaryotes. Curr Biol. 18:R1024-R1034.
8. Croucher NJ, Harris SR, Fraser C, Quail MA, Burton J, van der Linden M, McGee L, von Gottberg A, Song JH, Ko KS, et al. 2011. Rapid pneumococcal evolution in response to clinical interventions. Science 331: 430-434.
9. Cui Y, Yu C, Yan Y, Li D, Li Y, Jombart T, Weinert LA, Wang Z, Guo Z, Xu L, et al. 2013. Historical variations in mutation rate in an epidemic pathogen, Yersinia pestis. Proc Natl Acad Sci U S A. 110: 577-582.
10. Delcher AL, Salzberg SL, Phillippy AM. 2003. Using MUMmer to identify similar regions in large sequence sets. Curr Protoc Bioinformatics. Chapter 10Unit 10. 3.
11. Didelot X, Bowden R, Street T, Golubchik T, Spencer C, McVean G, Sangal V, Anjum MF, Achtman M, Falush D, et al. 2011. Recombination and population structure in Salmonella enterica. PLoS Genet. 7:e1002191.
12. Didelot X, Falush D. 2007. Inference of bacterial microevolution using multilocus sequence data. Genetics 175:1251-1266.
13. Didelot X, Meric G, Falush D, Darling AE. 2012. Impact of homologous and non-homologous recombination in the genomic evolution of Escherichia coli. BMC Genomics 13:256.
14. Didelot X, Nell S, Yang I, Woltemate S, van der Merwe S, Suerbaum S. 2013. Genomic evolution and transmission of Helicobacter pylori in two South African families. Proc Natl Acad Sci U S A. 110: 13880-13885.
15. Donati C, Hiller NL, Tettelin H, Muzzi A, Croucher NJ, Angiuoli SV, Oggioni M, Dunning Hotopp JC, Hu FZ, Riley DR, et al. 2010. Structure and dynamics of the pan-genome of Streptococcus pneumoniae and closely related species. Genome Biol. 11:R107.
16. Eldon B, Wakeley J. 2006. Coalescent processes when the distribution of offspring number among individuals is highly skewed. Genetics 172: 2621-2633.
17. Falush D, Stephens M, Pritchard JK. 2007. Inference of population structure using multilocus genotype data: dominant markers and null alleles. Mol Ecol Notes. 7:574-578.
18. Falush D, Wirth T, Linz B, Pritchard JK, Stephens M, Kidd M, Blaser MJ, Graham DY, Vacher S, Perez-Perez GI, et al. 2003. Traces of human migrations in Helicobacter pylori populations. Science 299: 1582-1585.
19. Ferreira RB, Chodur DM, Antunes LC, Trimble MJ, McCarter LL. 2012. Output targets and transcriptional regulation by a cyclic dimeric GMP-responsive circuit in the Vibrio parahaemolyticus Scr network. J Bacteriol. 194:914-924.
20. Fraser C, Alm EJ, Polz MF, Spratt BG, Hanage WP. 2009. The bacterial species challenge: making sense of genetic and ecological diversity. Science 323:741-746.
21. Fraser C, Hanage WP, Spratt BG. 2005. Neutral microepidemic evolution of bacterial pathogens. Proc Natl Acad Sci U S A. 102:1968-1973.
22. Fujino T, Miwatani T, Yasuda J, Kondo M, Takeda Y, Akita Y, Kotera K, Okada M, Nishimune H, Shimizu Y, et al. 1965. Taxonomic studies on the bacterial strains isolated from cases of "shirasu" food-poisoning (Pasteurella parahaemolytica) and relatedmicroorganisms. Biken J. 8:63-71.
23. Gomelsky M. 2012. Cyclic dimeric GMP-mediated decisions in surfacegrown Vibrio parahaemolyticus: A different kind of motile-To-sessile transition. J Bacteriol. 194:911-913.
24. Gressmann H, Linz B, Ghai R, Pleissner KP, Schlapbach R, Yamaoka Y, Kraft C, Suerbaum S, Meyer TF, Achtman M. 2005. Gain and loss of multiple genes during the evolution of Helicobacter pylori. PLoS Genet. 1:e43.
25. Grissa I, Vergnaud G, Pourcel C. 2007. The CRISPRdb database and tools to display CRISPRs and to generate dictionaries of spacers and repeats. BMC Bioinformatics 8:172.
26. Guindon S, Gascuel O. 2003. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol. 52: 696-704.
27. Han H, Wong HC, Kan B, Guo Z, Zeng X, Yin S, Liu X, Yang R, Zhou D. 2008. Genome plasticity of Vibrio parahaemolyticus: microevolution of the "pandemic group". BMC Genomics 9:570.
28. Hyatt D, Chen GL, Locascio PF, Land ML, Larimer FW, Hauser LJ. 2010. Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinformatics 11:119.
29. Jolley K, Wilson D, Kriz P, McVean G, Maiden M. 2005. The influence of mutation, recombination, population history, and selection on patterns of genetic diversity in Neisseria meningitidis. Mol Biol Evol. 22: 562-569.
30. Kennemann L, Didelot X, Aebischer T, Kuhn S, Drescher B, Droege M, Reinhardt R, Correa P, Meyer TF, Josenhans C. 2011. Helicobacter pylori genome evolution during human infection. Proc Natl Acad Sci U S A. 108:5033-5038.
31. Kulick S, Moccia C, Didelot X, Falush D, Kraft C, Suerbaum S. 2008. Mosaic DNA imports with interspersions of recipient sequence after natural transformation of Helicobacter pylori. PLoS One 3:e3797.
32. Lawson DJ, Falush D. 2012. Population identification using genetic data. Annu Rev Genomics Hum Genet. 13:337-361.
33. Lawson DJ, Hellenthal G, Myers S, Falush D. 2012. Inference of population structure using dense haplotype data. PLoS Genet. 8:e1002453.
34. Letunic I, Doerks T, Bork P. 2014. SMART: recent updates, new developments and status in 2015. Nucleic Acids Res. 43:D257-260.
35. Li H, Durbin R. 2011. Inference of human population history from individual whole-genome sequences. Nature 475:493-496.
36. Li R, Zhu H, Ruan J, Qian W, Fang X, Shi Z, Li Y, Li S, Shan G, Kristiansen K, et al. 2010. De novo assembly of human genomes with massively parallel short read sequencing. Genome Res. 20:265-272.
37. Marchler-Bauer A, Zheng C, Chitsaz F, Derbyshire MK, Geer LY, Geer RC, Gonzales NR, Gwadz M, Hurwitz DI, Lanczycki CJ, et al. 2013. CDD: conserved domains and protein three-dimensional structure. Nucleic Acids Res. 41:D348-D352.
38. Martiny JB, Bohannan BJ, Brown JH, Colwell RK, Fuhrman JA, Green JL, Horner-Devine MC, Kane M, Krumins JA, Kuske CR, et al. 2006. Microbial biogeography: putting microorganisms on the map. Nat Rev Microbiol. 4:102-112.
39. Matic I, RadmanM, Rayssiguier C. 1994. Structure of recombinants from conjugational crosses between Escherichia coli donor and mismatchrepair deficient Salmonella typhimurium recipients. Genetics 136: 17-26.
40. Maynard Smith J, Smith NH, O'Rourke M, Spratt BG. 1993. How clonal are bacteria? Proc Natl Acad Sci U S A. 90:4384-4388.
41. McCarthy ND, Colles FM, Dingle KE, Bagnall MC, Manning G, Maiden MC, Falush D. 2007. Host-Associated genetic import in Campylobacter jejuni. Emerg Infect Dis. 13:267-272.
42. Moodley Y, Linz B, Yamaoka Y, Windsor HM, Breurec S, Wu J-Y, Maady A, Bernhoft S, Thiberge J-M, Phuanukoonnon S. 2009. The peopling of the Pacific from a bacterial perspective. Science 323: 527-530.
43. Nair GB, Ramamurthy T, Bhattacharya SK, Dutta B, Takeda Y, Sack DA. 2007. Global dissemination of Vibrio parahaemolyticus serotype O3:K6 and its serovariants. Clin Microbiol Rev. 20::39-48.
44. Okuda J, Ishibashi M, Hayakawa E, Nishino T, Takeda Y, Mukhopadhyay AK, Garg S, Bhattacharya SK, Nair GB, Nishibuchi M. 1997. Emergence of a unique O3:K6 clone of Vibrio parahaemolyticus in Calcutta, India, and isolation of strains from the same clonal group from Southeast Asian travelers arriving in Japan. J Clin Microbiol. 35: 3150-3155.
45. Park L. 2012. Linkage disequilibrium decay and past population history in the human genome. PLoS One 7:e46603.
46. Pritchard JK, Stephens M, Donnelly P. 2000. Inference of population structure using multilocus genotype data. Genetics 155:945-959.
47. Rocha EP, Smith JM, Hurst LD, Holden MT, Cooper JE, Smith NH, Feil EJ. 2006. Comparisons of dN/dS are time dependent for closely related bacterial genomes. J Theor Biol. 239:226-235.
48. Rosenberg NA. 2004. DISTRUCT: A program for the graphical display of population structure. Mol Ecol Notes. 4:137-138.
49. Salomon D, Gonzalez H, Updegraff BL, Orth K. 2013. Vibrio parahaemolyticus type VI secretion system 1 is activated in marine conditions to target bacteria, and is differentially regulated from system 2. PLoS One 8:e61086.
50. Shapiro BJ, Friedman J, Cordero OX, Preheim SP, Timberlake SC, Szabo G, Polz MF, Alm EJ. 2012. Population genomics of early events in the ecological differentiation of bacteria. Science 336:48-51.
51. Shen P, Huang HV. 1986. Homologous recombination in Escherichia coli: dependence on substrate length and homology. Genetics 112: 441-457.
52. Sheppard SK, McCarthy ND, Falush D, Maiden MC. 2008. Convergence of Campylobacter species: implications for bacterial evolution. Science 320:237-239.
53. Su YC, Liu C. 2007. Vibrio parahaemolyticus: A concern of seafood safety. Food Microbiol. 24:549-558.
54. Tenaillon O, Skurnik D, Picard B, Denamur E. 2010. The population genetics of commensal Escherichia coli. Nat Rev Microbiol. 8:207-217.
55. Tischler AD, Camilli A. 2004. Cyclic diguanylate (c-di-GMP) regulates Vibrio cholerae biofilm formation. Mol Microbiol. 53:857-869.
56. Voight BF, Kudaravalli S, Wen X, Pritchard JK. 2006. A map of recent positive selection in the human genome. PLoS Biol. 4:e72.
57. Wang J. 2005. Estimation of effective population sizes from data on genetic markers. Philos Trans R Soc Lond B Biol Sci. 360:1395-1409.
58. Whitlock MC, McCauley DE. 1999. Indirect measures of gene flow and migration: FST6 1/(4Nm+ 1). Heredity 82:117-125.
59. Yahara K, Furuta Y, Oshima K, Yoshida M, Azuma T, Hattori M, Uchiyama I, Kobayashi I. 2013. Chromosome painting in silico in a bacterial species reveals fine population structure. Mol Biol Evol. 30: 1454-1464.
60. Yan Y, Cui Y, Han H, Xiao X, Wong HC, Tan Y, Guo Z, Liu X, Yang R, Zhou D. 2011. Extended MLST-based population genetics and phylogeny of Vibrio parahaemolyticus with high levels of recombination. Int J Food Microbiol. 145:106-112.
61. Yang Z. 2007. PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol. 24:1586-1591.
62. Yeung PS, Boor KJ. 2004. Epidemiology, pathogenesis, and prevention of foodborne Vibrio parahaemolyticus infections. Foodborne Pathog Dis. 1:74-88.
63. Yu Y, Yang H, Li J, Zhang P, Wu B, Zhu B, Zhang Y, Fang W. 2012. Putative type VI secretion systems of Vibrio parahaemolyticus contribute to adhesion to cultured cell monolayers. Arch Microbiol. 194: 827-835.
64. Zhou Z, McCann A, Weill FX, Blin C, Nair S, Wain J, Dougan G, Achtman M. 2014. Transient Darwinian selection in Salmonella enterica serovar Paratyphi A during 450 years of global spread of enteric fever. Proc Natl Acad Sci U S A. 111:12199-12204.