1887

Abstract

The decreased costs of genome sequencing have increased the capability to apply whole-genome sequencing to epidemiological surveillance of zoonotic Campylobacter jejuni. However, knowledge of the genetic diversity of this bacteria is vital for inferring relatedness between epidemiologically linked isolates and a necessary prerequisite for correct application of this methodology. To address this issue in C. jejuni we investigated the spatial and temporal signals in the genomes of a major clonal complex and generalist lineage, ST-45 CC, by analysing the population structure and genealogy as well as applying genome-wide association analysis of 340 isolates from across Europe collected over a wide time range. The occurrence and strength of the geographical signal varied between sublineages and followed the clonal frame when present, while no evidence of a temporal signal was found. Certain sublineages of ST-45 formed discrete and genetically isolated clades containing isolates with extremely similar genomes regardless of time and location of sampling. Based on a separate data set, these monomorphic genotypes represent successful C. jejuni clones, possibly spread around the globe by rapid animal (migrating birds), food or human movement. In addition, we observed an incongruence between the genealogy of the strains and multilocus sequence typing (MLST), challenging the existing clonal complex definition and the use of whole-genome gene-by-gene hierarchical nomenclature schemes for C. jejuni.

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2016-10-01
2019-09-22
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References

  1. Abascal F., Zardoya R., Telford M. J.. 2010; TranslatorX: multiple alignment of nucleotide sequences guided by amino acid translations. Nucleic Acids Res38:W7–13 [CrossRef][PubMed]
    [Google Scholar]
  2. Achtman M.. 2012; Insights from genomic comparisons of genetically monomorphic bacterial pathogens. Philos Trans R Soc Lond B Biol Sci367:860–867 [CrossRef][PubMed]
    [Google Scholar]
  3. Altschul S. F., Madden T. L., Schäffer A. A., Zhang J., Zhang Z., Miller W., Lipman D. J.. 1997; Gapped blast and PSI-blast: a new generation of protein database search programs. Nucleic Acids Res25:3389–3402 [CrossRef][PubMed]
    [Google Scholar]
  4. Aziz R. K., Bartels D., Best A. A., DeJongh M., Disz T., Edwards R. A., Formsma K., Gerdes S., Glass E. M. et al. 2008; The RAST Server: rapid annotations using subsystems technology. BMC Genomics9:9–75 [CrossRef][PubMed]
    [Google Scholar]
  5. Bankevich A., Nurk S., Antipov D., Gurevich A. A., Dvorkin M., Kulikov A. S., Lesin V. M., Nikolenko S. I., Pham S. et al. 2012; SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol19:455–47 [CrossRef][PubMed]
    [Google Scholar]
  6. Batchelor R. A., Pearson B. M., Friis L. M., Guerry P., Wells J. M.. 2004; Nucleotide sequences and comparison of two large conjugative plasmids from different Campylobacter species. Microbiology150:3507–3517 [CrossRef][PubMed]
    [Google Scholar]
  7. Blaser M., Engberg J.. 2008; Clinical aspects of Campylobacter jejuni and Campylobacter coli infections. In Campylobacter , pp.99–121 Edited by Nachamkin I., Szymanski C., Blaser M. J.. Washington, DC: ASM Press;
    [Google Scholar]
  8. Cheng L., Connor T. R., Sirén J., Aanensen D. M., Corander J.. 2013; Hierarchical and spatially explicit clustering of DNA sequences with BAPS software. Mol Biol Evol30:1224–1228 [CrossRef][PubMed]
    [Google Scholar]
  9. Ciccarelli F. D., Doerks T., von Mering C., Creevey C. J., Snel B., Bork P.. 2006; Toward automatic reconstruction of a highly resolved tree of life. Science311:1283–1287 [CrossRef][PubMed]
    [Google Scholar]
  10. Cody A. J., McCarthy N. D., Bray J. E., Wimalarathna H. M., Colles F. M., Jansen van Rensburg M. J., Dingle K. E., Waldenström J., Maiden M. C.. 2015; Wild bird-associated Campylobacter jejuni isolates are a consistent source of human disease, in Oxfordshire, United Kingdom. Environ Microbiol Rep7:782–788 [CrossRef][PubMed]
    [Google Scholar]
  11. de Haan C. P., Kivistö R., Hakkinen M., Rautelin H., Hänninen M. L.. 2010; Decreasing trend of overlapping multilocus sequence types between human and chicken Campylobacter jejuni isolates over a decade in Finland. Appl Environ Microbiol76:5228–5236 [CrossRef][PubMed]
    [Google Scholar]
  12. de Haan C. P., Llarena A. K., Revez J., Hänninen M. L.. 2012; Association of Campylobacter jejuni metabolic traits with multilocus sequence types. Appl Environ Microbiol78:5550–5554 [CrossRef][PubMed]
    [Google Scholar]
  13. Dearlove B., Cody A., Pascoe B., Meric G., Wilson D., Sheppard S.. 2015; Rapid host switching in generalist Campylobacter strains erodes the signal for tracing human infections. ISME Journal10:721–729
    [Google Scholar]
  14. Dingle K. E., Colles F. M., Wareing D. R., Ure R., Fox A. J., Bolton F. E., Bootsma H. J., Willems R. J., Urwin R., Maiden M. C.. 2001; Multilocus sequence typing system for Campylobacter jejuni. J Clin Microbiol39:14–23 [CrossRef][PubMed]
    [Google Scholar]
  15. Dingle K. E., Colles F. M., Ure R., Wagenaar J. A., Duim B., Bolton F. J., Fox A. J., Wareing D. R., Maiden M. C.. 2002; Molecular characterization of Campylobacter jejuni clones: a basis for epidemiologic investigation. Emerg Infect Dis8:949–955 [CrossRef][PubMed]
    [Google Scholar]
  16. Drummond A. J., Suchard M. A., Xie D., Rambaut A.. 2012; Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol Biol Evol29:1969–1973 [CrossRef][PubMed]
    [Google Scholar]
  17. Drummond A. J., Bouckaert R. R.. 2015; Bayesian Evolutionary Analysis with BEAST, 1st edn. Cambridge, UK: University Printing House;
    [Google Scholar]
  18. Edgar R. C.. 2004a; muscle: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics5:113
    [Google Scholar]
  19. Edgar R. C.. 2004b; muscle: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res32:1792–1797 [CrossRef][PubMed]
    [Google Scholar]
  20. Ekseth O. K., Kuiper M., Mironov V.. 2014; orthAgogue: an agile tool for the rapid prediction of orthology relations. Bioinformatics30:734–736 [CrossRef][PubMed]
    [Google Scholar]
  21. Enright A. J., Van Dongen S., Ouzounis C. A.. 2002; An efficient algorithm for large-scale detection of protein families. Nucleic Acids Res30:1575–1584 [CrossRef][PubMed]
    [Google Scholar]
  22. European Centre for Disease Prevention and Control (ECDC) 2015; Expert Opinion on the introduction of next-generation typing methods for food- and waterborne diseases in the EU and EEA Stockholm, Sweden: ECDC;
    [Google Scholar]
  23. European Food Safety Authority (EFSA) & European Centre for Disease Prevention and Control (ECDC) 2015; The European Union summary report on antimicrobial resistance in zoonotic and indicator bacteria from humans, animals and food in 2013. EFSA J13:4036
    [Google Scholar]
  24. European Food Safety Authority (EFSA) 2010; Analysis of the baseline survey on the prevalence of Campylobacter in broiler batches and of Campylobacter and Salmonella on broiler carcasses in the EU, 2008 – part A: Campylobacter and Salmonella prevalence estimates. EFSA Journal8:1503
    [Google Scholar]
  25. European Food Safety Authority (EFSA) 2014; EFSA Scientific colloquium summary report on use of whole-genome sequencing (WGS) of food-borne pathogens for public health protection Parma, Italy: EFSA;
    [Google Scholar]
  26. Fouts D. E., Mongodin E. F., Mandrell R. E., Miller W. G., Rasko D. A., Ravel J., Brinkac L. M., DeBoy R. T., Parker C. T. et al. 2005; Major structural differences and novel potential virulence mechanisms from the genomes of multiple Campylobacter species. PLoS Biol3:e15 [CrossRef][PubMed]
    [Google Scholar]
  27. French N., Yu S., Biggs P., Holland B., Fearnhead P., Binney B., Fox A., Grove-White D., Leigh J. et al. 2014; Evolution of Campylobacter species in New Zealand. In Campylobacter Ecology and Evolution , pp.221–204 Edited by Sheppard S., Meric G.. Swansea, UK: Caister Academic Press;
    [Google Scholar]
  28. Friis C., Wassenaar T. M., Javed M. A., Snipen L., Lagesen K., Hallin P. F., Newell D. G., Toszeghy M., Ridley A. et al. 2010; Genomic characterization of Campylobacter jejuni strain M1. PloS one5e12253
    [Google Scholar]
  29. Gripp E., Hlahla D., Didelot X., Kops F., Maurischat S., Tedin K., Alter T., Ellerbroek L., Schreiber K. et al. 2011; Closely related Campylobacter jejuni strains from different sources reveal a generalist rather than a specialist lifestyle. BMC Genomics12:584 [CrossRef][PubMed]
    [Google Scholar]
  30. Habib I., Louwen R., Uyttendaele M., Houf K., Vandenberg O., Nieuwenhuis E. E., Miller W. G., van Belkum A., De Zutter L.. 2009; Correlation between genotypic diversity, lipooligosaccharide gene locus class variation, and caco-2 cell invasion potential of Campylobacter jejuni isolates from chicken meat and humans: contribution to virulotyping. Appl Environ Microbiol75:4277–4288 [CrossRef][PubMed]
    [Google Scholar]
  31. Hammer Ø., Harper D. A. T., Ryan P. D.. 2001; PAST: paleontological statistics software package for education and data analysis. Palaeontol. Elect4:1–9
    [Google Scholar]
  32. Hasegawa M., Kishino H., Yano T.. 1985; Dating of the human–ape splitting by a molecular clock of mitochondrial DNA. J Mol Evol22:160–174 [CrossRef][PubMed]
    [Google Scholar]
  33. Hendriksen R. S., Price L. B., Schupp J. M., Gillece J. D., Kaas R. S., Engelthaler D. M., Bortolaia V., Pearson T., Waters A. E. et al. 2011; Population genetics of Vibrio cholerae from Nepal in 2010: evidence on the origin of the Haitian outbreak. MBio2:e0015711 [CrossRef][PubMed]
    [Google Scholar]
  34. Hofreuter D., Tsai J., Watson R. O., Novik V., Altman B., Benitez M., Clark C., Perbost C., Jarvie T. et al. 2006; Unique features of a highly pathogenic Campylobacter jejuni strain. Infect Immun74:4694–4707 [CrossRef][PubMed]
    [Google Scholar]
  35. Hofreuter D., Novik V., Galán J. E.. 2008; Metabolic diversity in Campylobacter jejuni enhances specific tissue colonization. Cell Host Microbe4:425–433 [CrossRef][PubMed]
    [Google Scholar]
  36. Holt K. E., Parkhill J., Mazzoni C. J., Roumagnac P., Weill F. X., Goodhead I., Rance R., Baker S., Maskell D. J. et al. 2008; High-throughput sequencing provides insights into genome variation and evolution in Salmonella Typhi. Nat Genet40:987–993 [CrossRef][PubMed]
    [Google Scholar]
  37. Jaakola S., Lyytikäinen O., Huusko S., Salmenlinna S., Pirohonen J., Savolainen- Korpa C., Liitsola K., Jalava J., Toropainen M. et al. 2015; Tartuntataudit Suomessa 2014. THL Reports11:
    [Google Scholar]
  38. Jolley K. A., Maiden M. C.. 2010; BIGSdb: scalable analysis of bacterial genome variation at the population level. BMC Bioinformatics11:595 [CrossRef][PubMed]
    [Google Scholar]
  39. Kivistö R. I., Kovanen S., Skarp-de Haan A., Schott T., Rahkio M., Rossi M., Hänninen M. L.. 2014; Evolution and comparative genomics of Campylobacter jejuni ST-677 clonal complex. Genome Bbiol Evol6:2424–2438 [CrossRef]
    [Google Scholar]
  40. Kovanen S., Kivistö R., Llarena A. K., Zhang J., Kärkkäinen U. M., Tuuminen T., Uksila J., Hakkinen M., Rossi M. et al. 2016; Tracing isolates from domestic human Campylobacter jejuni infections to chicken slaughter batches and swimming water using whole-genome multilocus sequence typing. Int J Food Microbiol226:53–60 [CrossRef][PubMed]
    [Google Scholar]
  41. Kovanen S. M., Kivistö R. I., Rossi M., Hänninen M.-L.. 2014a; A combination of MLST and CRISPR typing reveals dominant Campylobacter jejuni types in organically farmed laying hens. J Appl Microbiol117:249–257 [CrossRef]
    [Google Scholar]
  42. Kovanen S. M., Kivisto R. I., Rossi M., Schott T., Karkkainen U. M., Tuuminen T., Uksila J., Rautelin H., Hänninen M.-L.. 2014b; Multilocus sequence typing (MLST) and whole-genome MLST of Campylobacter jejuni isolates from human infections in three districts during a seasonal peak in Finland. J Clin Microbiol52:4147–4154 [CrossRef]
    [Google Scholar]
  43. Kuo C. H., Ochman H.. 2009; Inferring clocks when lacking rocks: the variable rates of molecular evolution in bacteria. Biol Direct4:35 [CrossRef][PubMed]
    [Google Scholar]
  44. Kärenlampi R., Rautelin H., Schönberg-Norio D., Paulin L., Hänninen M. L.. 2007; Longitudinal study of finnish Campylobacter jejuni and C. coli isolates from humans, using multilocus sequence typing, including comparison with epidemiological data and isolates from poultry and cattle. Appl Environ Microbiol73:148–155 [CrossRef][PubMed]
    [Google Scholar]
  45. Köser C. U., Holden M. T., Ellington M. J., Cartwright E. J., Brown N. M., Ogilvy-Stuart A. L., Hsu L. Y., Chewapreecha C., Croucher N. J. et al. 2012; Rapid whole-genome sequencing for investigation of a neonatal MRSA outbreak. N Engl J Med366:2267–2275 [CrossRef][PubMed]
    [Google Scholar]
  46. Lenski R. E., Travisano M.. 1994; Dynamics of adaptation and diversification: a 10 000-generation experiment with bacterial populations. Proc Natl Acad Sci U S A91:6808–6814 [CrossRef][PubMed]
    [Google Scholar]
  47. Leopold S. R., Magrini V., Holt N. J., Shaikh N., Mardis E. R., Cagno J., Ogura Y., Iguchi A., Hayashi T. et al. 2009; A precise reconstruction of the emergence and constrained radiations of Escherichia coli O157 portrayed by backbone concatenomic analysis. Proc Natl Acad Sci U S A106:8713–8718 [CrossRef][PubMed]
    [Google Scholar]
  48. Linz B., Balloux F., Moodley Y., Manica A., Liu H., Roumagnac P., Falush D., Stamer C., Prugnolle F. et al. 2007; An African origin for the intimate association between humans and Helicobacter pylori. Nature445:915–918 [CrossRef][PubMed]
    [Google Scholar]
  49. Llarena A. K., Skarp-de Haan C. P., Rossi M., Hänninen M. L.. 2015; Characterization of the Campylobacter jejuni population in the barnacle geese reservoir. Zoonoses Public Health62:209–221 [CrossRef][PubMed]
    [Google Scholar]
  50. Llarena A. K., Huneau A., Hakkinen M., Hänninen M. L.. 2015a; Predominant Campylobacter jejuni sequence types persist in finnish chicken production. PLoS One10:e0116585 [CrossRef]
    [Google Scholar]
  51. Marttinen P., Hanage W. P., Croucher N. J., Connor T. R., Harris S. R., Bentley S. D., Corander J.. 2012; Detection of recombination events in bacterial genomes from large population samples. Nucleic Acids Res40:e6 [CrossRef][PubMed]
    [Google Scholar]
  52. McCarthy N. D., Gillespie I. A., Lawson A. J., Richardson J., Neal K. R., Hawtin P. R., Maiden M. C., O'Brien S. J.. 2012; Molecular epidemiology of human Campylobacter jejuni shows association between seasonal and international patterns of disease. Epidemiol Infect140:2247–2255 [CrossRef][PubMed]
    [Google Scholar]
  53. Morelli G., Didelot X., Kusecek B., Schwarz S., Bahlawane C., Falush D., Suerbaum S., Achtman M.. 2010; Microevolution of Helicobacter pylori during prolonged infection of single hosts and within families. PLoS Genet6:e1001036 [CrossRef][PubMed]
    [Google Scholar]
  54. Müllner P., Collins-Emerson J. M., Midwinter A. C., Carter P., Spencer S. E., van der Logt P., Hathaway S., French N. P.. 2010; Molecular epidemiology of Campylobacter jejuni in a geographically isolated country with a uniquely structured poultry industry. Appl Environ Microbiol76:2145–2154 [CrossRef][PubMed]
    [Google Scholar]
  55. Rambaut A., Lam T. T., Max Carvalho L., Pybus O. G.. 2016; Exploring the temporal structure of heterochronous sequences using TempEst (formerly Path-O-Gen). Virus Evolution2:vew007 [CrossRef]
    [Google Scholar]
  56. Reeves P. R., Liu B., Zhou Z., Li D., Guo D., Ren Y., Clabots C., Lan R., Johnson J. R. et al. 2011; Rates of mutation and host transmission for an Escherichia coli clone over 3 years. PLoS One6:e26907 [CrossRef][PubMed]
    [Google Scholar]
  57. Revez J., Hänninen M. L.. 2012; Lipooligosaccharide locus classes are associated with certain Campylobacter jejuni multilocus sequence types. Eur J Clin Microbiol Infect Dis31:2203–2209 [CrossRef][PubMed]
    [Google Scholar]
  58. Revez J., Llarena A. K., Schott T., Kuusi M., Hakkinen M., Kivistö R., Hänninen M. L., Rossi M.. 2014a; Genome analysis of Campylobacter jejuni strains isolated from a waterborne outbreak. BMC Genomics15:768 [CrossRef]
    [Google Scholar]
  59. Revez J., Zhang J., Schott T., Kivistö R., Rossi M., Hänninen M. L.. 2014b; Genomic variation between milkborne outbreak-associated Campylobacter jejuni isolates. J Clin Microbiol52:2782–2786
    [Google Scholar]
  60. Sheppard S. K., Didelot X., Meric G., Torralbo A., Jolley K. A., Kelly D. J., Bentley S. D., Maiden M. C., Parkhill J. et al. 2013; Genome-wide association study identifies vitamin B5 biosynthesis as a host specificity factor in Campylobacter. Proc Natl Acad Sci U S A110:11923–11927 [CrossRef][PubMed]
    [Google Scholar]
  61. Sheppard S. K., Cheng L., Méric G., de Haan C. P., Llarena A. K., Marttinen P., Vidal A., Ridley A., Clifton-Hadley F. et al. 2014; Cryptic ecology among host generalist Campylobacter jejuni in domestic animals. Mol Ecol23:2442–2451 [CrossRef][PubMed]
    [Google Scholar]
  62. Skarp C. P., Akinrinade O., Nilsson A. J., Ellström P., Myllykangas S., Rautelin H.. 2015; Comparative genomics and genome biology of invasive Campylobacter jejuni. Sci Rep5:17300 [CrossRef][PubMed]
    [Google Scholar]
  63. Smith E. E., Buckley D. G., Wu Z., Saenphimmachak C., Hoffman L. R., D'Argenio D. A., Miller S. I., Ramsey B. W., Speert D. P. et al. 2006; Genetic adaptation by Pseudomonas aeruginosa to the airways of cystic fibrosis patients. Proc Natl Acad Sci U S A103:8487–8492 [CrossRef][PubMed]
    [Google Scholar]
  64. Stamatakis A.. 2014; RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics30:1312–1313 [CrossRef][PubMed]
    [Google Scholar]
  65. Taboada E. N., Mackinnon J. M., Luebbert C. C., Gannon V. P., Nash J. H., Rahn K.. 2008; Comparative genomic assessment of multi-locus sequence typing: rapid accumulation of genomic heterogeneity among clonal isolates of Campylobacter jejuni. BMC Evol Biol8:229 [CrossRef][PubMed]
    [Google Scholar]
  66. Tamura K., Peterson D., Peterson N., Stecher G., Nei M., Kumar S.. 2011; mega5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol28:2731–2739 [CrossRef][PubMed]
    [Google Scholar]
  67. Treangen T. J., Ondov B. D., Koren S., Phillippy A. M.. 2014; The Harvest suite for rapid core-genome alignment and visualization of thousands of intraspecific microbial genomes. Genome Biol15:524–539 [CrossRef][PubMed]
    [Google Scholar]
  68. Vorwerk H., Huber C., Mohr J., Bunk B., Bhuju S., Wensel O., Spröer C., Fruth A., Flieger A. et al. 2015; A transferable plasticity region in Campylobacter coli allows isolates of an otherwise non-glycolytic food-borne pathogen to catabolize glucose. Mol Microbiol98:809–830 [CrossRef][PubMed]
    [Google Scholar]
  69. Weinert L. A., Chaudhuri R. R., Wang J., Peters S. E., Corander J., Jombart T., Baig A., Howell K. J., Vehkala M. et al. 2015; Erratum: genomic signatures of human and animal disease in the zoonotic pathogen Streptococcus suis. Nat Commun6: [CrossRef][PubMed]
    [Google Scholar]
  70. Wilson D. J., Gabriel E., Leatherbarrow A. J., Cheesbrough J., Gee S., Bolton E., Fox A., Hart C. A., Diggle P. J. et al. 2009; Rapid evolution and the importance of recombination to the gastroenteric pathogen Campylobacter jejuni. Mol Biol Evol26:385–397 [CrossRef][PubMed]
    [Google Scholar]
  71. Zautner A. E., Ohk C., Tareen A. M., Lugert R., Gross U.. 2012; Epidemiological association of Campylobacter jejuni groups with pathogenicity-associated genetic markers. BMC Microbiol12:171–180 [CrossRef][PubMed]
    [Google Scholar]
  72. Zhang J., Halkilahti J., Hänninen M. L., Rossi M.. 2015; Refinement of whole-genome multilocus sequence typing analysis by addressing gene paralogy. J Clin Microbiol53:1765–1767 [CrossRef][PubMed]
    [Google Scholar]
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