Abstract
Single locus variants (SLVs) are bacterial sequence types that differ at only one of the seven canonical multilocus sequence typing (MLST) loci. Estimating the relative roles of recombination and point mutation in the generation of new alleles that lead to SLVs is helpful in understanding how organisms evolve. The relative rates of recombination and mutation for Campylobacter jejuni and Campylobacter coli were estimated at seven different housekeeping loci from publically available MLST data. The probability of recombination generating a new allele that leads to an SLV is estimated to be roughly seven times more than that of mutation for C. jejuni, but for C. coli recombination and mutation were estimated to have a similar contribution to the generation of SLVs. The majority of nucleotide differences (98 % for C. jejuni and 85 % for C. coli) between strains that make up an SLV are attributable to recombination. These estimates are much larger than estimates of the relative rate of recombination to mutation calculated from more distantly related isolates using MLST data. One explanation for this is that purifying selection plays an important role in the evolution of Campylobacter. A simulation study was performed to test the performance of our method under a range of biologically realistic parameters. We found that our method performed well when the recombination tract length was longer than 3 kb. For situations in which recombination may occur with shorter tract lengths, our estimates are likely to be an underestimate of the ratio of recombination to mutation, and of the importance of recombination for creating diversity in closely related isolates. A parametric bootstrap method was applied to calculate the uncertainty of these estimates.
Similar content being viewed by others
References
Biggs PJ, Fearnhead P, Hotter G, Mohan V, Collins-Emerson J, Kwan E, Besser TE, Cookson A, Carter PE, French NP (2011) Whole-genome comparison of two Campylobacter jejuni isolates of the same sequence type reveals multiple loci of different ancestral lineage. PLoS One 6(11):e27121
Clark CG, Bryden L, Cuff WR, Johnson PL, Jamieson F, Ciebin B, Wang G (2005) Use of the Oxford multilocus sequence typing protocol and sequencing of the flagellin short variable region to characterize isolates from a large outbreak of waterborne Campylobacter sp. strains in Walkerton, Ontario, Canada. J Clin Microbiol 43:2080
Dempster AP, Laird NM, Rubin DB (1977) Maximum likelihood from incomplete data via the EM algorithm. J Roy Statist Soc Ser B 39(1):1–38
Didelot X, Lawson D, Falush D (2009) Simmlst: simulation of multi-locus sequence typing data under a neutral model. Bioinformatics 25:1442
Dingle KE, Colles FM, Wareing DRA, Ure R, Fox AJ, Bolton FE, Bootsma HJ, Willems RJL, Urwin R, Maiden MCJ (2001) Multilocus sequence typing system for Campylobacter jejuni. J Clin Microbiol 39:14
Fearnhead P, Smith NGC, Barrigas M, Fox A, French N (2005) Analysis of recombination in Campylobacter jejuni from MLST population data. J Mol Evol 61:333–340
Feil EJ, Maiden MC, Achtman M, Spratt BG (1999) The relative contributions of recombination and mutation to the divergence of clones of Neisseria meningitidis. Mol Biol Evol 16:1496
Feil EJ, Smith JM, Enright MC, Spratt BG (2000) Estimating recombinational parameters in Streptococcus pneumoniae from multilocus sequence typing data. Genetics 154:1439
Feil EJ, Holmes EC, Bessen DE, Chan MS, Day NPJ, Enright MC, Goldstein R, Hood DW, Kalia A, Moore CE et al (2001) Recombination within natural populations of pathogenic bacteria: short-term empirical estimates and long-term phylogenetic consequences. Proc Natl Acad Sci 98:182
Feil EJ, Li BC, Aanensen DM, Hanage WP, Spratt BG (2004) eBURST: inferring patterns of evolutionary descent among clusters of related bacterial genotypes from multilocus sequence typing data. J Bacteriol 186:1518
Guttman DS, Dykhuizen DE (1994) Clonal divergence in Escherichia coli as a result of recombination, not mutation. Science 266:1380–1383
Hein J, Schierup MH, Wiuf C (2005) Gene genealogies, variation and evolution: a primer in coalescent theory. Oxford University Press, Oxford
Humphrey T, O’Brien S, Madsen M (2007) Campylobacters as zoonotic pathogens: a food production perspective. Int J Food Microbiol 117:237–257
Jolley KA, Maiden MCJ (2010) BIGSdb: scalable analysis of bacterial genome variation at the population level. BMC Bioinformatics 11:595
Konkel ME, Gray SA, Kim BJ, Garvis SG, Yoon J (1999) Identification of the enteropathogens Campylobacter jejuni and Campylobacter coli based on the cadF virulence gene and its product. J Clin Microbiol 37:510
Maiden MCJ, Bygraves JA, Feil EJ, Morelli G, Russell JE, Urwin R, Zhang Q, Zhou J, Zurth K, Caugant DA (1998) Multilocus sequence typing: a portable approach to the identification of clones within populations of pathogenic microorganisms. Proc Nat Acad Sci USA 95:3140
Meinersmann RJ, Hiett KL (2000) Concerted evolution of duplicate fla genes in Campylobacter. Microbiology 146:2283
Richman AD, Herrera LG, Nash D, Schierup MH (2003) Relative roles of mutation and recombination in generating allelic polymorphism at an MHC class II locus in Peromyscus maniculatus. Genet Res 82:89–99
Sarkar SF, Guttman DS (2004) Evolution of the core genome of Pseudomonas syringae, a highly clonal, endemic plant pathogen. Appl Environ Microbiol 70:1999
Schouls LM, Reulen S, Duim B, Wagenaar JA, Willems RJL, Dingle KE, Colles FM, Van Embden JDA (2003) Comparative genotyping of Campylobacter jejuni by amplified fragment length polymorphism, multilocus sequence typing, and short repeat sequencing: strain diversity, host range, and recombination. J Clin Microbiol 41:15
Sheppard SK, McCarthy ND, Falush D, Maiden MCJ (2008) Convergence of Campylobacter species: implications for bacterial evolution. Science 320:237–239
Sheppard SK, Dallas JF, Wilson DJ, Strachan NJC, McCarthy ND, et al. (2010) Evolution of an agriculture-associated disease causing Campylobacter coli clade: evidence from National Surveillance Data in Scotland. PLoS ONE 5(12)
Sheppard SK, McCarthy ND, Jolley KA, Maiden MCJ (2011) Introgression in the genus Campylobacter: generation and spread of mosaic alleles. Microbiology 157:1066–1074
Suerbaum S, Lohrengel M, Sonnevend A, Ruberg F, Kist M (2001) Allelic diversity and recombination in Campylobacter jejuni. J Bacteriol 183:2553
Tauxe RV, Nachamkin I, Blaser MJ, Tompkins LS (1992) Epidemiology of Campylobacter jejuni infections in the United States and other industrialized nations. MBio, Washington, DC
Vos M, Didelot X (2008) A comparison of homologous recombination rates in bacteria and archaea. ISME J 3:199–208
Wilson DJ, Gabriel E, Leatherbarrow AJH, Cheesbrough J, Gee S, Bolton E, Fox A, Hart CA, Diggle PJ, Fearnhead P (2009) Rapid evolution and the importance of recombination to the gastroenteric pathogen Campylobacter jejuni. Mol Biol Evol 26:385
Zhang Q, Meitzler JC, Huang S, Morishita T (2000) Sequence polymorphism, predicted secondary structures, and surface-exposed conformational epitopes of Campylobacter major outer membrane protein. Infect Immun 68:5679
Acknowledgments
The authors acknowledge the Marsden Fund project 08-MAU-099 (Cows, starlings and Campylobacter in New Zealand: unifying phylogeny, genealogy, and epidemiology to gain insight into pathogen evolution) for funding this project. This publication made use of the Campylobacter Multi Locus Sequence Typing website (http://pubmlst.org/campylobacter/) developed by Keith Jolley and sited at the University of Oxford (Jolley and Maiden 2010, BMC Bioinformatics, 11:595). The development of this site has been funded by the Wellcome Trust. BRH acknowledges the Australian Research Council (Grant FT100100031).
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Yu, S., Fearnhead, P., Holland, B.R. et al. Estimating the Relative Roles of Recombination and Point Mutation in the Generation of Single Locus Variants in Campylobacter jejuni and Campylobacter coli . J Mol Evol 74, 273–280 (2012). https://doi.org/10.1007/s00239-012-9505-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00239-012-9505-4