Location of Repository

Lineage specific recombination rates and microevolution in Listeria monocytogenes

By Henk C. den Bakker, Xavier Didelot, Esther D Fortes, Kendra K Nightingale and Martin Wiedmann

Abstract

Background: The bacterium Listeria monocytogenes is a saprotroph as well as an opportunistic human foodborne pathogen, which has previously been shown to consist of at least two widespread lineages (termed lineages I and II) and an uncommon lineage (lineage III). While some L. monocytogenes strains show evidence for considerable diversification by homologous recombination, our understanding of the contribution of recombination to L. monocytogenes evolution is still limited. We therefore used\ud STRUCTURE and ClonalFrame, two programs that model the effect of recombination, to make inferences about the population structure and different aspects of the recombination process in L. monocytogenes. Analyses were performed using sequences for seven loci (including the house-keeping genes gap, prs, purM and ribC, the stress response gene sigB, and the virulence genes actA and inlA) for 195 L. monocytogenes isolates.\ud Results: Sequence analyses with ClonalFrame and the Sawyer's test showed that recombination is more\ud prevalent in lineage II than lineage I and is most frequent in two house-keeping genes (ribC and purM) and the two virulence genes (actA and inlA). The relative occurrence of recombination versus point mutation is about six times higher in lineage II than in lineage I, which causes a higher genetic variability in lineage II. Unlike lineage I, lineage II represents a genetically heterogeneous population with a relatively high proportion (30% average) of genetic material imported from external sources. Phylograms, constructed with correcting for recombination, as well as Tajima's D data suggest that both lineages I and II have suffered a population bottleneck.\ud Conclusion: Our study shows that evolutionary lineages within a single bacterial species can differ\ud considerably in the relative contributions of recombination to genetic diversification. Accounting for recombination in phylogenetic studies is critical, and new evolutionary models that account for the possibility of changes in the rate of recombination would be required. While previous studies suggested that only L. monocytogenes lineage I has experienced a recent bottleneck, our analyses clearly show that lineage II experienced a bottleneck at about the same time, which was subsequently obscured by abundant\ud homologous recombination after the lineage II bottleneck. While lineage I and lineage II should be considered separate species from an evolutionary viewpoint, maintaining single species name may be warranted since both lineages cause the same type of human disease

Topics: QR
Publisher: BioMed Central Ltd.
Year: 2008
OAI identifier: oai:wrap.warwick.ac.uk:516

Suggested articles

Preview

Citations

  1. (2006). Application of phylogenetic networks in evolutionary studies. Mol Biol Evol
  2. (1995). Aquadro C: Properties of statistical tests of neutrality for DNA polymorphism data. Genetics
  3. (2006). Belkhir K: Mutation hot spots in mammalian mitochondrial DNA. Genome Res doi
  4. (2008). Brisse S: A New Perspective on Listeria monocytogenes Evolution. PLoS Pathog doi
  5. (1997). CA: Ribotypes and virulence gene polymorphisms suggest three distinct Listeria monocytogenes lineages with differences in pathogenic potential. Infect Immun
  6. (2003). Champness W: Molecular Genetics of Bacteria. 2nd edition. doi
  7. (1994). Clonal divergence in Escherichia coli as a result of recombination, not mutation. Science doi
  8. (2006). CW: Analysis of core housekeeping and virulence genes reveals cryptic lineages of Clostridium perfringens that are associated with distinct disease presentations. Genetics doi
  9. (1992). DB: Inference from Iterative Simulation Using Multiple Sequences. Statistical Science doi
  10. (2004). DISTRUCT: a program for the graphical display of population structure. Mol Ecol Notes doi
  11. (2003). DNA polymorphism analyses by the coalescent and other methods. Bioinformatics doi
  12. (2001). Do bacteria have sex? Nat Rev Genet doi
  13. (2001). E: The relative contributions of recombination and point mutation to the diversification of bacterial clones. Curr Opin Microbiol doi
  14. (2004). Ecology and transmission of Listeria monocytogenes infecting ruminants and in the farm environment. Appl Environ Microbiol doi
  15. (2003). et al.: Traces of human migrations in Helicobacter pylori populations. Science
  16. (2005). Evolution and molecular phylogeny of Listeria monocytogenes isolated from human and animal listeriosis cases and foods. doi
  17. (2006). F: Listeria monocytogenes subgroups IIIA, IIIB, and IIIC delineate genetically distinct populations with varied pathogenic potential. doi
  18. (1985). Factors determining the accuracy of cladogram estimation – evaluation using computer-simulation. Evolution doi
  19. (2007). Falush D: Inference of bacterial microevolution using multilocus sequence data. Genetics doi
  20. (2005). Fuzzy species among recombinogenic bacteria.
  21. (1999). GENECONV: A computer package for the statistical detection of gene conversion. Distributed by the author, Department of mathematics, Washington University in St louis
  22. (2006). Genetic and Phenotypic Characterization of Listeria monocytogenes lineage III. doi
  23. (2008). Genome-wide analyses reveal lineage specific contributions of positive selection and recombination to the evolution of Listeria monocytogenes. doi
  24. (2006). How the bacterial pathogen Listeria monocytogenes mediates the switch from environmental Dr. Jekyll to pathogenic Mr. Hyde. Infect Immun doi
  25. (2000). Identification in Listeria monocytogenes of MecA, a homologue of the Bacillus subtilis competence regulatory protein. doi
  26. (2003). Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics doi
  27. (2000). Inference of population structure using multilocus genotype data. Genetics doi
  28. (2004). Intraspecific phylogeny and lineage group identification based on the prfA virulence gene cluster of Listeria monocytogenes. doi
  29. (1995). Listeria monocytogenes exists in at least three evolutionary lines: evidence from flagellin, invasive associated protein and listeriolysin O genes. doi
  30. (2004). Listeria monocytogenes isolates from foods and humans form distinct but overlapping populations. Appl Environ Microbiol doi
  31. (2007). MC: Species status of Neisseria gonorrhoeae: evolutionary and epidemiological inferences from multilocus sequence typing. doi
  32. (2005). MC: The influence of mutation, recombination, population history, and selection on patterns of genetic diversity in Neisseria meningitidis. Mol Biol Evol
  33. (1999). MC: The influence of recombination on the population structure and evolution of the human pathogen Neisseria meningitidis. Mol Biol Evol doi
  34. (1981). McMorris FR: Consensus n-Trees. doi
  35. (2006). Molecular characterization of Listeria monocytogenes from natural and urban environments. J Food Prot doi
  36. (1990). Molecular evolution of the Escherichia coli chromosome. III. Clonal frames. Genetics
  37. (2004). Multilocus sequence typing of Listeria monocytogenes by use of hypervariable genes reveals clonal and recombination histories of three lineages. Appl Environ Microbiol doi
  38. (2005). Neutral microepidemic evolution of bacterial pathogens. doi
  39. (2006). Ochman H: Of what use is sex to bacteria? Curr Biol doi
  40. (2004). Pagotto F: Selective discrimination of Listeria monocytogenes epidemic strains by a mixed-genome DNA microarray compared to discrimination by pulsed-field gel electrophoresis, ribotyping, and multilocus sequence typing. doi
  41. (2001). Recombination and mutation during long-term gastric colonization by Helicobacter pylori: estimates of clock rates, recombination size, and minimal age. Proc Natl Acad Sci USA doi
  42. (2007). Recombination and positive selection contribute to evolution of Listeria monocytogenes inlA. doi
  43. (2007). Recombination and the nature of bacterial speciation. Science doi
  44. (2006). Sex and virulence in Escherichia coli: an evolutionary perspective. Mol Microbiol doi
  45. (2007). Stanhope MJ: Evolution of the core and pan-genome of Streptococcus: positive selection, recombination, and genome composition. Genome Biol doi
  46. (1989). Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics doi
  47. (2001). Statistical tests of selective neutrality in the age of genomics. Heredity doi
  48. (2007). Temporal fragmentation of speciation in bacteria. Science doi
  49. (1982). The Coalescent. Stochastic Processes and their Applications doi
  50. (2000). The genetic legacy of the Quaternary ice ages. Nature
  51. (2006). VN: Attributing risk to Listeria monocytogenes subgroups: dose response in relation to genetic lineages. J Food Prot

To submit an update or takedown request for this paper, please submit an Update/Correction/Removal Request.