Article

Coalescent framework for prokaryotes undergoing interspecific homologous recombination

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Abstract

Coalescent process for prokaryote species is theoretically considered. Prokaryotes undergo homologous recombination with individuals of the same species (intraspecific recombination) and with individuals of other species (interspecific recombination). This work particularly focuses on interspecific recombination because intraspecific recombination has been well incorporated in coalescent framework. We present a simulation framework for generating SNP (single-nucleotide polymorphism) patterns that allows external DNA integration into host genome from other species. Using this simulation tool, msPro, we observed that the joint processes of intra- and interspecific recombination generate complex SNP patterns. The direct effect of interspecific recombination includes increased polymorphism. Because interspecific recombination is very rare in nature, it generates regions with exceptionally high polymorphism. Following interspecific recombination, intraspecific recombination cuts the integrated external DNA into small fragments, generating a complex SNP pattern that appears as if external DNA was integrated multiple times. The insight gained from our work using the msPro simulator will be useful for understanding and evaluating the relative contributions of intra- and interspecific recombination events in generating complex SNP patters in prokaryotes.

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References

  1. Ansari MA, Didelot X (2014) Inference of the properties of the recombination process from whole bacterial genomes. Genetics 196:253–265

  2. Awadalla P (2003) The evolutionary genomics of pathogen recombination. Nat Rev Genet 4:50–60

  3. Azad RK, Lawrence JG (2012) Detecting laterally transferred genes. In: Anisimova M (ed.) Evolutionary Genomics, Humana Press, Methods in Molecular Biology, Clifton, NJ, p 281–308

  4. Brown T, Didelot X, Wilson DJ, De Maio N (2016) SimBac: simulation of whole bacterial genomes with homologous recombination. Microb Genom 2:1–6

  5. Cohan FM (2002a) Sexual isolation and speciation in bacteria. Genetica 116:359–370

  6. Cohan FM (2002b) What are bacterial species? Annu Rev Microbiol 56:457–487

  7. Cornejo OE, Lefébure T, Bitar PDP, Lang P, Richards VP, Eilertson K et al. (2013) Evolutionary and population genomics of the cavity causing bacteria Streptococcus mutans. Mol Biol Evol 30:881–893

  8. Croucher NJ, Harris SR, Barquist L, Parkhill J, Bentley SD (2012) A high-resolution view of genome-wide pneumococcal transformation. PLoS Pathog 8:e1002745

  9. De Maio N, Wilson DJ (2017) The bacterial sequential Markov coalescent. Genetics 206:333–343

  10. Didelot X, Falush D (2007) Inference of bacterial microevolution using multilocus sequence data. Genetics 175:1251–1266

  11. Didelot X, Lawson D, Falush D (2009) SimMLST: simulation of multi-locus sequence typing data under a neutral model. Bioinformatics 25:1442–1444

  12. Didelot X, Lawson D, Darling A, Falush D (2010) Inference of homologous recombination in bacteria using whole-genome sequences. Genetics 186:1435–1449

  13. Didelot X, Maiden MCJ (2010) Impact of recombination on bacterial evolution. Trends Microbiol 18:315–322

  14. Dobrindt U, Hochhut B, Hentschel U, Hacker J (2004) Genomic islands in pathogenic and environmental microorganisms. Nat Rev Microbiol 2:414–424

  15. Donati C, Hiller NL, Tettelin H, Muzzi A, Croucher NJ, Angiuoli SV et al (2010) Structure and dynamics of the pan-genome of Streptococcus pneumoniae and closely related species. Genome Biol 11:R107

  16. Donnelly P, Kurtz TG (1999) Genealogical processes for fleming-viot models with selection and recombination. Ann Appl Probab 9:1091–1148

  17. Doolittle WF, Papke RT (2006) Genomics and the bacterial species problem. Genome Biol 7:e116

  18. Earle SG, Wu CH, Charlesworth J, Stoesser N, Gordon NC, Walker TM et al. (2016) Identifying lineage effects when controlling for population structure improves power in bacterial association studies. Nat Microbiol 1:16041

  19. Falush D, Kraft C, Taylor NS, Correa P, Fox JG, Achtman M et al. (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 98:15056–15061

  20. 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

  21. Fraser C, Hanage WP, Spratt BG (2007) Recombination and the nature of bacterial speciation. Science 315:476–480

  22. Griffiths RC, Marjoram P (1996) Ancestral inference from samples of DNA sequences with recombination. J Comput Biol 3:479–502

  23. Hartl DL, Clark AG (2007) Principles of population genetics. Sinauer Associates, Sunderland

  24. Haven J, Vargas LC, Mongodin EF, Xue V, Hernandez Y, Pagan P et al (2011) Pervasive recombination and sympatric genome diversification driven by frequency-dependent selection in Borrelia burgdorferi, the lyme disease bacterium. Genetics 189:951–966

  25. Hudson RR (1983a) Properties of a neutral allele model with intragenic recombination. Theor Popul Biol 23:183–201

  26. Hudson RR (1983b) Testing the constant-rate neutral allele model with protein sequence data. Evolution 37:203–217

  27. Hudson RR (1990) Gene genealogies and the coalescent process. Oxf Surv Evol Biol 7:1–43

  28. Hudson RR (2001) Two-locus sampling distributions and their application. Genetics 159:1805–1817

  29. Hudson RR (2002) Generating samples under a wright-fisher neutral model of genetic variation. Bioinformatics 18:337–338

  30. Jolley KA, Wilson DJ, Kriz P, McVean G, Maiden MCJ (2005) The influence of mutation, recombination, population history, and selection on patterns of genetic diversity in Neisseria meningitidis. Mol Biol Evol 22:562–569

  31. Kingman JF (1982) On the genealogy of large populations. J Appl Probab 19:27–43

  32. Krone SM, Neuhauser C (1997) Ancestral processes with selection. Theor Popul Biol 51:210–237

  33. Lawrence JG (2013) Gradual speciation: Further entangling the tree of life. In: Gophna U (ed.) Lateral Gene Transfer in Evolution. Springer, New York, NY, p 243–262

  34. Lin EA, Zhang XS, Levine SM, Gill SR, Falush D, Blaser MJ (2009) Natural transformation of Helicobacter pylori involves the integration of short dna fragments interrupted by gaps of variable size. PLoS Pathog 5:e1000337

  35. Majewski J, Cohan FM (1998) The effect of mismatch repair and heteroduplex formation on sexual isolation in Bacillus. Genetics 148:13–18

  36. McVean G, Awadalla P, Fearnhead P (2002) A coalescent-based method for detecting and estimating recombination from gene sequences. Genetics 160:1231–1241

  37. Mell JC, Lee JY, Firme M, Sinha S, Redfield RJ (2014) Extensive cotransformation of natural variation into chromosomes of naturally competent Haemophilus influenzae. G3 4:717–731

  38. Nordborg M (2001) Coalescent theory. In: Balding DJ, Bishop M, Cannings C (eds.) Handbook of statistical genetics. Wiley-Blackwell, Chichester, UK

  39. Ochman H, Lawrence JG, Groisman EA (2000) Lateral gene transfer and the nature of bacterial innovation. Nature 405:299–304

  40. Pérez-Losada M, Browne EB, Madsen A, Wirth T, Viscidi RP, Crandall KA (2006) Population genetics of microbial pathogens estimated from multilocus sequence typing (MLST) data. Infect Genet Evol 6:97–112

  41. Rosen MJ, Davison M, Bhaya D, Fisher DS (2015) Fine-scale diversity and extensive recombination in a quasisexual bacterial population occupying a broad niche. Science 348:1019–1023

  42. Sawyer S (1989) Statistical tests for detecting gene conversion. Mol Biol Evol 6:526–538

  43. Shapiro BJ, Friedman J, Cordero OX, Preheim SP, Timberlake SC, Szabó G et al. (2012) Population genomics of early events in the ecological differentiation of bacteria. Science 336:48–51

  44. Shen P, Huang HV (1986) Homologous recombination in Escherichia coli: dependence on substrate length and homology. Genetics 112:441–457

  45. Snyder L, Peters JE, Henkin TM, Champness W (2013) Molecular genetics of bacteria. ASM Press, Washington, DC

  46. Tajima F (1983) Evolutionary relationship of DNA sequences in finite populations. Genetics 105:437–460

  47. Takuno S, Kado T, Sugino RP, Nakhleh L, Innan H (2012) Population genomics in bacteria: a case study of Staphylococcus aureus. Mol Biol Evol 29:797–809

  48. Touchon M, Hoede C, Tenaillon O, Barbe V, Baeriswyl S, Bidet P et al (2009) Organised genome dynamics in the Escherichia coli species results in highly diverse adaptive paths. PLoS Genet 5:e1000344

  49. Wakeley J (2008) Coalescent theory: An introduction. Roberts and Company, Greenwood Village, Colorado

  50. Wirth T, Falush D, Lan R, Colles F, Mensa P, Wieler LH et al. (2006) Sex and virulence in Escherichia coli: an evolutionary perspective. Mol Microbiol 60:1136–1151

  51. Wiuf C, Hein J (2000) The coalescent with gene conversion. Genetics 155:451–462

  52. Yahara K, Didelot X, Ansari MA, Sheppard SK, Falush D (2014) Efficient inference of recombination hot regions in bacterial genomes. Mol Biol Evol 31:1593–1605

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Acknowledgements

The authors very much thank the three reviewers for their useful and kind comments that improved the manuscript. This work was supported in part by the Japan Society for the Promotion of Science (JSPS).

Author information

Affiliations

  1. Graduate University for Advanced Studies, Hayama, Kanagawa, 240-0193, Japan

    • Tetsuya Akita
    • , Shohei Takuno
    •  & Hideki Innan
  2. National Research Institute of Far Seas Fisheries, Fisheries Research Agency, Yokohama, Kanagawa, 236-8648, Japan

    • Tetsuya Akita

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Conflict of interest

The authors declare that they have no competing interests.

Corresponding author

Correspondence to Hideki Innan.

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