A neutral theory of genome evolution and the frequency distribution of genes

BMC Genomics

Volumn 13, Issue 1, 2012, Pages

  Haegeman, Bart ^a   Weitz, Joshua S ^b  

^a UMR 729 MISTEA   (France)

^b GEORGIA INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

Bacteria; Neutral model; Pan genome; Population genomics; Selection

Indexed keywords

ARTICLE; BACTERIAL GENETICS; BACTERIAL VIRULENCE; CONTROLLED STUDY; GENE FREQUENCY; GENE LOSS; GENE TRANSFER; GENETIC MODEL; GENETIC VARIABILITY; GENOME ANALYSIS; GENOME SIZE; MICROBIAL POPULATION DYNAMICS; MOLECULAR EVOLUTION; NEUTRAL GENE THEORY; NONHUMAN; POPULATION GENETIC STRUCTURE; POPULATION GROWTH; POPULATION SIZE; PREDICTION; QUANTITATIVE TRAIT; BACTERIAL GENOME; BACTERIUM; BIOLOGICAL MODEL; GENETICS;

BACTERIA (MICROORGANISMS);

BACTERIA; EVOLUTION, MOLECULAR; GENE FREQUENCY; GENOME, BACTERIAL; MODELS, GENETIC;

EID: 84861206683     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-13-196     Document Type: Article

References (48)

1. Tettelin H, Masignani V, Cieslewicz MJ, Donati C, Medini D, Ward NL, Angiuoli SV, Crabtree J, Jones AL, Durkin AS, DeBoy RT, Davidsen TM, Mora M, Scarselli M, Margarit, Peterson JD, Hauser CR, Sundaram JP, Nelson WC, Madupu R, Brinkac LM, Dodson RJ, Rosovitz MJ, Sullivan SA, Daugherty SC, Haft DH, Selengut J, Gwinn ML, Zhou L, Zafar N, Khouri H, Radune D, Dimitrov G, Watkins K, O'Connor KJB, Smith S, Utterback TR, White O, Rubens CE, Grandi G, Madoff LC, Kasper DL, Telford JL, Wessels MR, Rappuoli R, Fraser CM. Genome analysis of multiple pathogenic isolates of Streptococcus agalactiae: Implications for the microbial "pan-genome. Proc Natl Acad Sci USA 2005, 102(39):13950-13955. 10.1073/pnas.0506758102, 1216834, 16172379.
2. Hotopp JDC, Grifantini R, Kumar N, Tzeng YLL, Fouts D, Frigimelica E, Draghi M, Giuliani MMM, Rappuoli R, Stephens DS, Grandi G, Tettelin H. Comparative genomics of Neisseria meningitidis: core genome, islands of horizontal transfer and pathogen-specific genes. Microbiology 2006, 152(12):3733-3749. 10.1099/mic.0.29261-0, 17159225.
3. Hogg J, Hu F, Janto B, Boissy R, Hayes J, Keefe R, Post JC, Ehrlich G. Characterization and modeling of the Haemophilus influenzae core and supragenomes based on the complete genomic sequences of Rd and 12 clinical nontypeable strains. Genome Biol 2007, 8(6):R103+. 2394751, 17550610.
4. Hiller NL, Janto B, Hogg JS, Boissy R, Yu S, Powell E, Keefe R, Ehrlich NE, Shen K, Hayes J, Barbadora K, Klimke W, Dernovoy D, Tatusova T, Parkhill J, Bentley SD, Post JC, Ehrlich GD, Hu FZ. Comparative genomic analyses of seventeen Streptococcus pneumoniae strains: insights into the pneumococcal supragenome. J Bacteriol 2007, 189(22):8186-8195. 10.1128/JB.00690-07, 2168654, 17675389.
5. Rasko DA, Rosovitz MJ, Myers GSA, Mongodin EF, Fricke WF, Gajer P, Crabtree J, Sebaihia M, Thomson NR, Chaudhuri R, Henderson IR, Sperandio V, Ravel J. The pangenome structure of Escherichia coli: comparative genomic analysis of E. coli commensal and pathogenic isolates. J Bacteriol 2008, 190(20):6881-6893. 10.1128/JB.00619-08, 2566221, 18676672.
6. Holt KE, Parkhill J, Mazzoni CJ, Roumagnac P, Weill FX, Goodhead I, Rance R, Baker S, Maskell D, Wain J, Dolecek C, Achtman M, Dougan G. High-throughput sequencing provides insights into genome variation and evolution in Salmonella Typhi. Nat Gen 2008, 40(8):987-993.
7. Reno ML, Held NL, Fields CJ, Burke PV, Whitaker RJ. Biogeography of the Sulfolobus islandicus pan-genome. Proc Natl Acad Sci USA 2009, 106(21):8605-8610. 10.1073/pnas.0808945106, 2689034, 19435847.
8. Schoen C, Tettelin H, Parkhill J, Frosch M. Genome flexibility in Neisseria meningitidis. Vaccine 2009, 275(S2):B103-B111.
9. Chen PE, et al. Genome characterization of the Yersinia genus. Genome Biol 2010, 11(1):R1. 10.1186/gb-2010-11-1-r1, 2847712, 20047673.
10. D'Auria G, Jimenez-Hernandez N, Peris-Bondia F, Moya A, Latorre A. Legionella pneumophila pangenome reveals strain-specific virulence factors. BMC Genomics 2010, 17:181.
11. Lapierre P, Gogarten JP. Estimating the size of the bacterial pan-genome. Trends in Genet 2009, 25(3):107-110.
12. Hubbell SP. The Unified Neutral Theory of Biodiversity and Biogeography 2001, Princeton: Princeton University Press.
13. Gravel D, Canham CD, Beaudet M, Messier C. Reconciling niche and neutrality: the continuum hypothesis. Ecol Lett 2006, 9(4):399-409. 10.1111/j.1461-0248.2006.00884.x, 16623725.
14. Adler PB, HilleRisLambers J, Levine JM. A niche for neutrality. Ecol Lett 2007, 10(2):95-104. 10.1111/j.1461-0248.2006.00996.x, 17257097.
15. Rosindell J, Hubbell SP, Etienne RS. The unified neutral theory of biodiversity and biogeography at age ten. Trends in Ecol & Evol 2011, 26(7):340-348. 10.1016/j.tree.2011.03.024, 22639070.
16. Berg OG, Kurland CG. Evolution of microbial genomes: sequence acquisition and loss. Mol Biol Evol 2002, 19(12):2265-2276. 10.1093/oxfordjournals.molbev.a004050, 12446817.
17. Novozhilov AS, Karev GP, Koonin EV. Mathematical modeling of evolution of horizontally transferred genes. Mol Biol Evol 2005, 22(8):1721-1732. 10.1093/molbev/msi167, 15901840.
18. Baumdicker F, Hess W, Pfaffelhuber P. The diversity of a distributed genome in bacterial popoulations. Ann Appl Probab 2010, 20(5):1567-1606.
19. Kislyuk AO, Haegeman B, Bergman NH, Weitz JS. Genomic fluidity: an integrative view of gene diversity within microbial populations. BMC Genomics 2011, 12:32. 10.1186/1471-2164-12-32, 3030549, 21232151.
20. Ewens W. Mathematical Population Genetics 2005, New York: Springer, 2.
21. Wakeley J. Coalescent Theory: An Introduction 2009, Greenwood Village: Roberts and Company.
22. Gogarten JP, Townsend JP. Horizontal gene transfer, genome innovation and evolution. Nat Rev Microbiol 2005, 3(9):679-687. 10.1038/nrmicro1204, 16138096.
23. Kislyuk AO, Katz LS, Agrawal S, Hagen MS, Conley AB, Jayaraman P, Nelakuditi V, Humphrey JC, Sammons SA, Govil D, Mair RD, Tatti KM, Tondella ML, Harcourt BH, Mayer LW, Jordan IK. A computational genomics pipeline for prokaryotic sequencing projects. Bioinformatics 2010, 26(15):1819-1826. 10.1093/bioinformatics/btq284, 2905547, 20519285.
24. Fraser C, Hanage W, Spratt B. Recombination and the nature of bacterial speciation. Science 2007, 315(5811):476-480. 10.1126/science.1127573, 2220085, 17255503.
25. Fraser C, Alm EJ, Polz MF, Spratt BG, Hanage WP. The bacterial species challenge: making sense of genetic and ecological diversity. Science 2009, 323(5915):741-746. 10.1126/science.1159388, 19197054.
26. Dorer MS, Fero J, Salama NR. DNA damage triggers genetic exchange in Helicobacter pylori. PLoS Pathogens 2010, 6(7):e1001026. 10.1371/journal.ppat.1001026, 2912397, 20686662.
27. Duffin P, Seifer H. DNA uptake sequence-mediated enhancement of transformation in Neisseria gonorroeae is strain dependent. J Bacteriol 2010, 192(17):4436-4444. 10.1128/JB.00442-10, 2937394, 20601472.
28. Gutenkunst RN, Waterfall JJ, Casey FP, Brown KS, Myers CR, Sethna JP. Universally sloppy parameter sensitivities in systems biology models. PLoS Comput Biol 2007, 3(10):e189.
29. Ochman H, Lawrence JG, Groisman EA. Lateral gene transfer and the nature of bacterial innovation. Nature 2000, 405(6784):299-304. 10.1038/35012500, 10830951.
30. Koonin EV, Makarova KS, Aravind L. Horizontal gene transfer in prokaryotes: quantification and classification. Annu Rev Microbiol 2001, 55(1):709-742. 10.1146/annurev.micro.55.1.709, 11544372.
31. Gogarten JP, Doolittle WF, Lawrence JG. Prokaryotic evolution in light of gene transfer. Mol Biol Evol 2002, 19(12):2226-2238. 10.1093/oxfordjournals.molbev.a004046, 12446813.
32. Huynen MA, van Nimwegen E. The frequency distribution of gene family sizes in complete genomes. Mol Biol Evol 1998, 15(5):583-589. 10.1093/oxfordjournals.molbev.a025959, 9580988.
33. Qian J, Luscombe NM, Gerstein M. Protein family and fold occurrence in genomes: power-law behaviour and evolutionary model. J Mol Biol 2001, 313(4):673-681. 10.1006/jmbi.2001.5079, 11697896.
34. Cosentino Lagomarsino M, Sellerio A, Heijning P, Bassetti B. Universal features in the genome-level evolution of protein domains. Genome Biol 2009, 10(1):R12. 10.1186/gb-2009-10-1-r12, 2687789, 19183449.
35. Vetsigian K, Goldenfeld N. Global divergence of microbial genome sequences mediated by propagating fronts. Proc Natl Acad Sci USA 2005, 102(120):7332-7337. 1129147, 15878987.
36. Maynard Smith J, Smith NH, O'Rourke M, Spratt BG. How clonal are bacteria?. Proc Natl Acad Sci USA 1993, 90(10):4384-4388. 10.1073/pnas.90.10.4384, 46515, 8506277.
37. Fraser C, Hanage WP, Spratt BG. Neutral microepidemic evolution of bacterial pathogens. Proc Natl Acad Sci USA 2005, 102(6):1968-1973. 10.1073/pnas.0406993102, 548543, 15684071.
38. Baumdicker F, Pfaffelhuber P. Evolution of bacterial genomes under horizontal gene transfer. Proceedings of the 58th World Statistics Congress (ISI2011) 2011,
39. Koonin EV, Wolf YI, Karev GP. The structure of the protein universe and genome evolution. Nature 2002, 420(6912):218-223. 10.1038/nature01256, 12432406.
40. Maslov S, Krishna S, Pang TY, Sneppen K. Toolbox model of evolution of prokaryotic metabolic networks and their regulation. Proc Nat Acad Sci USA 2009, 106(24):9743-9748. 10.1073/pnas.0903206106, 2701025, 19482938.
41. Shendure J, Ji HL. Next-generation DNA sequencing. Nature Biotechnology 2008, 26(10):1135-1145. 10.1038/nbt1486, 18846087.
42. Konstantinidis KT, Tiedje JM. Genomic insights that advance the species definition for prokaryotes. Proc Natl Acad Sci USA 2005, 102(7):2567-2572. 10.1073/pnas.0409727102, 549018, 15701695.
43. Beiko RG, Doolittle WF, Charlebois RL. The impact of reticulate evolution on genome phylogeny. Syst Biol 2008, 57(6):844-856. 10.1080/10635150802559265, 19085328.
44. Kimura M. The Neutral Theory of Molecular Evolution 1983, Cambridge: Cambridge University Press.
45. Nei M, Suzuki Y, Nozawa M. The neutral theory of molecular evolution in the genomic era. Annu Rev Genomics Hum Genet 2010, 11:265-289. 10.1146/annurev-genom-082908-150129, 20565254.
46. Harpole WS, Tilman D. Non-neutral patterns of species abundance in grassland communities. Ecol Lett 2006, 9(1):15-23.
47. Kraft NJB, Valencia R, Ackerly DD. Functional traits and niche-based tree community assembly in an amazonian forest. Science 2008, 322(5901):580-582. 10.1126/science.1160662, 18948539.
48. Koonin EV. Are there laws of genome evolution?. PLoS Comput Biol 2011, 7(8):e1002173. 10.1371/journal.pcbi.1002173, 3161903, 21901087.