A null model for microbial diversification

Proceedings of the National Academy of Sciences of the United States of America

Volumn 114, Issue 27, 2017, Pages E5414-E5423

  Straub, Timothy J ^a,c   Zhaxybayeva, Olga ^a,b  

^a Lamont Doherty Earth Observatory   (United States)

^b Dartmouth College   (United States)

^c BROAD INSTITUTE OF MIT AND HARVARD   (United States)

Author keywords

Bacterial species; Genetic drift; Neutral evolution; Pathogen typing; Prokaryotic diversity

Indexed keywords

RNA 16S;

ARTICLE; BACTERIAL GENE; BACTERIAL GENOME; BORRELIA; DNA SEQUENCE; ESCHERICHIA; EVOLUTION; GENE SEQUENCE; GENEALOGY; GENETIC DRIFT; HELICOBACTER PYLORI; MICROBIAL DIVERSITY; MULTIGENE FAMILY; MULTILOCUS SEQUENCE TYPING; NEISSERIA; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENETIC TREE; POPULATION GENETICS; PRIORITY JOURNAL; PROKARYOTE; SPECIES DIFFERENTIATION; ANIMAL; BACTERIUM IDENTIFICATION; BIODIVERSITY; BIOLOGICAL MODEL; CLUSTER ANALYSIS; COMPUTER SIMULATION; GENETIC VARIATION; GENETICS; MOLECULAR EVOLUTION; PHYLOGENY; SPECIES DIFFERENCE;

ANIMALS; BACTERIAL TYPING TECHNIQUES; BIODIVERSITY; BORRELIA; CLUSTER ANALYSIS; COMPUTER SIMULATION; ESCHERICHIA; EVOLUTION, MOLECULAR; GENES, BACTERIAL; GENETIC DRIFT; GENETIC SPECIATION; GENETIC VARIATION; HELICOBACTER PYLORI; MODELS, GENETIC; NEISSERIA; PHYLOGENY; RNA, RIBOSOMAL, 16S; SPECIES SPECIFICITY;

EID: 85021707206     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1619993114     Document Type: Article

References (110)

1. Locey KJ, Lennon JT (2016) Scaling laws predict global microbial diversity. Proc Natl Acad Sci USA 113:5970-5975.
2. Hanage WP, Fraser C, Spratt BG (2006) Sequences, sequence clusters and bacterial species. Philos Trans R Soc Lond B Biol Sci 361:1917-1927.
3. Hunt DE, et al. (2008) Resource partitioning and sympatric differentiation among closely related bacterioplankton. Science 320:1081-1085.
4. Caro-Quintero A, Konstantinidis KT (2012) Bacterial species may exist, metagenomics reveal. Environ Microbiol 14:347-355.
5. Acinas SG, et al. (2004) Fine-scale phylogenetic architecture of a complex bacterial community. Nature 430:551-554.
6. Cohan FM, Perry EB (2007) A systematics for discovering the fundamental units of bacterial diversity. Curr Biol 17:R373-R386.
7. Cohan FM (2016) Bacterial speciation: Genetic sweeps in bacterial species. Curr Biol 26:R112-R115.
8. Hanage WP, Spratt BG, Turner KM, Fraser C (2006) Modelling bacterial speciation. Philos Trans R Soc Lond B Biol Sci 361:2039-2044.
9. Feil EJ (2004) Small change: Keeping pace with microevolution. Nat Rev Microbiol 2: 483-495.
10. Shapiro BJ, et al. (2012) Population genomics of early events in the ecological differentiation of bacteria. Science 336:48-51.
11. Shapiro BJ, Polz MF (2014) Ordering microbial diversity into ecologically and genetically cohesive units. Trends Microbiol 22:235-247.
12. Bendall ML, et al. (2016) Genome-wide selective sweeps and gene-specific sweeps in natural bacterial populations. ISME J 10:1589-1601.
13. Mende DR, Sunagawa S, Zeller G, Bork P (2013) Accurate and universal delineation of prokaryotic species. Nat Methods 10:881-884.
14. Thompson CC, et al. (2015) Microbial taxonomy in the post-genomic era: Rebuilding from scratch? Arch Microbiol 197:359-370
15. Whitman W, ed (2015) Bergey's Manual of Systematics of Archaea and Bacteria (Bergey's Manual Trust, Athens, GA).
16. Huse SM, et al. (2014) VAMPS: A website for visualization and analysis of microbial population structures. BMC Bioinformatics 15:41.
17. Wakeley J (2009) Coalescent Theory: An Introduction (Roberts and Company, Greenwood Village, CO).
18. Kingman JFC (1982) The coalescent. Stochastic Process Appl 13:235-248.
19. Felsenstein J (1981) Evolutionary trees from DNA sequences: A maximum likelihood approach. J Mol Evol 17:368-376.
20. Welch RA (2006) The genus Escherichia. Proteobacteria: Gamma Subclass, The Prokaryotes, eds Dworkin M, Falkow S, Rosenberg E, Schleifer K-H, Stackebrandt E (Springer, New York), Vol 6, pp 60-71.
21. Luo C, et al. (2011) Genome sequencing of environmental Escherichia coli expands understanding of the ecology and speciation of the model bacterial species. Proc Natl Acad Sci USA 108:7200-7205.
22. Walk ST (2015) The "cryptic" Escherichia. EcoSal Plus 6:10.1128/ecosalplus.ESP- 0002-2015.
23. Octavia S, Lan R (2014) The family Enterobacteriaceae. The Prokaryotes: Gammaproteobacteria, eds Rosenberg E, DeLong EF, Lory S, Stackebrandt E, Thompson F (Springer, Berlin), pp 225-286.
24. Liu S, et al. (2015) Escherichia marmotae sp. nov., isolated from faeces of Marmota himalayana. Int J Syst Evol Microbiol 65:2130-2134.
25. Bennett JS, Bratcher HB, Brehony C, Harrison OB, Maiden MCJ (2014) The genus Neisseria. The Prokaryotes: Alphaproteobacteria and Betaproteobacteria, eds Rosenberg E, DeLong EF, Lory S, Stackebrandt E, Thompson F (Springer, Berlin), pp 881-900.
26. Maiden MCJ, Harrison OB (2016) Population and functional genomics of Neisseria revealed with gene-by-gene approaches. J Clin Microbiol 54:1949-1955.
27. Bennett JS, et al. (2012) A genomic approach to bacterial taxonomy: An examination and proposed reclassification of species within the genus Neisseria. Microbiology 158:1570-1580.
28. Bratcher HB, Bennett JS, Maiden MCJ (2012) Evolutionary and genomic insights into meningococcal biology. Future Microbiol 7:873-885.
29. Rotman E, Seifert HS (2014) The genetics of Neisseria species. Annu Rev Genet 48: 405-431.
30. Caimano M (2006) The genus Borrelia. Proteobacteria: Delta, Epsilon subclass, The Prokaryotes, eds Dworkin M, Falkow S, Rosenberg E, Schleifer K-H, Stackebrandt E (Springer, New York), Vol 7, pp 235-293.
31. Karami A, Sarshar M, Ranjbar R, Zanjani RS (2014) The phylum Spirochaetaceae. The Prokaryotes: Other Major Lineages of Bacteria and The Archaea, eds Rosenberg E, DeLong EF, Lory S, Stackebrandt E, Thompson F (Springer, Berlin), pp 915-929.
32. Wang G, Schwartz I (2015) Borrelia. Bergey's Manual of Systematics of Archaea and Bacteria (John Wiley, New York).
33. Margos G, et al. (2009) A new Borrelia species defined by multilocus sequence analysis of housekeeping genes. Appl Environ Microbiol 75:5410-5416.
34. Mitchell HM, Rocha GA, Kaakoush NO, O'Rourke JL, Queiroz DMM (2014) The family Helicobacteraceae. The Prokaryotes: Deltaproteobacteria and Epsilonproteobacteria, eds Rosenberg E, DeLong EF, Lory S, Stackebrandt E, Thompson F (Springer, Berlin), pp 337-392.
35. Moodley Y, et al. (2012) Age of the association between Helicobacter pylori and man. PLoS Pathog 8:e1002693.
36. Alm RA, et al. (1999) Genomic-sequence comparison of two unrelated isolates of the human gastric pathogen Helicobacter pylori. Nature 397:176-180.
37. Morelli G, et al. (2010) Microevolution of Helicobacter pylori during prolonged infection of single hosts and within families. PLoS Genet 6:e1001036.
38. Dorer MS, Sessler TH, Salama NR (2011) Recombination and DNA repair in Helicobacter pylori. Annu Rev Microbiol 65:329-348.
39. Jolley KA, Maiden MC (2010) BIGSdb: Scalable analysis of bacterial genome variation at the population level. BMC Bioinformatics 11:595.
40. Wirth T, et al. (2006) Sex and virulence in Escherichia coli: An evolutionary perspective. Mol Microbiol 60:1136-1151.
41. Medini D, et al. (2008) Microbiology in the post-genomic era. Nat Rev Microbiol 6: 419-430.
42. Cordero OX, Polz MF (2014) Explaining microbial genomic diversity in light of evolutionary ecology. Nat Rev Microbiol 12:263-273.
43. Kashtan N, et al. (2014) Single-cell genomics reveals hundreds of coexisting subpopulations in wild Prochlorococcus. Science 344:416-420.
44. Schloss PD, et al. (2009) Introducing mothur: Open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537-7541.
45. Goris J, et al. (2007) DNA-DNA hybridization values and their relationship to wholegenome sequence similarities. Int J Syst Evol Microbiol 57:81-91.
46. Stackebrandt E, Ebers J (2006) Taxonomic parameters revisited: Tarnished gold standards. Microbiol Today 33:152-155.
47. Massey FJ (1951) The Kolmogorov-Smirnov test for goodness of fit. J Am Stat Assoc 46:68-78.
48. Maiden MCJ, et al. (2013) MLST revisited: The gene-by-gene approach to bacterial genomics. Nat Rev Microbiol 11:728-736.
49. Achtman M, Wagner M (2008) Microbial diversity and the genetic nature of microbial species. Nat Rev Microbiol 6:431-440.
50. Morlon H, Potts MD, Plotkin JB (2010) Inferring the dynamics of diversification: A coalescent approach. PLoS Biol 8:e1000493.
51. McPeek MA (2008) The ecological dynamics of clade diversification and community assembly. Am Nat 172:E270-E284.
52. Ferretti L, Disanto F, Wiehe T (2013) The effect of single recombination events on coalescent tree height and shape. PLoS One 8:e60123.
53. Suerbaum S, Josenhans C (2007) Helicobacter pylori evolution and phenotypic diversification in a changing host. Nat Rev Microbiol 5:441-452.
54. Kennemann L, et al. (2011) Helicobacter pylori genome evolution during human infection. Proc Natl Acad Sci USA 108:5033-5038.
55. Vos M, Didelot X (2009) A comparison of homologous recombination rates in bacteria and archaea. ISME J 3:199-208.
56. Huse SM, Welch DM, Morrison HG, Sogin ML (2010) Ironing out the wrinkles in the rare biosphere through improved OTU clustering. Environ Microbiol 12:1889-1898.
57. Revell LJ, Harmon LJ, Glor RE (2005) Underparameterized model of sequence evolution leads to bias in the estimation of diversification rates from molecular phylogenies. Syst Biol 54:973-983.
58. Jordan IK, Rogozin IB, Wolf YI, Koonin EV (2002) Essential genes are more evolutionarily conserved than are nonessential genes in bacteria. Genome Res 12:962-968.
59. Wang L, Rothemund D, Curd H, Reeves PR (2003) Species-wide variation in the Escherichia coli flagellin (H-antigen) gene. J Bacteriol 185:2936-2943.
60. Wicker E, et al. (2012) Contrasting recombination patterns and demographic histories of the plant pathogen Ralstonia solanacearum inferred from MLSA. ISME J 6: 961-974.
61. Monteil CL, et al. (2013) Nonagricultural reservoirs contribute to emergence and evolution of Pseudomonas syringae crop pathogens. New Phytol 199:800-811.
62. Smith KD, et al. (2003) Toll-like receptor 5 recognizes a conserved site on flagellin required for protofilament formation and bacterial motility. Nat Immunol 4: 1247-1253.
63. Vinatzer BA, Monteil CL, Clarke CR (2014) Harnessing population genomics to understand how bacterial pathogens emerge, adapt to crop hosts, and disseminate. Annu Rev Phytopathol 52:19-43.
64. Rao DN, Dryden DTF, Bheemanaik S (2014) Type III restriction-modification enzymes: A historical perspective. Nucleic Acids Res 42:45-55.
65. de Vries N, et al. (2002) Transcriptional phase variation of a type III restrictionmodification system in Helicobacter pylori. J Bacteriol 184:6615-6623.
66. Kojima KK, et al. (2016) Population evolution of Helicobacter pylori through diversification in DNA methylation and interstrain sequence homogenization. Mol Biol Evol 33:2848-2859.
67. Tomb J-F, et al. (1997) The complete genome sequence of the gastric pathogen Helicobacter pylori. Nature 388:539-547.
68. Oleastro M, Ménard A (2013) The role of Helicobacter pylori outer membrane proteins in adherence and pathogenesis. Biology (Basel) 2:1110-1134.
69. Hobbs M, Collie ESR, Free PD, Livingston SP, Mattick JS (1993) PilS and PilR, a twocomponent transcriptional regulatory system controlling expression of type 4 fimbriae in Pseudomonas aeruginosa. Mol Microbiol 7:669-682.
70. Eriksson J, et al. (2015) Characterization of motility and piliation in pathogenic Neisseria. BMC Microbiol 15:92.
71. Carrick CS, Fyfe JAM, Davies JK (2000) The genome of Neisseria gonorrhoeae retains the remnants of a two-component regulatory system that once controlled piliation. FEMS Microbiol Lett 186:197-201.
72. Denamur E, et al. (2000) Evolutionary implications of the frequent horizontal transfer of mismatch repair genes. Cell 103:711-721.
73. Lin Z, Nei M, Ma H (2007) The origins and early evolution of DNA mismatch repair genes-Multiple horizontal gene transfers and co-evolution. Nucleic Acids Res 35: 7591-7603.
74. Heymans R, Golparian D, Bruisten SM, Schouls LM, Unemo M (2012) Evaluation of Neisseria gonorrhoeae multiple-locus variable-number tandem-repeat analysis, N. gonorrhoeae Multiantigen sequence typing, and full-length porB gene sequence analysis for molecular epidemiological typing. J Clin Microbiol 50:180-183.
75. Trees DL, Schultz AJ, Knapp JS (2000) Use of the neisserial lipoprotein (Lip) for subtyping Neisseria gonorrhoeae. J Clin Microbiol 38:2914-2916.
76. Beutin L, Delannoy S, Fach P (2015) Genetic diversity of the fliC genes encoding the flagellar antigen H19 of Escherichia coli and application to the specific identification of enterohemorrhagic E. coli O121:H19. Appl Environ Microbiol 81:4224-4230.
77. Beutin L, Strauch E (2007) Identification of sequence diversity in the Escherichia coli fliC genes encoding flagellar types H8 and H40 and its use in typing of Shiga toxinproducing E. coli O8, O22, O111, O174, and O179 strains. J Clin Microbiol 45:333-339.
78. Iguchi A, et al. (2015) A complete view of the genetic diversity of the Escherichia coli O-antigen biosynthesis gene cluster. DNA Res 22:101-107.
79. Cheng K, et al. (2016) Phenotypic H-antigen typing by mass spectrometry combined with genetic typing of H antigens, O antigens, and toxins by whole-genome sequencing enhances identification of Escherichia coli isolates. J Clin Microbiol 54: 2162-2168.
80. Barraclough TG, Balbi KJ, Ellis RJ (2012) Evolving concepts of bacterial species. Evol Biol 39:148-157.
81. Doolittle WF (2012) Population genomics: How bacterial species form and why they don't exist. Curr Biol 22:R451-R453.
82. Wattam AR, et al. (2014) PATRIC, the bacterial bioinformatics database and analysis resource. Nucleic Acids Res 42:D581-D591.
83. Mahmood K, Webb GI, Song J, Whisstock JC, Konagurthu AS (2012) Efficient largescale protein sequence comparison and gene matching to identify orthologs and coorthologs. Nucleic Acids Res 40:e44.
84. Dice LR (1945) Measures of the amount of ecologic association between species. Ecology 26:297-302.
85. Sørensen TJ (1948) A method of establishing groups of equal amplitude in plant sociology based on similarity of species content and its application to analyses of the vegetation on Danish commons. Biol Skr 5:1-34.
86. Van Dongen S (2000) Graph clustering by flow simulation. Ph.D dissertation (Univ Utrecht, Utrecht, The Netherlands).
87. Enright AJ, Van Dongen S, Ouzounis CA (2002) An efficient algorithm for large-scale detection of protein families. Nucleic Acids Res 30:1575-1584.
88. Hey J (1992) Using phylogenetic trees to study speciation and extinction. Evolution 46:627-640.
89. Moran PAP (1958) A general theory of the distribution of gene frequencies. I. Overlapping generations. Proc R Soc Lond B Biol Sci 149:102-112.
90. Saitou N, Nei M (1987) The neighbor-joining method: A new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406-425.
91. Cock PJA, et al. (2009) Biopython: Freely available Python tools for computational molecular biology and bioinformatics. Bioinformatics 25:1422-1423.
92. Rambaut A, Grassly NC (1997) Seq-Gen: An application for the Monte Carlo simulation of DNA sequence evolution along phylogenetic trees. Comput Appl Biosci 13: 235-238.
93. Acinas SG, Marcelino LA, Klepac-Ceraj V, Polz MF (2004) Divergence and redundancy of 16S rRNA sequences in genomes with multiple rrn operons. J Bacteriol 186: 2629-2635.
94. Pei AY, et al. (2010) Diversity of 16S rRNA genes within individual prokaryotic genomes. Appl Environ Microbiol 76:3886-3897.
95. Edgar RC (2004) MUSCLE: Multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792-1797.
96. Pruesse E, Peplies J, Glöckner FO (2012) SINA: Accurate high-throughput multiple sequence alignment of ribosomal RNA genes. Bioinformatics 28:1823-1829.
97. Wollenberg K, Arnold J, Avise JC (1996) Recognizing the forest for the trees: Testing temporal patterns of cladogenesis using a null model of stochastic diversification. Mol Biol Evol 13:833-849.
98. Bewick V, Cheek L, Ball J (2004) Statistics review 9: One-way analysis of variance. Crit Care 8:130-136.
99. Altschul SF, et al. (1997) Gapped BLAST and PSI-BLAST: A new generation of protein database search programs. Nucleic Acids Res 25:3389-3402.
100. Galperin MY, Makarova KS, Wolf YI, Koonin EV (2015) Expanded microbial genome coverage and improved protein family annotation in the COG database. Nucleic Acids Res 43:D261-D269.
101. Fisher RA (1922) On the interpretation of χ2 from contingency tables, and the calculation of P. JR Stat Soc 85:87-94.
102. Abascal F, Zardoya R, Telford MJ (2010) TranslatorX: Multiple alignment of nucleotide sequences guided by amino acid translations. Nucleic Acids Res 38:W7-13.
103. Stamatakis A (2014) RAxML version 8: A tool for phylogenetic analysis and postanalysis of large phylogenies. Bioinformatics 30:1312-1313.
104. Yang Z, Wong WSW, Nielsen R (2005) Bayes empirical bayes inference of amino acid sites under positive selection. Mol Biol Evol 22:1107-1118.
105. Yang Z (2007) PAML 4: Phylogenetic analysis by maximum likelihood. Mol Biol Evol 24:1586-1591.
106. Harvey PH, May RM, Nee S (1994) Phylogenies without fossils. Evolution 48:523-529.
107. Martin AP, Costello EK, Meyer AF, Nemergut DR, Schmidt SK (2004) The rate and pattern of cladogenesis in microbes. Evolution 58:946-955.
108. Pybus OG, Harvey PH (2000) Testing macro-evolutionary models using incomplete molecular phylogenies. Proc Biol Sci 267:2267-2272.
109. Byers DM, Gong H (2007) Acyl carrier protein: Structure-function relationships in a conserved multifunctional protein family. Biochem Cell Biol 85:649-662.
110. Barnwal RP, Van Voorhis WC, Varani G (2011) NMR structure of an acyl-carrier protein from Borrelia burgdorferi. Acta Crystallogr Sect F Struct Biol Cryst Commun 67: 1137-1140.