Quantitative and Theoretical Microbial Population Biology

  • Martin F. Polz
  • William P. Hanage


Microbes are extraordinarily diverse, not only in terms of their genetics and metabolism, but even in the fundamental evolutionary processes that give rise to their diversity. Because the biological species concept, largely developed for vertebrate animals, does not apply to bacteria and archaea, it has been challenging to conceptualize what a microbial population should be. However, recent evidence suggests that akin to populations of animals and plants, genotypic clusters can be recognized among co-existing microbes. These represent tractable units to address fundamental ecological and evolutionary questions with first results suggesting cohesive ecological properties in spite of high genetic diversity within clusters. Progress in genomic sequencing and computational tools are leading toward an integrated understanding of how mutation, recombination and gene transfer combine with selection to create microbial diversity, and how populations adapt to novel environmental challenges.


Internal Transcribe Spacer Homologous Recombination Acid Mine Drainage Geographic Isolation Approximate Bayesian Computation 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



We thank Nick Croucher for valuable discussions and suggestions. Funding was provided by the National Science Foundation, the National Institutes of Health and the Gordon and Betty Moore Foundation.


  1. Acinas SG, Klepac-Ceraj V, Hunt DE, Pharino C, Ceraj I, Distel DL, Polz MF (2004) Fine-scale phylogenetic architecture of a complex bacterial community. Nature 430:551–554PubMedCrossRefGoogle Scholar
  2. Allen EE, Tyson GW, Whitaker RJ, Detter JC, Richardson PM, Banfield JF (2007) Genome dynamics in a natural archaeal population. Proc Natl Acad Sci USA 104:1883–1888PubMedCrossRefGoogle Scholar
  3. Anderson MT, Seifert HS (2011) Opportunity and means: horizontal gene transfer from the human host to a bacterial pathogen. mBio 2:e00005–e00011PubMedCrossRefGoogle Scholar
  4. Andersson AF, Banfield JF (2008) Virus population dynamics and acquired resistance in natural microbial communities. Science 320:1047–1050PubMedCrossRefGoogle Scholar
  5. Azam F, Long RA (2001) Oceanography – sea snow microcosms. Nature 414:495PubMedCrossRefGoogle Scholar
  6. Bart A, Barnabe C, Achtman M, Dankert J, van der Ende A, Tibayrenc M (2001) The population structure of Neisseria meningitidis serogroup A fits the predictions for clonality. Infect Genet Evol 1:117–122PubMedCrossRefGoogle Scholar
  7. Becraft ED, Cohan FM, Kühl M, Jensen SI, Ward DM (2011) Fine-scale distribution patterns of Synechococcus ecological diversity in microbial mats of Mushroom Springs, Yellowstone. Appl Environ Microbiol 77:7689–7697PubMedCrossRefGoogle Scholar
  8. Bentley SD, Aanensen DM, Mavroidi A, Saunders D, Rabbinowitsch E, Collins M, Donohoe K, Harris D, Murphy L, Quail MA, Samuel G, Skovsted IC, Kaltoft MS, Barrell B, Reeves PR, Parkhill J, Spratt BG (2006) Genetic analysis of the capsular biosynthetic locus from all 90 pneumococcal serotypes. PLoS Genet 2:e31PubMedCrossRefGoogle Scholar
  9. Boucher Y, Cordero OX, Takemura A, Hunt DE, Schliep K, Bapteste E, Lopez P, Tarr CL, Polz MF (2011) Local mobile gene pools rapidly cross species boundaries to create endemicity within global Vibrio cholerae populations. mBio 2:e00335–00310PubMedCrossRefGoogle Scholar
  10. Bouman HA, Ulloa O, Scanlan DJ, Zwirglmaier K, Li WKW, Platt T, Stuart V, Barlow R, Leth O, Clementson L, Lutz V, Fukasawa M, Watanabe S, Sathyendranath S (2006) Oceanographic basis of the global surface distribution of Prochlorococcus ecotypes. Science 312:918–921PubMedCrossRefGoogle Scholar
  11. Cadillo-Quiroz H, Didelot X, Heid NL, Herrara A, Darling A, Reno ML, Krause DJ, Whitaker RJ (2012) Patterns of gene flow define species of thermophilic archaea. PLoS Biol 10:e1001265PubMedCrossRefGoogle Scholar
  12. Cambray G, Guerout AM, Mazel D (2010) Integrons. Annu Rev Genet 44:141–166PubMedCrossRefGoogle Scholar
  13. Canchaya C, Fournous G, Chibani-Chennoufi S, Dillmann ML, Brussow H (2003) Phage as agents of lateral gene transfer. Curr Opin Microbiol 6:417–424PubMedCrossRefGoogle Scholar
  14. Caro-Quintero A, Rodriguez-Castano GP, Konstantinidis KT (2009) Genomic insights into the convergence and pathogenicity factors of Campylobacter jejuni and Campylobacter coli species. J Bacteriol 191:5824–5831PubMedCrossRefGoogle Scholar
  15. Cheng L, Connor TR, Aanensen DM, Spratt BG, Corander J (2011) Bayesian semi-supervised classification of bacterial samples using MLST databases. BMC Bioinformatics 12:302PubMedCrossRefGoogle Scholar
  16. Cohan FM (1994) The effects of rare but promiscuous genetic exchange on evolutionary divergence in prokaryotes. Am Nat 143:965–986CrossRefGoogle Scholar
  17. Cohan FM (2002) What are bacterial species. Annu Rev Microbiol 56:457–487PubMedCrossRefGoogle Scholar
  18. Coleman ML, Chisholm SW (2010) Ecosystem-specific selection pressures revealed through comparative population genomics. Proc Natl Acad Sci USA 107:18634–18639PubMedCrossRefGoogle Scholar
  19. Connor N, Sikorski J, Rooney AP, Kopac S, Koeppel AF, Burger A, Cole SG, Perry EB, Krizanc D, Field NC, Slaton M, Cohan FM (2010) Ecology of speciation in the genus Bacillus. Appl Environ Microbiol 76:1349–1358PubMedCrossRefGoogle Scholar
  20. Corander J, Marttinen P, Siren J, Tang J (2008) Enhanced Bayesian modelling in BAPS software for learning genetic structures of populations. BMC Bioinformatics 9:539PubMedCrossRefGoogle Scholar
  21. Corander J, Tang J (2007) Bayesian analysis of population structure based on linked molecular information. Math Biosci 205:19–31PubMedCrossRefGoogle Scholar
  22. Corander J, Waldmann P, Sillanpaa MJ (2003) Bayesian analysis of genetic differentiation between populations. Genetics 163:367–374PubMedGoogle Scholar
  23. Croucher NJ, Harris SR, Fraser C, Quail MA, Burton J, van der Linden M, McGee L, von Gottberg A, Song JH, Ko KS, Pichon B, Baker S, Parry CM, Lambertsen LM, Shahinas D, Pillai DR, Mitchell TJ, Dougan G, Tomasz A, Klugman KP, Parkhill J, Hanage WP, Bentley SD (2011) Rapid pneumococcal evolution in response to clinical interventions. Science 331:430–434PubMedCrossRefGoogle Scholar
  24. Denamur E, Lecointre G, Darlu P, Tenaillon O, Acquaviva C, Sayada C, Sunjevaric I, Rothstein R, Elion J, Taddei F, Radman M, Matic I (2000) Evolutionary implications of the frequent horizontal transfer of mismatch repair genes. Cell 103:711–721PubMedCrossRefGoogle Scholar
  25. Denef VJ, Kalnejais LH, Mueller RS, Wilmes P, Baker BJ, Thomas BC, VerBerkmoes NC, Hettich RL, Banfield JF (2010a) Proteogenomic basis for ecological divergence of closely related bacteria in natural acidophilic microbial communities. Proc Natl Acad Sci USA 107:2383–2390PubMedCrossRefGoogle Scholar
  26. Denef VJ, Mueller RS, Banfield JF (2010b) AMD biofilms: using model communities to study microbial evolution and ecological complexity in nature. ISME J 4:599–610PubMedCrossRefGoogle Scholar
  27. Didelot X, Falush D (2007) Inference of bacterial microevolution using multilocus sequence data. Genetics 175:1251–1266PubMedCrossRefGoogle Scholar
  28. Didelot X, Lawson D, Darling A, Falush D (2010) Inference of homologous recombination in bacteria using whole-genome sequences. Genetics 186:1435–1449PubMedCrossRefGoogle Scholar
  29. Doolittle WF, Papke RT (2006) Genomics and the bacterial species problem. Genome Biol 7:116PubMedCrossRefGoogle Scholar
  30. Dunning Hotopp JC, Clark ME, Oliveira DC, Foster JM, Fischer P, Munoz Torres MC, Giebel JD, Kumar N, Ishmael N, Wang S, Ingram J, Nene RV, Shepard J, Tomkins J, Richards S, Spiro DJ, Ghedin E, Slatko BE, Tettelin H, Werren JH (2007) Widespread lateral gene transfer from intracellular bacteria to multicellular eukaryotes. Science 317:1753–1756PubMedCrossRefGoogle Scholar
  31. Eppley JM, Tyson GW, Getz WM, Banfield JF (2007) Genetic exchanges across a species boundary in the archaeal genus Ferroplasma. Genetics 177:407–416PubMedCrossRefGoogle Scholar
  32. Falush D, Wirth T, Linz B, Pritchard JK, Sephens M, Kidd M, Blaser MJ, Graham DY, Vacher S, Perez-Perez GI, Yamaoka Y, Mégraud F, Otto K, Reichard U, Katzowitsch E, Wang X, Achtman M, Suerbaum S (2003) Traces of human migrations in Helicobacter pylori populations. Science 299:1582–1585PubMedCrossRefGoogle Scholar
  33. Falush D, Stephens M, Pritchard JK (2007) Inference of population structure using multilocus genotype data: dominant markers and null alleles. Mol Ecol Notes. doi:10.1111/j.1471-8286.2007.01758.xGoogle Scholar
  34. Feil EJ, Enright MC, Spratt BG (2000) Estimating the relative contributions of mutation and recombination to clonal diversification: a comparison between Neisseria meningitidis and Streptococcus pneumoniae. Res Microbiol 151:465–469PubMedCrossRefGoogle Scholar
  35. Feil EJ, Holmes EC, Bessen DE, Chan MS, Day NP, Enright MC, Goldstein R, Hood DW, Kalia A, Moore CE, Zhou J, Spratt BG (2001) Recombination within natural populations of pathogenic bacteria: short-term empirical estimates and long-term phylogenetic consequences. Proc Natl Acad Sci USA 98:182–187PubMedCrossRefGoogle Scholar
  36. Feil EJ, Cooper JE, Grundmann H, Robinson DA, Enright MC, Berendt T, Peacock SJ, Smith JM, Murphy M, Spratt BG, Moore CE, Day NP (2003) How clonal is Staphylococcus aureus? J Bacteriol 185:3307–3316PubMedCrossRefGoogle Scholar
  37. Ferris MJ, Kühl M, Wieland A, Ward DM (2003) Cyanobacterial ecotypes in different optical microenvironments of a 68 degrees hot spring mat community revealed by 16 S-23 S rRNA internal transcribed spacer region variation. Appl Environ Microbiol 69:2893–2898PubMedCrossRefGoogle Scholar
  38. Fraser C, Hanage WP, Spratt BG (2005) Neutral microepidemic evolution of bacterial pathogens. Proc Natl Acad Sci USA 102:1968–1973PubMedCrossRefGoogle Scholar
  39. Fraser C, Hanage WP, Spratt BG (2007) Recombination and the nature of bacterial speciation. Science 315:476–480PubMedCrossRefGoogle Scholar
  40. Fraser C, Alm EJ, Polz MF, Spratt BG, Hanage WP (2009) The bacterial species challenge: making sense of genetic and ecological diversity. Science 232:741–746CrossRefGoogle Scholar
  41. Gal-Mor O, Finlay BB (2006) Pathogenicity islands: a molecular toolbox for bacterial virulence. Cell Microbiol 8:1707–1719PubMedCrossRefGoogle Scholar
  42. Gevers D, Cohan FM, Lawrence JG, Spratt BG, Coenye T, Feil EJ, Stackebrandt E, Van de Peer Y, Vandamme P, Thompson FL, Swings J (2005) Re-evaluating prokaryotic species. Nat Rev Microbiol 3:733–739PubMedCrossRefGoogle Scholar
  43. Goodfellow M, Manfio GP, Chun J (1997) Towards a practical species concept for cultivable bacteria. In: Claridge MF, Dawah HA, Wilson MR (eds) The units of biodiversity. Chapman and Hall, LondonGoogle Scholar
  44. Grogan DW, Stengel KR (2008) Recombination of synthetic oligonucleotides with prokaryotic chromosomes: substrate requirements of the Escherichia coli 1 Red and Sulfolobus acidocaldarius recombination systems. Mol Microbiol 69:1255–1265PubMedCrossRefGoogle Scholar
  45. Guttman DS, Dykhuizen DE (1994) Detecting selective sweeps in naturally occurring Escherichia coli. Genetics 138:993–1003PubMedGoogle Scholar
  46. Hacker J, Carniel E (2001) Ecological fitness, genomic islands and bacterial pathogenicity – a Darwinian view of the evolution of microbes. EMBO Rep 2:376–381PubMedGoogle Scholar
  47. Hanage WP, Fraser C, Spratt BG (2005) Fuzzy species among recombinogenic bacteria. BMC Biol 3. doi:10.1186/1741-7007-1183-1186Google Scholar
  48. Hanage WP, Fraser C, Spratt BG (2006a) The impact of homologous recombination on the generation of diversity in bacteria. J Theor Biol 239:210–219PubMedCrossRefGoogle Scholar
  49. Hanage WP, Fraser C, Spratt BG (2006b) Sequences, sequence clusters and bacterial species. Philos Trans R Soc Lond B 361:1917–1927CrossRefGoogle Scholar
  50. Hanage WP, Spratt BG, Turner KM, Fraser C (2006c) Modeling bacterial speciation. Philos Trans R Soc Lond B Biol Sci 361:2039–2044PubMedCrossRefGoogle Scholar
  51. Hanage WP, Fraser C, Tang J, Connor TR, Corander J (2009) Hyper-recombination, diversity, and antibiotic resistance in pneumococcus. Science 324:1454–1457PubMedCrossRefGoogle Scholar
  52. Harris SR, Feil EJ, Holden MT, Quail MA, Nickerson EK, Chantratita N, Gardete S, Tavares A, Day N, Lindsay JA, Edgeworth JD, de Lencastre H, Parkhill J, Peacock SJ, Bentley SD (2010) Evolution of MRSA during hospital transmission and intercontinental spread. Science 327:469–474PubMedCrossRefGoogle Scholar
  53. Hubisz MJ, Falush D, Stephens M, Pritchard JK (2009) Inferring weak population structure with the assistance of sample group information. Mol Ecol Resour 9:1322–1332PubMedCrossRefGoogle Scholar
  54. Hunt DE, David LD, Gevers D, Preheim SP, Alm EJ, Polz MF (2008) Resource partitioning and sympatric differentiation among closely related bacterioplankton. Science 320:1081–1085PubMedCrossRefGoogle Scholar
  55. Johnson ZI, Zinser ER, Coe A, McNulty NP, Woodward EMS, Chisholm SW (2006) Niche partitioning among Prochlorococcus ecotypes along ocean-scale environmental gradients. Science 311:1737–1740PubMedCrossRefGoogle Scholar
  56. Juhas M, van der Meer JR, Gaillard M, Harding RM, Hood DW, Crook DW (2009) Genomic islands: tools of bacterial horizontal gene transfer and evolution. FEMS Microbiol Rev 33:376–393PubMedCrossRefGoogle Scholar
  57. Keswani J, Whitman WB (2001) Relationship of 16 S rRNA sequence similarity to DNA hybridization in prokaryotes. Int J Syst Evol Microbiol 51:667–678PubMedGoogle Scholar
  58. Koeppel A, Perry EB, Sikorski J, Krizanc D, Warner A, Ward DM, Rooney AP, Brambilla E, Connor N, Ratcliff RM, Nevo E, Cohan FM (2008) Identifying the fundamental units of bacterial diversity: a paradigm shift to incorporate ecology into bacterial systematics. Proc Natl Acad Sci USA 105:2504–2509PubMedCrossRefGoogle Scholar
  59. Konstantinidis KT, DeLong EF (2008) Genomic patterns of recombination, clonal divergence and environment in marine microbial populations. ISME J 10:1052–1065CrossRefGoogle Scholar
  60. Lawrence JG (2002) Gene transfer in bacteria: speciation without species? Theor Pop Biol 61:449–460CrossRefGoogle Scholar
  61. Lederberg J (1947) Gene Recombination and linked segregations in Escherichia coli. Genetics 32:505–525PubMedGoogle Scholar
  62. Lederberg J (1952) Cell genetics and hereditary symbiosis. Physiol Rev 32:403–430PubMedGoogle Scholar
  63. Lee JY, Song JH, Ko KS (2010) Recombination rates of Streptococcus pneumoniae isolates with both erm(B) and mef(A) genes. FEMS Microbiol Lett 309:163–169PubMedGoogle Scholar
  64. Lo I, Denef VJ, VerBerkmoes NC, Shah M, Goltsman D, DiBartolo G, Tyson GW, Allen EE, Ram RJ, Detter JC, Richardson PM, Thelen MP, Hettich RL, Banfield JF (2007) Strain-resolved community proteomics reveals recombining genomes of acidophilic bacteria. Nature 446:537–541PubMedCrossRefGoogle Scholar
  65. Maiden MC (2006) Multilocus sequence typing of bacteria. Annu Rev Microbiol 60:561–588PubMedCrossRefGoogle Scholar
  66. Maiden MC, Bygraves JA, Feil E, Morelli G, Russel JE, Urwin R, Zhang Q, Zhou J, Zurth K, Caugant DA, Feavers IM, Achtman M, Spratt BG (1998) Multilocus sequence typing: a portable approach to the identification of clones within populations of pathogenic microorganisms. Proc Natl Acad Sci USA 95:3140–3145PubMedCrossRefGoogle Scholar
  67. Majewski J (2001) Sexual isolation in bacteria. FEMS Microbiol Lett 199:161–169PubMedCrossRefGoogle Scholar
  68. Marttinen P, Hanage WP, Croucher NJ, Connor TR, Harris SR, Bentley SD, Corander J (2012) Detection of recombination events in bacterial genomes from large population samples. Nucleic Acids Res 40:e6PubMedCrossRefGoogle Scholar
  69. Mavroidi A, Aanensen DM, Godoy D, Skovsted IC, Kaltoft MS, Reeves PR, Bentley SD, Spratt BG (2007) Genetic relatedness of the Streptococcus pneumoniae capsular biosynthetic loci. J Bacteriol 189:7841–7855PubMedCrossRefGoogle Scholar
  70. McInerney JO, Pisani D, Bapteste E, O’Connell MJ (2011) The public goods hypothesis for the evolution of life on earth. Biol Direct 6:41PubMedCrossRefGoogle Scholar
  71. Meats E, Feil EJ, Stringer S, Cody AJ, Goldstein R, Kroll JS, Popovic T, Spratt BG (2003) Characterization of encapsulated and noncapsulated Haemophilus influenzae and determination of phylogenetic relationships by multilocus sequence typing. J Clin Microbiol 41:1623–1636PubMedCrossRefGoogle Scholar
  72. Medini D, Donati C, Tettelin H, Masignani V, Rappuoli R (2005) The microbial pan-genome. Curr Opin Genet Dev 15:589–594PubMedCrossRefGoogle Scholar
  73. Moore LR, Rocap G, Chisholm SW (1998) Physiology and molecular phylogeny of coexisting Prochlorococcus ecotypes. Nature 393:464–467PubMedCrossRefGoogle Scholar
  74. Nazer HM (1992) Early diagnosis of cystic fibrosis in Jordanian children. J Trop Pediatr 38:113–115PubMedCrossRefGoogle Scholar
  75. Orozco-terWengel P, Corander J, Schlotterer C (2011) Genealogical lineage sorting leads to significant, but incorrect Bayesian multilocus inference of population structure. Mol Ecol 20:1108–1121PubMedCrossRefGoogle Scholar
  76. Papke RT, Ramsing NB, Bateson MM, Ward DM (2003) Geographical isolation in hot spring cyanobacteria. Environ Microbiol 5:650–659PubMedCrossRefGoogle Scholar
  77. Papke RT, Zhaxybayeva O, Feil EJ, Sommerfeld K, Muise D, Doolittle WF (2007) Searching for species in haloarchaea. Proc Natl Acad Sci USA 104:14092–14097PubMedCrossRefGoogle Scholar
  78. Polz MF, Hunt DE, Preheim SP, Weinreich DM (2006) Patterns and mechanisms of genetic and phenotypic differentiation in marine microbes. Phil Trans R Soc Lond B 361:2009–2021CrossRefGoogle Scholar
  79. Preheim SP, Boucher Y, Wildschutte H, David LA, Veneziano D, Alm EJ, Polz MF (2011a) Metapopulation structure of Vibrionaceae among coastal marine invertebrates. Environ Microbiol 13:265–275PubMedCrossRefGoogle Scholar
  80. Preheim SP, Timberlake S, Polz MF (2011b) Merging taxonomy with ecological population prediction: a case study of Vibrionaceae. Appl Environ Microbiol 77:7195–7206PubMedCrossRefGoogle Scholar
  81. Price LB, Stegger M, Hasman H, Aziz M, Larsen J, Andersen PS, Pearson T, Waters AE, Foster JT, Schupp J, Gillece J, Driebe E, Liu CM, Springer B, Zdovc I, Battisti A, Franco A, Zmudzki J, Schwarz S, Butaye P, Jouy E, Pomba C, Porrero MC, Ruimy R, Smith TC, Robinson DA, Weese JS, Arriola CS, Yu F, Laurent F, Keim P, Skov R, Aarestrup FM (2012) Staphylococcus aureus CC398: host adaptation and emergence of methicillin resistance in livestock. mBio 3:e00305–e00311PubMedCrossRefGoogle Scholar
  82. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959PubMedGoogle Scholar
  83. Robinson DA, Enright MC (2004) Evolution of Staphylococcus aureus by large chromosomal replacements. J Bacteriol 186:1060–1064PubMedCrossRefGoogle Scholar
  84. Rocap G, Larimer FW, Lamerdin J, Malfatti S, Chain P, Ahlgren NA, Arellano A, Coleman M, Hauser L, Hess WR, Johnson ZI, Land M, Lindell D, Post AF, Regala W, Shah M, Shaw SL, Steglich C, Sullivan MB, Ting CS, Tolonen A, Webb EA, Zinser ER, Chisholm SW (2003) Genome divergence in two Prochlorococcus ecotypes reflects oceanic niche differentiation. Nature 424:1042–1047PubMedCrossRefGoogle Scholar
  85. Rosselló-Mora R, Amann R (2001) The species concept for prokaryotes. FEMS Microbiol Rev 25:39–67PubMedCrossRefGoogle Scholar
  86. Shapiro BJ, David LA, Friedman J, Alm EJ (2009) Looking for Darwin’s footprints in the microbial world. Trends Microbiol 17:196–204PubMedCrossRefGoogle Scholar
  87. Shapiro BJ, Friedman J, Cordero OX, Preheim SP, Timberlake SC, Szabo G, Polz MF, Alm EJ (2012) Population genomics of early events in the ecological differentiation of bacteria. Science 336:48–51PubMedCrossRefGoogle Scholar
  88. Sheppard SK, McCarthy ND, Falush D, Maiden MCJ (2008) Convergence of Campylobacter species: implications for bacterial evolution. Science 320:237–239PubMedCrossRefGoogle Scholar
  89. Smilllie CS, Smith MB, Friedman J, Cordero OX, Alm EJ (2011) Ecology drives a global network of gene exchange connecting the human microbiome. Nature 480:241–244CrossRefGoogle Scholar
  90. Smith JM, Smith NH, O’Rourke M, Spratt BG (1993) How clonal are bacteria? Proc Natl Acad Sci USA 90:4384–4388PubMedCrossRefGoogle Scholar
  91. Smith JM, Feil EJ, Smith NH (2000) Population structure and evolutionary dynamics of pathogenic bacteria. BioEssays 22:1115–1122PubMedCrossRefGoogle Scholar
  92. Spratt BG, Hanage WP, Feil EJ (2001a) The relative contribution of recombination and point mutation to the diversification of bacterial clones. Curr Opin Microbiol 4:602–606PubMedCrossRefGoogle Scholar
  93. Spratt BG, Hanage WP, Feil EJ (2001b) The relative contributions of recombination and point mutation to the diversification of bacterial clones. Curr Opin Microbiol 4:602–606PubMedCrossRefGoogle Scholar
  94. Stackebrandt E, Goebel BM (1994) Taxonomic note: a place for DNA-DNA reassociation kinetics and sequence analysis in the present species definition in bacteriology. Int J Syst Bacteriol 44:846–849CrossRefGoogle Scholar
  95. Szabo G, Preheim SP, Kauffman AKM, David LA, Shapiro BJ, Alm EJ, Polz MF (2012) Reproducibility of Vibrionaceae population structure in coastal bacterioplankton (Submitted)Google Scholar
  96. Tang J, Hanage WP, Fraser C, Corander J (2009) Identifying currents in the gene pool for bacterial populations using an integrative approach. PLoS Comput Biol 5:e1000455PubMedCrossRefGoogle Scholar
  97. Taylor JW, Jacobson DJ, Kroken S, Kasuga T, Geiser DM, Hibbett DS, Fisher MC (2000) Phylogenetic species recognition and species concept in fungi. Fungal Genet Biol 31:21–32PubMedCrossRefGoogle Scholar
  98. Tettelin H, Riley D, Cattuto C, Medini D (2008) Comparative genomics: the bacterial pan-genome. Curr Opin Microbiol 12:472–477CrossRefGoogle Scholar
  99. Thompson JR, Pacocha S, Pharino C, Klepac-Ceraj V, Hunt DE, Benoit J, Sarma-Rupavtarm R, Distel DL, Polz MF (2005) Genotypic diversity within a natural coastal bacterioplankton population. Science 307:1311–1313PubMedCrossRefGoogle Scholar
  100. Tyson GW, Banfield JF (2008) Rapidly evolving CRISPRs implicated in acquired resistance of microorganisms. Environ Microbiol 10:200–207PubMedGoogle Scholar
  101. Tyson GW, Chapman J, Hugenholtz P, Allen EE, Ram RJ, Richardson PM, Solovyev VV, Rubin EM, Rokhsar DS, Banfield JF (2004) Community structure and metabolism through reconstruction of microbial genomes from the environment. Nature 428:37–43PubMedCrossRefGoogle Scholar
  102. Waples RS, Gaggiotti O (2006) What is a population? An empirical evaluation of some genetic methods for identifying the number of gene pools and their degree of connectivity. Mol Ecol 15:1419–1439PubMedCrossRefGoogle Scholar
  103. Whitaker RJ, Grogan DW, Taylor JW (2003) Geographic barriers isolate endemic populations of hyperthermophilic archaea. Science 301:976–978PubMedCrossRefGoogle Scholar
  104. Wilmes P, Simmons SL, Denef VJ, Banfield JF (2009) The dynamic genetic repertoire of microbial communities. FEMS Microbiol Rev 33:109–132PubMedCrossRefGoogle Scholar
  105. Wozniak RA, Waldor MK (2010) Integrative and conjugative elements: mosaic mobile genetic elements enabling dynamic lateral gene flow. Nat Rev Microbiology 8:552–563CrossRefGoogle Scholar

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© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  1. 1.Parsons Laboratory, Department of Civil and Environmental EngineeringMassachusetts Institute of TechnologyCambridgeUSA
  2. 2.Department of EpidemiologyHarvard School of Public HealthBostonUSA

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