1887
No metrics data to plot.
The attempt to load metrics for this article has failed.
The attempt to plot a graph for these metrics has failed.

Transmission in the Origins of Bacterial Diversity, From Ecotypes to Phyla

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.
Buy this Microbiology Spectrum Article
Price Non-Member $15.00
  • Author: Frederick M. Cohan1
  • Editors: Fernando Baquero2, Emilio Bouza3, J.A. Gutiérrez-Fuentes4, Teresa M. Coque5
  • VIEW AFFILIATIONS HIDE AFFILIATIONS
    Affiliations: 1: Department of Biology, Wesleyan University, Middletown, CT; 2: Hospital Ramón y Cajal (IRYCIS), Madrid, Spain; 3: Hospital Ramón y Cajal (IRYCIS), Madrid, Spain; 4: Complutensis University, Madrid, Spain; 5: Hospital Ramón y Cajal (IRYCIS), Madrid, Spain
  • Source: microbiolspec October 2017 vol. 5 no. 5 doi:10.1128/microbiolspec.MTBP-0014-2016
  • Received 20 March 2017 Accepted 28 June 2017 Published 12 October 2017
  • Frederick M. Cohan, fcohan@wesleyan.edu
image of Transmission in the Origins of Bacterial Diversity, From Ecotypes to Phyla
    Preview this microbiology spectrum article:
    Zoom in
    Zoomout

    Transmission in the Origins of Bacterial Diversity, From Ecotypes to Phyla, Page 1 of 2

    | /docserver/preview/fulltext/microbiolspec/5/5/MTBP-0014-2016-1.gif /docserver/preview/fulltext/microbiolspec/5/5/MTBP-0014-2016-2.gif
  • Abstract:

    Any two lineages, no matter how distant they are now, began their divergence as one population splitting into two lineages that could coexist indefinitely. The rate of origin of higher-level taxa is therefore the product of the rate of speciation times the probability that two new species coexist long enough to reach a particular level of divergence. Here I have explored these two parameters of disparification in bacteria. Owing to low recombination rates, sexual isolation is not a necessary milestone of bacterial speciation. Rather, irreversible and indefinite divergence begins with ecological diversification, that is, transmission of a bacterial lineage to a new ecological niche, possibly to a new microhabitat but at least to new resources. Several algorithms use sequence data from a taxon of focus to identify phylogenetic groups likely to bear the dynamic properties of species. Identifying these newly divergent lineages allows us to characterize the genetic bases of speciation, as well as the ecological dimensions upon which new species diverge. Speciation appears to be least frequent when a given lineage has few new resources it can adopt, as exemplified by photoautotrophs, C1 heterotrophs, and obligately intracellular pathogens; speciation is likely most rapid for generalist heterotrophs. The genetic basis of ecological divergence may determine whether ecological divergence is irreversible and whether lineages will diverge indefinitely into the future. Long-term coexistence is most likely when newly divergent lineages utilize at least some resources not shared with the other and when the resources themselves will coexist into the remote future.

  • Citation: Cohan F. 2017. Transmission in the Origins of Bacterial Diversity, From Ecotypes to Phyla. Microbiol Spectrum 5(5):MTBP-0014-2016. doi:10.1128/microbiolspec.MTBP-0014-2016.

Key Concept Ranking

Bacteria and Archaea
0.6211038
Severe Acute Respiratory Syndrome
0.492275
0.6211038

References

1. Woese CR. 1987. Bacterial evolution. Microbiol Rev 51:221–271. [PubMed]
2. Rappé MS, Giovannoni SJ. 2003. The uncultured microbial majority. Annu Rev Microbiol 57:369–394. http://dx.doi.org/10.1146/annurev.micro.57.030502.090759. [PubMed]
3. Schloss PD, Handelsman J. 2004. Status of the microbial census. Microbiol Mol Biol Rev 68:686–691. http://dx.doi.org/10.1128/MMBR.68.4.686-691.2004. [PubMed]
4. Yarza P, Yilmaz P, Pruesse E, Glöckner FO, Ludwig W, Schleifer KH, Whitman WB, Euzéby J, Amann R, Rosselló-Móra R. 2014. Uniting the classification of cultured and uncultured bacteria and archaea using 16S rRNA gene sequences. Nat Rev Microbiol 12:635–64.5 http://dx.doi.org/10.1038/nrmicro3330. [PubMed]
5. Hug LA, Baker BJ, Anantharaman K, Brown CT, Probst AJ, Castelle CJ, Butterfield CN, Hernsdorf AW, Amano Y, Ise K, Suzuki Y, Dudek N, Relman DA, Finstad KM, Amundson R, Thomas BC, Banfield JF. 2016. A new view of the tree of life. Nat Microbiol 1:16048. http://dx.doi.org/10.1038/nmicrobiol.2016.48. [PubMed]
6. Sutcliffe IC. 2010. A phylum level perspective on bacterial cell envelope architecture. Trends Microbiol 18:464–470. http://dx.doi.org/10.1016/j.tim.2010.06.005. [PubMed]
7. Schimel J, Balser TC, Wallenstein M. 2007. Microbial stress-response physiology and its implications for ecosystem function. Ecology 88:1386–1394. http://dx.doi.org/10.1890/06-0219. [PubMed]
8. Adams PG, Cadby AJ, Robinson B, Tsukatani Y, Tank M, Wen J, Blankenship RE, Bryant DA, Hunter CN. 2013. Comparison of the physical characteristics of chlorosomes from three different phyla of green phototrophic bacteria. Biochim Biophys Acta 1827:1235–1244. http://dx.doi.org/10.1016/j.bbabio.2013.07.004. [PubMed]
9. Ward NL. 2010. Phylum XXV. Planctomycetes Garrity and Holt 2001, 137 emend. Ward (this volume), p 879–925. In Krieg NR, Staley JT, Brown DR, Hedlund BP, Paster BJ, Ward NL, Ludwig W, Whitman WB (ed), Bergey’s Manual of Systematic Bacteriology, 2nd ed, vol 4. The Bacteroidetes, Spirochaetes, Tenericutes (Mollicutes), Acidobacteria, Fibrobacteres, Fusobacteria, Dictyoglomi, Gemmatimonadetes, Lentisphaerae, Verrucomicrobia, Chlamydiae, and Planctomycetes. Springer, New York, NY.
10. Klein EA, Schlimpert S, Hughes V, Brun YV, Thanbichler M, Gitai Z. 2013. Physiological role of stalk lengthening in Caulobacter crescentus. Commun Integr Biol 6:e24561. http://dx.doi.org/10.4161/cib.24561. [PubMed]
11. Wagner JK, Setayeshgar S, Sharon LA, Reilly JP, Brun YV. 2006. A nutrient uptake role for bacterial cell envelope extensions. Proc Natl Acad Sci U S A 103:11772–11777. http://dx.doi.org/10.1073/pnas.0602047103. [PubMed]
12. Brochier-Armanet C, Talla E, Gribaldo S. 2009. The multiple evolutionary histories of dioxygen reductases: implications for the origin and evolution of aerobic respiration. Mol Biol Evol 26:285–297. http://dx.doi.org/10.1093/molbev/msn246. [PubMed]
13. Summers AO. 2006. Genetic linkage and horizontal gene transfer, the roots of the antibiotic multi-resistance problem. Anim Biotechnol 17:125–135. http://dx.doi.org/10.1080/10495390600957217. [PubMed]
14. Ray A, Kinch LN, de Souza Santos M, Grishin NV, Orth K, Salomon D. 2016. Proteomics analysis reveals previously uncharacterized virulence factors in Vibrio proteolyticus. mBio 7:e01077-e16. http://dx.doi.org/10.1128/mBio.01077-16. [PubMed]
15. Cohan FM. 2010. Synthetic biology: now that we’re creators, what should we create? Curr Biol 20:R675–R677. http://dx.doi.org/10.1016/j.cub.2010.07.005. [PubMed]
16. Martiny JB, Jones SE, Lennon JT, Martiny AC. 2015. Microbiomes in light of traits: a phylogenetic perspective. Science 350:aac9323. http://dx.doi.org/10.1126/science.aac9323. [PubMed]
17. Mulkidjanian AY, Koonin EV, Makarova KS, Mekhedov SL, Sorokin A, Wolf YI, Dufresne A, Partensky F, Burd H, Kaznadzey D, Haselkorn R, Galperin MY. 2006. The cyanobacterial genome core and the origin of photosynthesis. Proc Natl Acad Sci U S A 103:13126–13131. http://dx.doi.org/10.1073/pnas.0605709103. [PubMed]
18. Philippot L, Andersson SG, Battin TJ, Prosser JI, Schimel JP, Whitman WB, Hallin S. 2010. The ecological coherence of high bacterial taxonomic ranks. Nat Rev Microbiol 8:523–529. http://dx.doi.org/10.1038/nrmicro2367. [PubMed]
19. Antunes LC, Poppleton D, Klingl A, Criscuolo A, Dupuy B, Brochier-Armanet C, Beloin C, Gribaldo S. 2016. Phylogenomic analysis supports the ancestral presence of LPS-outer membranes in the Firmicutes. eLife 5:e14589. http://dx.doi.org/10.7554/eLife.14589. [PubMed]
20. Fierer N, Bradford MA, Jackson RB. 2007. Toward an ecological classification of soil bacteria. Ecology 88:1354–1364. http://dx.doi.org/10.1890/05-1839. [PubMed]
21. Tindall BJ, Rosselló-Móra R, Busse HJ, Ludwig W, Kämpfer P. 2010. Notes on the characterization of prokaryote strains for taxonomic purposes. Int J Syst Evol Microbiol 60:249–266. http://dx.doi.org/10.1099/ijs.0.016949-0. [PubMed]
22. Lagier JC, Khelaifia S, Alou MT, Ndongo S, Dione N, Hugon P, Caputo A, Cadoret F, Traore SI, Seck EH, Dubourg G, Durand G, Mourembou G, Guilhot E, Togo A, Bellali S, Bachar D, Cassir N, Bittar F, Delerce J, Mailhe M, Ricaboni D, Bilen M, Dangui Nieko NP, Dia Badiane NM, Valles C, Mouelhi D, Diop K, Million M, Musso D, Abrahão J, Azhar EI, Bibi F, Yasir M, Diallo A, Sokhna C, Djossou F, Vitton V, Robert C, Rolain JM, La Scola B, Fournier PE, Levasseur A, Raoult D. 2016. Culture of previously uncultured members of the human gut microbiota by culturomics. Nat Microbiol 1:16203. http://dx.doi.org/10.1038/nmicrobiol.2016.203. [PubMed]
23. Lerat E, Daubin V, Ochman H, Moran NA. 2005. Evolutionary origins of genomic repertoires in bacteria. PLoS Biol 3:e130. http://dx.doi.org/10.1371/journal.pbio.0030130. [PubMed]
24. de Queiroz K. 2005. Ernst Mayr and the modern concept of species. Proc Natl Acad Sci U S A 102(Suppl 1):6600–6607. http://dx.doi.org/10.1073/pnas.0502030102. [PubMed]
25. Cohan FM. 2017. Species. In Osmanaj B, Escalante Santos L (ed), Reference Module in Life Sciences HYPERLINK doi.org/10.1016/B978-0-12-809633-8.07184-3. Elsevier.
26. Cohan FM. 1994. The effects of rare but promiscuous genetic exchange on evolutionary divergence in prokaryotes. Am Nat 143:965–986. http://dx.doi.org/10.1086/285644.
27. Mallet J. 1995. A species definition for the modern synthesis. Trends Ecol Evol 10:294–299. http://dx.doi.org/10.1016/0169-5347(95)90031-4. [PubMed]
28. Cohan FM. 2011. Are species cohesive?—A view from bacteriology, p 43–65. In Walk S, Feng P (ed), Bacterial Population Genetics: A Tribute to Thomas S Whittam. American Society for Microbiology Press, Washington, DC. http://dx.doi.org/10.1128/9781555817114.ch5.
29. Negri MC, Lipsitch M, Blázquez J, Levin BR, Baquero F. 2000. Concentration-dependent selection of small phenotypic differences in TEM β-lactamase-mediated antibiotic resistance. Antimicrob Agents Chemother 44:2485–2491. http://dx.doi.org/10.1128/AAC.44.9.2485-2491.2000. [PubMed]
30. Ward DM, Cohan FM. 2005. Microbial diversity in hot spring cyanobacterial mats: pattern and prediction, p 185–202. In Inskeep WP, McDermott T (ed), Geothermal Biology and Geochemistry in Yellowstone National Park. Thermal Biology Institute, Bozeman, MT.
31. Levin BR, Bull JJ. 1994. Short-sighted evolution and the virulence of pathogenic microorganisms. Trends Microbiol 2:76–81. http://dx.doi.org/10.1016/0966-842X(94)90538-X.
32. Mayr E. 1963. Animal Species and Evolution. Belknap Press of Harvard University Press, Cambridge, MA. http://dx.doi.org/10.4159/harvard.9780674865327.
33. Wilkins JS. 2009. Species: A History of the Idea. University of California, Berkeley, CA.
34. Cohan FM. 2013. Species, p 56–511. In Maloy S, Hughes K (ed), Brenner’s Encyclopedia of Genetics, 2nd ed. Elsevier, Amsterdam, The Netherlands. https://doi.org/10.1016/B978-0-12-374984-0.01454-6.
35. Mallet J. 2008. Hybridization, ecological races and the nature of species: empirical evidence for the ease of speciation. Philos Trans R Soc Lond B Biol Sci 363:2971–2986. http://dx.doi.org/10.1098/rstb.2008.0081. [PubMed]
36. Schluter D. 2009. Evidence for ecological speciation and its alternative. Science 323:737–741. http://dx.doi.org/10.1126/science.1160006. [PubMed]
37. Rainey PB, Travisano M. 1998. Adaptive radiation in a heterogeneous environment. Nature 394:69–72. http://dx.doi.org/10.1038/27900. [PubMed]
38. Koeppel AF, Wertheim JO, Barone L, Gentile N, Krizanc D, Cohan FM. 2013. Speedy speciation in a bacterial microcosm: new species can arise as frequently as adaptations within a species. ISME J 7:1080–1091. http://dx.doi.org/10.1038/ismej.2013.3. [PubMed]
39. Treves DS, Manning S, Adams J. 1998. Repeated evolution of an acetate-crossfeeding polymorphism in long-term populations of Escherichia coli. Mol Biol Evol 15:789–797. http://dx.doi.org/10.1093/oxfordjournals.molbev.a025984. [PubMed]
40. Blount ZD, Borland CZ, Lenski RE. 2008. Historical contingency and the evolution of a key innovation in an experimental population of Escherichia coli. Proc Natl Acad Sci U S A 105:7899–7906. http://dx.doi.org/10.1073/pnas.0803151105. [PubMed]
41. Ellegaard KM, Klasson L, Näslund K, Bourtzis K, Andersson SG. 2013. Comparative genomics of Wolbachia and the bacterial species concept. PLoS Genet 9:e1003381. http://dx.doi.org/10.1371/journal.pgen.1003381. [PubMed]
42. Cadillo-Quiroz H, Didelot X, Held NL, Herrera A, Darling A, Reno ML, Krause DJ, Whitaker RJ. 2012. Patterns of gene flow define species of thermophilic Archaea. PLoS Biol 10:e1001265. http://dx.doi.org/10.1371/journal.pbio.1001265. [PubMed]
43. Shapiro BJ, Friedman J, Cordero OX, Preheim SP, Timberlake SC, Szabó G, Polz MF, Alm EJ. 2012. Population genomics of early events in the ecological differentiation of bacteria. Science 336:48–51. http://dx.doi.org/10.1126/science.1218198. [PubMed]
44. Melendrez MC, Becraft ED, Wood JM, Olsen MT, Bryant DA, Heidelberg JF, Rusch DB, Cohan FM, Ward DM. 2016. Recombination does not hinder formation or detection of ecological species of Synechococcus inhabiting a hot spring cyanobacterial mat. Front Microbiol 6:1540. http://dx.doi.org/10.3389/fmicb.2015.01540. [PubMed]
45. Hunt DE, David LA, Gevers D, Preheim SP, Alm EJ, Polz MF. 2008. Resource partitioning and sympatric differentiation among closely related bacterioplankton. Science 320:1081–1085. http://dx.doi.org/10.1126/science.1157890. [PubMed]
46. Cohan FM. 2016. Prokaryotic species concepts, p 119–129. In Kliman RM (ed), Encyclopedia of Evolutionary Biology, vol X. Academic Press, Oxford, United Kingdom.
47. Wiedenbeck J, Cohan FM. 2011. Origins of bacterial diversity through horizontal genetic transfer and adaptation to new ecological niches. FEMS Microbiol Rev 35:957–976. http://dx.doi.org/10.1111/j.1574-6976.2011.00292.x. [PubMed]
48. Haldane JB. 1932. The Causes of Evolution. Longmans, Green, and Co, London, United Kingdom.
49. Ward DM, Cohan FM, Bhaya D, Heidelberg JF, Kühl M, Grossman A. 2008. Genomics, environmental genomics and the issue of microbial species. Heredity (Edinb) 100:207–219. http://dx.doi.org/10.1038/sj.hdy.6801011. [PubMed]
50. Konstantinidis KT, Tiedje JM. 2005. Genomic insights that advance the species definition for prokaryotes. Proc Natl Acad Sci U S A 102:2567–2572. http://dx.doi.org/10.1073/pnas.0409727102. [PubMed]
51. Coyne JA, Orr HA. 2004. Speciation. Sinauer Associates, Sunderland, MA.
52. Cohan FM, Kopac SM. 2017. A theory-based pragmatism for discovering and classifying newly divergent species of bacterial pathogens, p 25–49. In Tibayrenc M (ed), Genetics and Evolution of Infectious Diseases, 2nd ed. Elsevier, Oxford, United Kingdom. http://dx.doi.org/10.1016/B978-0-12-799942-5.00002-0.
53. Cohan FM. 2016. Bacterial species concepts, p 119–129. In Kliman RM (ed), Encyclopedia of Evolutionary Biology, vol 1. Academic Press, Oxford, United Kingdom. http://dx.doi.org/10.1016/B978-0-12-800049-6.00230-4.
54. Staley JT. 2006. The bacterial species dilemma and the genomic-phylogenetic species concept. Philos Trans R Soc Lond B Biol Sci 361:1899–1909. http://dx.doi.org/10.1098/rstb.2006.1914. [PubMed]
55. Sikorski J. 2008. Populations under microevolutionary scrutiny: what will we gain? Arch Microbiol 189:1–5. http://dx.doi.org/10.1007/s00203-007-0294-x. [PubMed]
56. Ward DM. 1998. A natural species concept for prokaryotes. Curr Opin Microbiol 1:271–277. http://dx.doi.org/10.1016/S1369-5274(98)80029-5. [PubMed]
57. Rosselló-Mora R, Amann R. 2001. The species concept for prokaryotes. FEMS Microbiol Rev 25:39–67. http://dx.doi.org/10.1111/j.1574-6976.2001.tb00571.x. [PubMed]
58. Ward DM, Bateson MM, Ferris MJ, Kühl M, Wieland A, Koeppel A, Cohan FM. 2006. Cyanobacterial ecotypes in the microbial mat community of Mushroom Spring (Yellowstone National Park, Wyoming) as species-like units linking microbial community composition, structure and function. Philos Trans R Soc Lond B Biol Sci 361:1997–2008. http://dx.doi.org/10.1098/rstb.2006.1919. [PubMed]
59. Touchon M, Hoede C, Tenaillon O, Barbe V, Baeriswyl S, Bidet P, Bingen E, Bonacorsi S, Bouchier C, Bouvet O, Calteau A, Chiapello H, Clermont O, Cruveiller S, Danchin A, Diard M, Dossat C, Karoui ME, Frapy E, Garry L, Ghigo JM, Gilles AM, Johnson J, Le Bouguénec C, Lescat M, Mangenot S, Martinez-Jéhanne V, Matic I, Nassif X, Oztas S, Petit MA, Pichon C, Rouy Z, Ruf CS, Schneider D, Tourret J, Vacherie B, Vallenet D, Médigue C, Rocha EP, Denamur E. 2009. Organised genome dynamics in the Escherichia coli species results in highly diverse adaptive paths. PLoS Genet 5:e1000344. http://dx.doi.org/10.1371/journal.pgen.1000344. [PubMed]
60. Walk ST, Alm EW, Gordon DM, Ram JL, Toranzos GA, Tiedje JM, Whittam TS. 2009. Cryptic lineages of the genus Escherichia. Appl Environ Microbiol 75:6534–6544. http://dx.doi.org/10.1128/AEM.01262-09. [PubMed]
61. Gordon DM, Lee J. 1999. The genetic structure of enteric bacteria from Australian mammals. Microbiology 145:2673–2682. http://dx.doi.org/10.1099/00221287-145-10-2673. [PubMed]
62. Walk ST, Alm EW, Calhoun LM, Mladonicky JM, Whittam TS. 2007. Genetic diversity and population structure of Escherichia coli isolated from freshwater beaches. Environ Microbiol 9:2274–2288. http://dx.doi.org/10.1111/j.1462-2920.2007.01341.x. [PubMed]
63. Cohan FM, Kopac SM. 2011. Microbial genomics: E. coli relatives out of doors and out of body. Curr Biol 21:R587–R589. http://dx.doi.org/10.1016/j.cub.2011.06.011. [PubMed]
64. Welch RA, Burland V, Plunkett G III, Redford P, Roesch P, Rasko D, Buckles EL, Liou SR, Boutin A, Hackett J, Stroud D, Mayhew GF, Rose DJ, Zhou S, Schwartz DC, Perna NT, Mobley HL, Donnenberg MS, Blattner FR. 2002. Extensive mosaic structure revealed by the complete genome sequence of uropathogenic Escherichia coli. Proc Natl Acad Sci U S A 99:17020–17024. http://dx.doi.org/10.1073/pnas.252529799. [PubMed]
65. Lefébure T, Stanhope MJ. 2007. Evolution of the core and pan-genome of Streptococcus: positive selection, recombination, and genome composition. Genome Biol 8:R71. http://dx.doi.org/10.1186/gb-2007-8-5-r71. [PubMed]
66. Paul S, Dutta A, Bag SK, Das S, Dutta C. 2010. Distinct, ecotype-specific genome and proteome signatures in the marine cyanobacteria Prochlorococcus. BMC Genomics 11:103. http://dx.doi.org/10.1186/1471-2164-11-103. [PubMed]
67. Vernikos GS, Thomson NR, Parkhill J. 2007. Genetic flux over time in the Salmonella lineage. Genome Biol 8:R100. http://dx.doi.org/10.1186/gb-2007-8-6-r100. [PubMed]
68. Marri PR, Hao W, Golding GB. 2006. Gene gain and gene loss in Streptococcus: is it driven by habitat? Mol Biol Evol 23:2379–2391. http://dx.doi.org/10.1093/molbev/msl115. [PubMed]
69. Aboal M, Werner O, García-Fernández ME, Palazón JA, Cristóbal JC, Williams W. 2016. Should ecomorphs be conserved? The case of Nostoc flagelliforme, an endangered extremophile cyanobacteria. J Nat Conserv 30:52–64. http://dx.doi.org/10.1016/j.jnc.2016.01.001.
70. Dugat T, Lagrée AC, Maillard R, Boulouis HJ, Haddad N. 2015. Opening the black box of Anaplasma phagocytophilum diversity: current situation and future perspectives. Front Cell Infect Microbiol 5:61. http://dx.doi.org/10.3389/fcimb.2015.00061. [PubMed]
71. Kettler GC, Martiny AC, Huang K, Zucker J, Coleman ML, Rodrigue S, Chen F, Lapidus A, Ferriera S, Johnson J, Steglich C, Church GM, Richardson P, Chisholm SW. 2007. Patterns and implications of gene gain and loss in the evolution of Prochlorococcus. PLoS Genet 3:e231. http://dx.doi.org/10.1371/journal.pgen.0030231. [PubMed]
72. Oh PL, Benson AK, Peterson DA, Patil PB, Moriyama EN, Roos S, Walter J. 2010. Diversification of the gut symbiont Lactobacillus reuteri as a result of host-driven evolution. ISME J 4:377–387. http://dx.doi.org/10.1038/ismej.2009.123. [PubMed]
73. Choudhary DK, Johri BN. 2011. Ecological significance of microdiversity: coexistence among casing soil bacterial strains through allocation of nutritional resource. Indian J Microbiol 51:8–13. http://dx.doi.org/10.1007/s12088-011-0068-7. [PubMed]
74. Jaspers E, Overmann J. 2004. Ecological significance of microdiversity: identical 16S rRNA gene sequences can be found in bacteria with highly divergent genomes and ecophysiologies. Appl Environ Microbiol 70:4831–4839. http://dx.doi.org/10.1128/AEM.70.8.4831-4839.2004. [PubMed]
75. García-Martínez J, Acinas SG, Massana R, Rodríguez-Valera F. 2002. Prevalence and microdiversity of Alteromonas macleodii-like microorganisms in different oceanic regions. Environ Microbiol 4:42–50. http://dx.doi.org/10.1046/j.1462-2920.2002.00255.x. [PubMed]
76. Zimmerman AE, Martiny AC, Allison SD. 2013. Microdiversity of extracellular enzyme genes among sequenced prokaryotic genomes. ISME J 7:1187–1199. http://dx.doi.org/10.1038/ismej.2012.176. [PubMed]
77. Lanza VF, Baquero F, de la Cruz F, Coque TM. 2017. AcCNET (Accessory Genome Constellation Network): comparative genomics software for accessory genome analysis using bipartite networks. Bioinformatics 33:283–285. http://dx.doi.org/10.1093/bioinformatics/btw601. [PubMed]
78. 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 76:1349–1358. http://dx.doi.org/10.1128/AEM.01988-09. [PubMed]
79. 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 U S A 105:2504–2509. http://dx.doi.org/10.1073/pnas.0712205105. [PubMed]
80. Becraft ED, Wood JM, Rusch DB, Kühl M, Jensen SI, Bryant DA, Roberts DW, Cohan FM, Ward DM. 2015. The molecular dimension of microbial species: 1. Ecological distinctions among, and homogeneity within, putative ecotypes of Synechococcus inhabiting the cyanobacterial mat of Mushroom Spring, Yellowstone National Park. Front Microbiol 6:590. http://dx.doi.org/10.3389/fmicb.2015.00590. [PubMed]
81. Kopac S, Wang Z, Wiedenbeck J, Sherry J, Wu M, Cohan FM. 2014. Genomic heterogeneity and ecological speciation within one subspecies of Bacillus subtilis. Appl Environ Microbiol 80:4842–4853. http://dx.doi.org/10.1128/AEM.00576-14. [PubMed]
82. Stackebrandt E, Ebers J. 2006. Taxonomic parameters revisited: tarnished gold standards. Microbiol Today 33:152–155.
83. Francisco JC, Cohan FM, Krizanc D. 2014. Accuracy and efficiency of algorithms for the demarcation of bacterial ecotypes from DNA sequence data. Int J Bioinform Res Appl 10:409–425. http://dx.doi.org/10.1504/IJBRA.2014.062992. [PubMed]
84. Corander J, Marttinen P, Sirén J, Tang J. 2008. Enhanced Bayesian modelling in BAPS software for learning genetic structures of populations. BMC Bioinformatics 9:539. http://dx.doi.org/10.1186/1471-2105-9-539. [PubMed]
85. Barraclough TG, Hughes M, Ashford-Hodges N, Fujisawa T. 2009. Inferring evolutionarily significant units of bacterial diversity from broad environmental surveys of single-locus data. Biol Lett 5:425–428. http://dx.doi.org/10.1098/rsbl.2009.0091. [PubMed]
86. Eren AM, Morrison HG, Lescault PJ, Reveillaud J, Vineis JH, Sogin ML. 2015. Minimum entropy decomposition: unsupervised oligotyping for sensitive partitioning of high-throughput marker gene sequences. ISME J 9:968–979. http://dx.doi.org/10.1038/ismej.2014.195. [PubMed]
87. Cohan FM, Koeppel AF. 2008. The origins of ecological diversity in prokaryotes. Curr Biol 18:R1024–R1034. http://dx.doi.org/10.1016/j.cub.2008.09.014. [PubMed]
88. Cohan FM, Koeppel A, Krizanc D. 2006. Sequence-based discovery of ecological diversity within Legionella, p 367–376. In Cianciotto NP, Abu Kwaik Y, Edelstein PH, Fields BS, Geary DF, Harrison TG, Joseph C, Ratcliff RM, Stout JE, Swanson MS (ed), Legionella: State of the Art 30 Years after Its Recognition. ASM Press, Washington, DC. http://dx.doi.org/10.1128/9781555815660.ch88
89. Manning SD, Motiwala AS, Springman AC, Qi W, Lacher DW, Ouellette LM, Mladonicky JM, Somsel P, Rudrik JT, Dietrich SE, Zhang W, Swaminathan B, Alland D, Whittam TS. 2008. Variation in virulence among clades of Escherichia coli O157:H7 associated with disease outbreaks. Proc Natl Acad Sci U S A 105:4868–4873. http://dx.doi.org/10.1073/pnas.0710834105. [PubMed]
90. Smith NH, Gordon SV, de la Rua-Domenech R, Clifton-Hadley RS, Hewinson RG. 2006. Bottlenecks and broomsticks: the molecular evolution of Mycobacterium bovis. Nat Rev Microbiol 4:670–681. http://dx.doi.org/10.1038/nrmicro1472. [PubMed]
91. Brisson D, Dykhuizen DE. 2004. ospC diversity in Borrelia burgdorferi: different hosts are different niches. Genetics 168:713–722. http://dx.doi.org/10.1534/genetics.104.028738. [PubMed]
92. Sikorski J, Brambilla E, Kroppenstedt RM, Tindall BJ. 2008. The temperature-adaptive fatty acid content in Bacillus simplex strains from ’Evolution Canyon’, Israel. Microbiology 154:2416–2426. http://dx.doi.org/10.1099/mic.0.2007/016105-0. [PubMed]
93. Allewalt JP, Bateson MM, Revsbech NP, Slack K, Ward DM. 2006. Effect of temperature and light on growth of and photosynthesis by Synechococcus isolates typical of those predominating in the octopus spring microbial mat community of Yellowstone National Park. Appl Environ Microbiol 72:544–550. http://dx.doi.org/10.1128/AEM.72.1.544-550.2006. [PubMed]
94. Bhaya D, Grossman AR, Steunou AS, Khuri N, Cohan FM, Hamamura N, Melendrez MC, Bateson MM, Ward DM, Heidelberg JF. 2007. Population level functional diversity in a microbial community revealed by comparative genomic and metagenomic analyses. ISME J 1:703–713. http://dx.doi.org/10.1038/ismej.2007.46. [PubMed]
95. Olsen MT, Nowack S, Wood JM, Becraft ED, LaButti K, Lipzen A, Martin J, Schackwitz WS, Rusch DB, Cohan FM, Bryant DA, Ward DM. 2015. The molecular dimension of microbial species: 3. Comparative genomics of Synechococcus strains with different light responses and in situ diel transcription patterns of associated putative ecotypes in the Mushroom Spring microbial mat. Front Microbiol 6:604. http://dx.doi.org/10.3389/fmicb.2015.00604. [PubMed]
96. Gogarten JP, Townsend JP. 2005. Horizontal gene transfer, genome innovation and evolution. Nat Rev Microbiol 3:679–687. http://dx.doi.org/10.1038/nrmicro1204. [PubMed]
97. Ochman H, Lawrence JG, Groisman EA. 2000. Lateral gene transfer and the nature of bacterial innovation. Nature 405:299–304. http://dx.doi.org/10.1038/35012500. [PubMed]
98. Bantinaki E, Kassen R, Knight CG, Robinson Z, Spiers AJ, Rainey PB. 2007. Adaptive divergence in experimental populations of Pseudomonas fluorescens. III. Mutational origins of wrinkly spreader diversity. Genetics 176:441–453. http://dx.doi.org/10.1534/genetics.106.069906. [PubMed]
99. Koeppel AF, Wertheim JO, Barone L, Gentile N, Krizanc D, Cohan FM. 2013. Speedy speciation in a bacterial microcosm: New species can arise as frequently as adaptations within a species. ISME J 7:1080–1091. [PubMed]
100. Blount ZD, Barrick JE, Davidson CJ, Lenski RE. 2012. Genomic analysis of a key innovation in an experimental Escherichia coli population. Nature 489:513–518. http://dx.doi.org/10.1038/nature11514. [PubMed]
101. Becker NS, Margos G, Blum H, Krebs S, Graf A, Lane RS, Castillo-Ramírez S, Sing A, Fingerle V. 2016. Recurrent evolution of host and vector association in bacteria of the Borrelia burgdorferi sensu lato species complex. BMC Genomics 17:734. http://dx.doi.org/10.1186/s12864-016-3016-4. [PubMed]
102. Sokurenko EV, Chesnokova V, Dykhuizen DE, Ofek I, Wu XR, Krogfelt KA, Struve C, Schembri MA, Hasty DL. 1998. Pathogenic adaptation of Escherichia coli by natural variation of the FimH adhesin. Proc Natl Acad Sci U S A 95:8922–8926. http://dx.doi.org/10.1073/pnas.95.15.8922. [PubMed]
103. D’Argenio DA, Wu M, Hoffman LR, Kulasekara HD, Déziel E, Smith EE, Nguyen H, Ernst RK, Larson Freeman TJ, Spencer DH, Brittnacher M, Hayden HS, Selgrade S, Klausen M, Goodlett DR, Burns JL, Ramsey BW, Miller SI. 2007. Growth phenotypes of Pseudomonas aeruginosa lasR mutants adapted to the airways of cystic fibrosis patients. Mol Microbiol 64:512–533. http://dx.doi.org/10.1111/j.1365-2958.2007.05678.x. [PubMed]
104. Mowat E, Paterson S, Fothergill JL, Wright EA, Ledson MJ, Walshaw MJ, Brockhurst MA, Winstanley C. 2011. Pseudomonas aeruginosa population diversity and turnover in cystic fibrosis chronic infections. Am J Respir Crit Care Med 183:1674–1679. http://dx.doi.org/10.1164/rccm.201009-1430OC. [PubMed]
105. Chaloner GL, Palmira Ventosilla, Birtles RJ. 2011. Multi-locus sequence analysis reveals profound genetic diversity among isolates of the human pathogen Bartonella bacilliformis. PLoS Negl Trop Dis 5:e1248. http://dx.doi.org/10.1371/journal.pntd.0001248. [PubMed]
106. Paul S, Minnick MF, Chattopadhyay S. 2016. Mutation-driven divergence and convergence indicate adaptive evolution of the intracellular human-restricted pathogen, Bartonella bacilliformis. PLoS Negl Trop Dis 10:e0004712. http://dx.doi.org/10.1371/journal.pntd.0004712. [PubMed]
107. Wildschutte H, Lawrence JG. 2007. Differential Salmonella survival against communities of intestinal amoebae. Microbiology 153:1781–1789. http://dx.doi.org/10.1099/mic.0.2006/003616-0. [PubMed]
108. Toll-Riera M, San Millan A, Wagner A, MacLean RC. 2016. The genomic basis of evolutionary innovation in Pseudomonas aeruginosa. PLoS Genet 12:e1006005. http://dx.doi.org/10.1371/journal.pgen.1006005. [PubMed]
109. Popa O, Dagan T. 2011. Trends and barriers to lateral gene transfer in prokaryotes. Curr Opin Microbiol 14:615–623. http://dx.doi.org/10.1016/j.mib.2011.07.027. [PubMed]
110. Zawadzki P, Cohan FM. 1995. The size and continuity of DNA segments integrated in Bacillus transformation. Genetics 141:1231–1243. [PubMed]
111. Derbyshire KM, Gray TA. 2014. Distributive conjugal transfer: new insights into horizontal gene transfer and genetic exchange in mycobacteria. Microbiol Spectr 2:MGM2-0022-2013. http://dx.doi.org/10.1128/microbiolspec.MGM2-0022-2013.
112. Novais C, Tedim AP, Lanza VF, Freitas AR, Silveira E, Escada R, Roberts AP, Al-Haroni M, Baquero F, Peixe L, Coque TM. 2016. Co-diversification of Enterococcus faecium core genomes and PBP5: evidences of pbp5 horizontal transfer. Front Microbiol 7:1581. http://dx.doi.org/10.3389/fmicb.2016.01581. [PubMed]
113. Lassalle F, Campillo T, Vial L, Baude J, Costechareyre D, Chapulliot D, Shams M, Abrouk D, Lavire C, Oger-Desfeux C, Hommais F, Guéguen L, Daubin V, Muller D, Nesme X. 2011. Genomic species are ecological species as revealed by comparative genomics in Agrobacterium tumefaciens. Genome Biol Evol 3:762–781. http://dx.doi.org/10.1093/gbe/evr070. [PubMed]
114. Gogarten JP, Townsend JP. 2005. Horizontal gene transfer, genome innovation, and evolution. Nat Rev Microbiol 3:679–687. http://dx.doi.org/10.1038/nrmicro1204. [PubMed]
115. Anantha RP, McVeigh AL, Lee LH, Agnew MK, Cassels FJ, Scott DA, Whittam TS, Savarino SJ. 2004. Evolutionary and functional relationships of colonization factor antigen I and other class 5 adhesive fimbriae of enterotoxigenic Escherichia coli. Infect Immun 72:7190–7201. http://dx.doi.org/10.1128/IAI.72.12.7190-7201.2004. [PubMed]
116. Fondi M, Fani R. 2010. The horizontal flow of the plasmid resistome: clues from inter-generic similarity networks. Environ Microbiol 12:3228–3242. http://dx.doi.org/10.1111/j.1462-2920.2010.02295.x. [PubMed]
117. Amarir-Bouhram J, Goin M, Petit MA. 2011. Low efficiency of homology-facilitated illegitimate recombination during conjugation in Escherichia coli. PLoS One 6:e28876. http://dx.doi.org/10.1371/journal.pone.0028876. [PubMed]
118. Smith JM, Dowson CG, Spratt BG. 1991. Localized sex in bacteria. Nature 349:29–31. http://dx.doi.org/10.1038/349029a0. [PubMed]
119. Jacob F, Monod J. 1961. Genetic regulatory mechanisms in the synthesis of proteins. J Mol Biol 3:318–356. http://dx.doi.org/10.1016/S0022-2836(61)80072-7. [PubMed]
120. Lawrence JG, Ochman H. 1998. Molecular archaeology of the Escherichia coli genome. Proc Natl Acad Sci U S A 95:9413–9417. http://dx.doi.org/10.1073/pnas.95.16.9413. [PubMed]
121. Lawrence JG, Roth JR. 1996. Selfish operons: horizontal transfer may drive the evolution of gene clusters. Genetics 143:1843–1860. [PubMed]
122. Lawrence JG. 1997. Selfish operons and speciation by gene transfer. Trends Microbiol 5:355–359. http://dx.doi.org/10.1016/S0966-842X(97)01110-4. [PubMed]
123. Lawrence JG. 1999. Gene transfer, speciation, and the evolution of bacterial genomes. Curr Opin Microbiol 2:519–523. http://dx.doi.org/10.1016/S1369-5274(99)00010-7. [PubMed]
124. Kashtan N, Roggensack SE, Rodrigue S, Thompson JW, Biller SJ, Coe A, Ding H, Marttinen P, Malmstrom RR, Stocker R, Follows MJ, Stepanauskas R, Chisholm SW. 2014. Single-cell genomics reveals hundreds of coexisting subpopulations in wild Prochlorococcus. Science 344:416–420. http://dx.doi.org/10.1126/science.1248575. [PubMed]
125. López-Pérez M, Gonzaga A, Rodriguez-Valera F. 2013. Genomic diversity of “deep ecotype” Alteromonas macleodii isolates: evidence for Pan-Mediterranean clonal frames. Genome Biol Evol 5:1220–1232. http://dx.doi.org/10.1093/gbe/evt089. [PubMed]
126. Arsène-Ploetze F, Koechler S, Marchal M, Coppée JY, Chandler M, Bonnefoy V, Brochier-Armanet C, Barakat M, Barbe V, Battaglia-Brunet F, Bruneel O, Bryan CG, Cleiss-Arnold J, Cruveiller S, Erhardt M, Heinrich-Salmeron A, Hommais F, Joulian C, Krin E, Lieutaud A, Lièvremont D, Michel C, Muller D, Ortet P, Proux C, Siguier P, Roche D, Rouy Z, Salvignol G, Slyemi D, Talla E, Weiss S, Weissenbach J, Médigue C, Bertin PN. 2010. Structure, function, and evolution of the Thiomonas spp. genome. PLoS Genet 6:e1000859. http://dx.doi.org/10.1371/journal.pgen.1000859. [PubMed]
127. Barlow M. 2009. What antimicrobial resistance has taught us about horizontal gene transfer. Methods Mol Biol 532:397–411. http://dx.doi.org/10.1007/978-1-60327-853-9_23. [PubMed]
128. Croucher NJ, Klugman KP. 2014. The emergence of bacterial “hopeful monsters”. mBio 5:e01550-e14. http://dx.doi.org/10.1128/mBio.01550-14. [PubMed]
129. Goldschmidt R. 1933. Some aspects of evolution. Science 78:539–547. http://dx.doi.org/10.1126/science.78.2033.539. [PubMed]
130. Segovia L, Piñero D, Palacios R, Martínez-Romero E. 1991. Genetic structure of a soil population of nonsymbiotic Rhizobium leguminosarum. Appl Environ Microbiol 57:426–433. [PubMed]
131. Robins-Browne RM, Holt KE, Ingle DJ, Hocking DM, Yang J, Tauschek M. 2016. Are Escherichia coli pathotypes still relevant in the era of whole-genome sequencing? Front Cell Infect Microbiol 6:141. http://dx.doi.org/10.3389/fcimb.2016.00141. [PubMed]
132. Lanza VF, de Toro M, Garcillán-Barcia MP, Mora A, Blanco J, Coque TM, de la Cruz F. 2014. Plasmid flux in Escherichia coli ST131 sublineages, analyzed by plasmid constellation network (PLACNET), a new method for plasmid reconstruction from whole genome sequences. PLoS Genet 10:e1004766. http://dx.doi.org/10.1371/journal.pgen.1004766. [PubMed]
133. Kumar N, Lad G, Giuntini E, Kaye ME, Udomwong P, Shamsani NJ, Young JP, Bailly X. 2015. Bacterial genospecies that are not ecologically coherent: population genomics of Rhizobium leguminosarum. Open Biol 5:140133. http://dx.doi.org/10.1098/rsob.140133. [PubMed]
134. Wernegreen JJ, Harding EE, Riley MA. 1997. Rhizobium gone native: unexpected plasmid stability of indigenous Rhizobium leguminosarum. Proc Natl Acad Sci U S A 94:5483–5488. http://dx.doi.org/10.1073/pnas.94.10.5483. [PubMed]
135. Smith JM, Smith NH, O’Rourke M, Spratt BG. 1993. How clonal are bacteria? Proc Natl Acad Sci U S A 90:4384–4388. http://dx.doi.org/10.1073/pnas.90.10.4384. [PubMed]
136. Baltrus DA. 2013. Exploring the costs of horizontal gene transfer. Trends Ecol Evol 28:489–495. http://dx.doi.org/10.1016/j.tree.2013.04.002. [PubMed]
137. Hao W, Golding GB. 2006. The fate of laterally transferred genes: life in the fast lane to adaptation or death. Genome Res 16:636–643. http://dx.doi.org/10.1101/gr.4746406. [PubMed]
138. Andersson DI, Levin BR. 1999. The biological cost of antibiotic resistance. Curr Opin Microbiol 2:489–493. http://dx.doi.org/10.1016/S1369-5274(99)00005-3. [PubMed]
139. Cohan FM, King EC, Zawadzki P. 1994. Amelioration of the deleterious pleiotropic effects of an adaptive mutation in Bacillus subtilis. Evolution 48:81–95. http://dx.doi.org/10.1111/j.1558-5646.1994.tb01296.x. [PubMed]
140. Maisnier-Patin S, Paulander W, Pennhag A, Andersson DI. 2007. Compensatory evolution reveals functional interactions between ribosomal proteins S12, L14 and L19. J Mol Biol 366:207–215. http://dx.doi.org/10.1016/j.jmb.2006.11.047. [PubMed]
141. Dougherty K, Smith BA, Moore AF, Maitland S, Fanger C, Murillo R, Baltrus DA. 2014. Multiple phenotypic changes associated with large-scale horizontal gene transfer. PLoS One 9:e102170. http://dx.doi.org/10.1371/journal.pone.0102170. [PubMed]
142. Levin BR, Perrot V, Walker N. 2000. Compensatory mutations, antibiotic resistance and the population genetics of adaptive evolution in bacteria. Genetics 154:985–997. [PubMed]
143. Liu Y, Lai Q, Göker M, Meier-Kolthoff JP, Wang M, Sun Y, Wang L, Shao Z. 2015. Genomic insights into the taxonomic status of the Bacillus cereus group. Sci Rep 5:14082. http://dx.doi.org/10.1038/srep14082. [PubMed]
144. Clausen J, Keck DD, Hiesey WM. 1947. Heredity of geographically and ecologically isolated races. Am Nat 81:114–133. http://dx.doi.org/10.1086/281507. [PubMed]
145. Summers RW, Broome A. 2012. Associations between crossbills and North American conifers in Scotland. For Ecol Manage 271:37–45. http://dx.doi.org/10.1016/j.foreco.2012.01.016.
146. Wilson DS, Yoshimura J. 1994. On the coexistence of specialists and generalists. Am Nat 144:692–707. http://dx.doi.org/10.1086/285702.
147. Morris JJ. 2015. Black Queen evolution: the role of leakiness in structuring microbial communities. Trends Genet 31:475–482. http://dx.doi.org/10.1016/j.tig.2015.05.004. [PubMed]
148. Fry JD. 1996. The evolution of host-specialization: are trade-offs overrated? Am Nat 148:S84–S107. http://dx.doi.org/10.1086/285904.
149. Cui B, He Q, Zhang K, Chen X. 2011. Determinants of annual-perennial plant zonation across a salt-fresh marsh interface: a multistage assessment. Oecologia 166:1067–1075. http://dx.doi.org/10.1007/s00442-011-1944-x. [PubMed]
150. Becraft ED, Cohan FM, Kühl M, Jensen SI, Ward DM. 2011. Fine-scale distribution patterns of Synechococcus ecological diversity in microbial mats of Mushroom Spring, Yellowstone National Park. Appl Environ Microbiol 77:7689–7697. http://dx.doi.org/10.1128/AEM.05927-11. [PubMed]
151. Martiny AC, Tai AP, Veneziano D, Primeau F, Chisholm SW. 2009. Taxonomic resolution, ecotypes and the biogeography of Prochlorococcus. Environ Microbiol 11:823–832. http://dx.doi.org/10.1111/j.1462-2920.2008.01803.x. [PubMed]
152. Nevo E. 2014. Evolution in action: adaptation and incipient sympatric speciation with gene flow across life at “Evolution Canyon”, Israel. Isr J Ecol Evol 60:85–98. http://dx.doi.org/10.1080/15659801.2014.986879.
153. Perry EB. 2007. Sequence-based discovery of ecological diversity in Bacillus from natural communities. M.S thesis. Wesleyan University, Middletown, CT.
154. Kopac SM. 2014. Ecological dimensions of significance in speciation in Bacillus subtilis and Bacillus licheniformis. Ph.D. dissertation. Wesleyan University, Middletown, CT.
155. Feingersch R, Philosof A, Mejuch T, Glaser F, Alalouf O, Shoham Y, Béjà O. 2012. Potential for phosphite and phosphonate utilization by Prochlorococcus. ISME J 6:827–834. http://dx.doi.org/10.1038/ismej.2011.149. [PubMed]
156. Cohan FM. 2016. Bacterial speciation: genetic sweeps in bacterial species. Curr Biol 26:R112–R115. http://dx.doi.org/10.1016/j.cub.2015.10.022. [PubMed]
157. Puentes-Téllez PE, van Elsas JD. 2015. Differential stress resistance and metabolic traits underlie coexistence in a sympatrically evolved bacterial population. Environ Microbiol 17:889–900. http://dx.doi.org/10.1111/1462-2920.12551. [PubMed]
158. Deng J, Brettar I, Luo C, Auchtung J, Konstantinidis KT, Rodrigues JLM, Höfle M, Tiedje JM. 2014. Stability, genotypic and phenotypic diversity of Shewanella baltica in the redox transition zone of the Baltic Sea. Environ Microbiol 16:1854–1866. http://dx.doi.org/10.1111/1462-2920.12344. [PubMed]
159. Biderre-Petit C, Jézéquel D, Dugat-Bony E, Lopes F, Kuever J, Borrel G, Viollier E, Fonty G, Peyret P. 2011. Identification of microbial communities involved in the methane cycle of a freshwater meromictic lake. FEMS Microbiol Ecol 77:533–545. http://dx.doi.org/10.1111/j.1574-6941.2011.01134.x. [PubMed]
160. Kalyuzhnaya MG, Lapidus A, Ivanova N, Copeland AC, McHardy AC, Szeto E, Salamov A, Grigoriev IV, Suciu D, Levine SR, Markowitz VM, Rigoutsos I, Tringe SG, Bruce DC, Richardson PM, Lidstrom ME, Chistoserdova L. 2008. High-resolution metagenomics targets specific functional types in complex microbial communities. Nat Biotechnol 26:1029–1034. http://dx.doi.org/10.1038/nbt.1488. [PubMed]
161. Smith NH, Kremer K, Inwald J, Dale J, Driscoll JR, Gordon SV, van Soolingen D, Hewinson RG, Smith JM. 2006. Ecotypes of the Mycobacterium tuberculosis complex. J Theor Biol 239:220–225. http://dx.doi.org/10.1016/j.jtbi.2005.08.036. [PubMed]
162. Mechai S, Margos G, Feil EJ, Barairo N, Lindsay LR, Michel P, Ogden NH. 2016. Evidence for host-genotype associations of Borrelia burgdorferi sensu stricto. PLoS One 11:e0149345. http://dx.doi.org/10.1371/journal.pone.0149345. [PubMed]
163. Vuong HB, Canham CD, Fonseca DM, Brisson D, Morin PJ, Smouse PE, Ostfeld RS. 2014. Occurrence and transmission efficiencies of Borrelia burgdorferi ospC types in avian and mammalian wildlife. Infect Genet Evol 27:594–600. http://dx.doi.org/10.1016/j.meegid.2013.12.011. [PubMed]
164. Clark MA, Moran NA, Baumann P, Wernegreen JJ. 2000. Cospeciation between bacterial endosymbionts (Buchnera) and a recent radiation of aphids (Uroleucon) and pitfalls of testing for phylogenetic congruence. Evolution 54:517–525. http://dx.doi.org/10.1111/j.0014-3820.2000.tb00054.x. [PubMed]
165. Jackson AP, Charleston MA. 2004. A cophylogenetic perspective of RNA-virus evolution. Mol Biol Evol 21:45–57. http://dx.doi.org/10.1093/molbev/msg232. [PubMed]
166. Woolhouse M, Gaunt E. 2007. Ecological origins of novel human pathogens. Crit Rev Microbiol 33:231–242. http://dx.doi.org/10.1080/10408410701647560. [PubMed]
167. Himsworth CG, Parsons KL, Jardine C, Patrick DM. 2013. Rats, cities, people, and pathogens: a systematic review and narrative synthesis of literature regarding the ecology of rat-associated zoonoses in urban centers. Vector Borne Zoonotic Dis 13:349–359. http://dx.doi.org/10.1089/vbz.2012.1195. [PubMed]
168. Azhar EI, El-Kafrawy SA, Farraj SA, Hassan AM, Al-Saeed MS, Hashem AM, Madani TA. 2014. Evidence for camel-to-human transmission of MERS coronavirus. N Engl J Med 370:2499–2505. http://dx.doi.org/10.1056/NEJMoa1401505. [PubMed]
169. Mindell DP. 2006. The Evolving World: Evolution in Everyday Life. Harvard University Press, Cambridge, MA. http://dx.doi.org/10.4159/9780674041080.
170. Reusken CB, Raj VS, Koopmans MP, Haagmans BL. 2016. Cross host transmission in the emergence of MERS coronavirus. Curr Opin Virol 16:55–62. http://dx.doi.org/10.1016/j.coviro.2016.01.004. [PubMed]
171. Lo Presti A, Cella E, Giovanetti M, Lai A, Angeletti S, Zehender G, Ciccozzi M. 2016. Origin and evolution of Nipah virus. J Med Virol 88:380–388. http://dx.doi.org/10.1002/jmv.24345. [PubMed]
172. Field HE. 2016. Hendra virus ecology and transmission. Curr Opin Virol 16:120–125. http://dx.doi.org/10.1016/j.coviro.2016.02.004. [PubMed]
173. Han HJ, Wen HL, Zhou CM, Chen FF, Luo LM, Liu JW, Yu XJ. 2015. Bats as reservoirs of severe emerging infectious diseases. Virus Res 205:1–6. http://dx.doi.org/10.1016/j.virusres.2015.05.006. [PubMed]
174. Marí Saéz A, Weiss S, Nowak K, Lapeyre V, Zimmermann F, Düx A, Kühl HS, Kaba M, Regnaut S, Merkel K, Sachse A, Thiesen U, Villányi L, Boesch C, Dabrowski PW, Radonić A, Nitsche A, Leendertz SA, Petterson S, Becker S, Krähling V, Couacy-Hymann E, Akoua-Koffi C, Weber N, Schaade L, Fahr J, Borchert M, Gogarten JF, Calvignac-Spencer S, Leendertz FH. 2015. Investigating the zoonotic origin of the West African Ebola epidemic. EMBO Mol Med 7:17–23. http://dx.doi.org/10.15252/emmm.201404792. [PubMed]
175. Streicker DG, Turmelle AS, Vonhof MJ, Kuzmin IV, McCracken GF, Rupprecht CE. 2010. Host phylogeny constrains cross-species emergence and establishment of rabies virus in bats. Science 329:676–679. http://dx.doi.org/10.1126/science.1188836. [PubMed]
176. Fisher ML, Castillo C, Mecsas J. 2007. Intranasal inoculation of mice with Yersinia pseudotuberculosis causes a lethal lung infection that is dependent on Yersinia outer proteins and PhoP. Infect Immun 75:429–442. http://dx.doi.org/10.1128/IAI.01287-06. [PubMed]
177. Sun YC, Jarrett CO, Bosio CF, Hinnebusch BJ. 2014. Retracing the evolutionary path that led to flea-borne transmission of Yersinia pestis. Cell Host Microbe 15:578–586. http://dx.doi.org/10.1016/j.chom.2014.04.003. [PubMed]
178. Bessen DE. 2009. Population biology of the human restricted pathogen, Streptococcus pyogenes. Infect Genet Evol 9:581–593. http://dx.doi.org/10.1016/j.meegid.2009.03.002. [PubMed]
179. Gonzales-Siles L, Sjöling Å. 2016. The different ecological niches of enterotoxigenic Escherichia coli. Environ Microbiol 18:741–751. http://dx.doi.org/10.1111/1462-2920.13106. [PubMed]
180. Linke K, Rückerl I, Brugger K, Karpiskova R, Walland J, Muri-Klinger S, Tichy A, Wagner M, Stessl B. 2014. Reservoirs of Listeria species in three environmental ecosystems. Appl Environ Microbiol 80:5583–5592. http://dx.doi.org/10.1128/AEM.01018-14. [PubMed]
181. Zhu B, Ibrahim M, Cui Z, Xie G, Jin G, Kube M, Li B, Zhou X. 2016. Multi-omics analysis of niche specificity provides new insights into ecological adaptation in bacteria. ISME J 10:2072–2075. http://dx.doi.org/10.1038/ismej.2015.251. [PubMed]
182. Cutter AD, Gray JC. 2016. Ephemeral ecological speciation and the latitudinal biodiversity gradient. Evolution 70:2171–2185. http://dx.doi.org/10.1111/evo.13030. [PubMed]
183. Vos M, Didelot X. 2009. A comparison of homologous recombination rates in bacteria and archaea. ISME J 3:199–208. http://dx.doi.org/10.1038/ismej.2008.93. [PubMed]
184. Sheppard SK, McCarthy ND, Jolley KA, Maiden MC. 2011. Introgression in the genus Campylobacter: generation and spread of mosaic alleles. Microbiology 157:1066–1074. http://dx.doi.org/10.1099/mic.0.045153-0. [PubMed]
185. Baquero F. 2011. The 2010 Garrod Lecture: The dimensions of evolution in antibiotic resistance: ex unibus plurum et ex pluribus unum. J Antimicrob Chemother 66:1659–1672. http://dx.doi.org/10.1093/jac/dkr214. [PubMed]
186. Vos M. 2011. A species concept for bacteria based on adaptive divergence. Trends Microbiol 19:1–7. http://dx.doi.org/10.1016/j.tim.2010.10.003. [PubMed]
187. Doolittle WF, Zhaxybayeva O. 2009. On the origin of prokaryotic species. Genome Res 19:744–756. http://dx.doi.org/10.1101/gr.086645.108. [PubMed]
188. Bendall ML, Stevens SL, Chan LK, Malfatti S, Schwientek P, Tremblay J, Schackwitz W, Martin J, Pati A, Bushnell B, Froula J, Kang D, Tringe SG, Bertilsson S, Moran MA, Shade A, Newton RJ, McMahon KD, Malmstrom RR. 2016. Genome-wide selective sweeps and gene-specific sweeps in natural bacterial populations. ISME J 10:1589–1601. http://dx.doi.org/10.1038/ismej.2015.241. [PubMed]
189. Fuxelius HH, Darby A, Min CK, Cho NH, Andersson SG. 2007. The genomic and metabolic diversity of Rickettsia. Res Microbiol 158:745–753. http://dx.doi.org/10.1016/j.resmic.2007.09.008. [PubMed]
190. Papke RT, Zhaxybayeva O, Feil EJ, Sommerfeld K, Muise D, Doolittle WF. 2007. Searching for species in haloarchaea. Proc Natl Acad Sci U S A 104:14092–14097. http://dx.doi.org/10.1073/pnas.0706358104. [PubMed]
191. Guttman DS, Dykhuizen DE. 1994. Detecting selective sweeps in naturally occurring Escherichia coli. Genetics 138:993–1003. [PubMed]
192. Kopac SM, Cohan FM. 2012. Comment on “Population genomics of early events in the ecological differentiation of bacteria”. Science 336:48–51. http://comments.sciencemag.org/content/10.1126/science.1218198#comments. [PubMed]
193. Cohan FM. 2005. Periodic selection and ecological diversity in bacteria, p 78–93. In Nurminsky D (ed), Selective Sweep. Landes Bioscience, Georgetown, TX. http://dx.doi.org/10.1007/0-387-27651-3_7.
194. Majewski J, Cohan FM. 1999. Adapt globally, act locally: the effect of selective sweeps on bacterial sequence diversity. Genetics 152:1459–1474. [PubMed]
195. Takeuchi N, Cordero OX, Koonin EV, Kaneko K. 2015. Gene-specific selective sweeps in bacteria and archaea caused by negative frequency-dependent selection. BMC Biol 13:20. http://dx.doi.org/10.1186/s12915-015-0131-7. [PubMed]
196. Roy K, Hunt G, Jablonski D. 2009. Phylogenetic conservatism of extinctions in marine bivalves. Science 325:733–737. http://dx.doi.org/10.1126/science.1173073. [PubMed]
197. Dunn RR, Harris NC, Colwell RK, Koh LP, Sodhi NS. 2009. The sixth mass coextinction: are most endangered species parasites and mutualists? Proc Biol Sci 276:3037–3045. http://dx.doi.org/10.1098/rspb.2009.0413. [PubMed]
198. Jorth P, Staudinger BJ, Wu X, Hisert KB, Hayden H, Garudathri J, Harding CL, Radey MC, Rezayat A, Bautista G, Berrington WR, Goddard AF, Zheng C, Angermeyer A, Brittnacher MJ, Kitzman J, Shendure J, Fligner CL, Mittler J, Aitken ML, Manoil C, Bruce JE, Yahr TL, Singh PK. 2015. Regional isolation drives bacterial diversification within cystic fibrosis lungs. Cell Host Microbe 18:307–319. http://dx.doi.org/10.1016/j.chom.2015.07.006. [PubMed]
199. Oliver A, Cantón R, Campo P, Baquero F, Blázquez J. 2000. High frequency of hypermutable Pseudomonas aeruginosa in cystic fibrosis lung infection. Science 288:1251–1254. http://dx.doi.org/10.1126/science.288.5469.1251. [PubMed]
200. López-Collazo E, Jurado T, de Dios Caballero J, Pérez-Vázquez M, Vindel A, Hernández-Jiménez E, Tamames J, Cubillos-Zapata C, Manrique M, Tobes R, Máiz L, Cantón R, Baquero F, Del Campo R. 2015. In vivo attenuation and genetic evolution of a ST247-SCCmecI MRSA clone after 13 years of pathogenic bronchopulmonary colonization in a patient with cystic fibrosis: implications of the innate immune response. Mucosal Immunol 8:362–371. http://dx.doi.org/10.1038/mi.2014.73. [PubMed]
201. Hoboth C, Hoffmann R, Eichner A, Henke C, Schmoldt S, Imhof A, Heesemann J, Hogardt M. 2009. Dynamics of adaptive microevolution of hypermutable Pseudomonas aeruginosa during chronic pulmonary infection in patients with cystic fibrosis. J Infect Dis 200:118–130. http://dx.doi.org/10.1086/599360. [PubMed]
202. Warner DF, Koch A, Mizrahi V. 2015. Diversity and disease pathogenesis in Mycobacterium tuberculosis. Trends Microbiol 23:14–21. http://dx.doi.org/10.1016/j.tim.2014.10.005. [PubMed]
203. Ebrahimi-Rad M, Bifani P, Martin C, Kremer K, Samper S, Rauzier J, Kreiswirth B, Blazquez J, Jouan M, van Soolingen D, Gicquel B. 2003. Mutations in putative mutator genes of Mycobacterium tuberculosis strains of the W-Beijing family. Emerg Infect Dis 9:838–845. http://dx.doi.org/10.3201/eid0907.020803.
204. Cohan FM, Perry EB. 2007. A systematics for discovering the fundamental units of bacterial diversity. Curr Biol 17:R373–R386. http://dx.doi.org/10.1016/j.cub.2007.03.032. [PubMed]
205. Achtman M, Wagner M. 2008. Microbial diversity and the genetic nature of microbial species. Nat Rev Microbiol 6:431–440. http://dx.doi.org/10.1038/nrmicro1872. [PubMed]
206. Baldan R, Testa F, Lorè NI, Bragonzi A, Cichero P, Ossi C, Biancardi A, Nizzero P, Moro M, Cirillo DM. 2012. Factors contributing to epidemic MRSA clones replacement in a hospital setting. PLoS One 7:e43153. http://dx.doi.org/10.1371/journal.pone.0043153. [PubMed]
207. Remonsellez F, Galleguillos F, Moreno-Paz M, Parro V, Acosta M, Demergasso C. 2009. Dynamic of active microorganisms inhabiting a bioleaching industrial heap of low-grade copper sulfide ore monitored by real-time PCR and oligonucleotide prokaryotic acidophile microarray. Microb Biotechnol 2:613–624. http://dx.doi.org/10.1111/j.1751-7915.2009.00112.x. [PubMed]
microbiolspec.MTBP-0014-2016.citations
cm/5/5
content/journal/microbiolspec/10.1128/microbiolspec.MTBP-0014-2016
Loading

Citations loading...

Loading

Article metrics loading...

/content/journal/microbiolspec/10.1128/microbiolspec.MTBP-0014-2016
2017-10-12
2017-12-12

Abstract:

Any two lineages, no matter how distant they are now, began their divergence as one population splitting into two lineages that could coexist indefinitely. The rate of origin of higher-level taxa is therefore the product of the rate of speciation times the probability that two new species coexist long enough to reach a particular level of divergence. Here I have explored these two parameters of disparification in bacteria. Owing to low recombination rates, sexual isolation is not a necessary milestone of bacterial speciation. Rather, irreversible and indefinite divergence begins with ecological diversification, that is, transmission of a bacterial lineage to a new ecological niche, possibly to a new microhabitat but at least to new resources. Several algorithms use sequence data from a taxon of focus to identify phylogenetic groups likely to bear the dynamic properties of species. Identifying these newly divergent lineages allows us to characterize the genetic bases of speciation, as well as the ecological dimensions upon which new species diverge. Speciation appears to be least frequent when a given lineage has few new resources it can adopt, as exemplified by photoautotrophs, C1 heterotrophs, and obligately intracellular pathogens; speciation is likely most rapid for generalist heterotrophs. The genetic basis of ecological divergence may determine whether ecological divergence is irreversible and whether lineages will diverge indefinitely into the future. Long-term coexistence is most likely when newly divergent lineages utilize at least some resources not shared with the other and when the resources themselves will coexist into the remote future.

Highlighted Text: Show | Hide
Loading full text...

Full text loading...

Figures

Image of FIGURE 1
FIGURE 1

The ecological divergence between ecotypes is sufficient for them to coexist into the indefinite future. Ecotypes are defined so that any ecological differences among lineages within ecotypes are not sufficient to allow them to coexist indefinitely. We may thus refer to ecologically distinct lineages within ecotypes as “ephemeral ecotypes.” The different styles of dashed lines within ecotype 1 refer to different ephemeral ecotypes; note that only one of these lineages persists to the present. The different weights of solid lines represent different ephemeral ecotypes within ecotype 2 ( 52 ). Used with permission from Elsevier.

Source: microbiolspec October 2017 vol. 5 no. 5 doi:10.1128/microbiolspec.MTBP-0014-2016
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 2
FIGURE 2

Improvement of an ecological function by mutation or HGT (indicated by the enlarged triangle) can lead to a periodic selection event (A) or an ecotype formation event (B or C). Each individual is represented by a circle, and each individual’s degree of adaptation to two resources (or conditions) is indicated by the sizes of the square and triangle, respectively. In panel A, adaptation to the triangle resource or condition is increased in one individual (indicated by increased triangle size), and the resultant strain is now able to outcompete the membership of its ecotype by virtue of its more generalist ecology. In panel B, the increase in adaptation to the triangle resource intrinsically decreases the adaptation to the square resource. Thus, increase in one ecological capability comes at the expense of a preexisting capability. In this case, acquisition of the new function leads to a new ecotype, which can coexist with the preexisting ecotype. This has been seen repeatedly in experimental populations of that primarily used glucose for carbon; a mutation to utilize secreted acetate created a new ecotype because the acetate-utilizing bacteria were less able to utilize glucose ( 39 , 47 ). An alternative possibility is shown in panel C, where there is no intrinsic trade-off to the new adaptation yet a new ecotype can form. Here the new genotype invades a new habitat where the new adaptation is selected for. If the “square” adaptation is not utilized in one habitat and the “triangle” adaptation is not utilized in the other, under the Black Queen hypothesis, the unnecessary adaptations may be lost ( 147 ). This will make each ecotype the superior competitor in its own microhabitat. Adapted with permission from reference 47 .

Source: microbiolspec October 2017 vol. 5 no. 5 doi:10.1128/microbiolspec.MTBP-0014-2016
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 3
FIGURE 3

Ecotypes are represented by different colors, periodic selection events are indicated by asterisks, and extinct lineages are represented by dashed lines. The letters at the top represent the resources that each group of organisms can utilize. In cases where ecotypes utilize the same set of resources but in different proportions, the predominant resource of each ecotype is noted by a capital letter. (A) The stable ecotype model. In the stable ecotype model, each ecotype endures many periodic selection events during its long lifetime. The stable ecotype model generally yields a one-to-one correspondence between ecotypes and sequence clusters because ecotypes are formed at a low rate. The ecotypes are able to coexist indefinitely because each has a resource not shared with the others. (B) The speedy speciation model. This model is much like the stable ecotype model, except that speciation occurs so rapidly that most newly divergent ecotypes cannot be detected as sequence clusters in multilocus analyses. (C) The nano-niche model of bacterial speciation. In the figure, there are three nano-niche ecotypes that use the same set of resources but in different proportions (noted by Abc, aBc, and abC). Each nano-niche ecotype can coexist with the other two because they have partitioned their resources, at least quantitatively. However, because the ecotypes share all their resources, each is vulnerable to a possible speciation-quashing mutation that may arise in the other ecotypes. (D) The species-less model. Here the diversity within an ecotype is limited not by periodic selection but instead by the short time from the ecotype’s invention as a single mutant until its extinction. The origination and extinction of each ecotype is indicated by and , respectively. In the absence of periodic selection, each extant ecotype that has given rise to another ecotype is a paraphyletic group, and each recent ecotype that has not yet given rise to another ecotype is monophyletic ( 81 ). (E) Recurrent niche invasion model. Here a lineage may move, frequently and recurrently, from one ecotype to another, usually by acquisition and loss of niche-determining plasmids. Red lines indicate the times in which a lineage is in the plasmid-containing ecotype; blue lines indicate the times when the lineage is in the plasmid-absent ecotype. Periodic selection events within one ecotype extinguish only the lineages of the same ecotype. For example, in the most ancient periodic selection event shown, which is in the plasmid-absent (blue) ecotype, only the lineages missing the plasmid at the time of periodic selection are extinguished, while the plasmid-containing lineages (red) persist. Ecotypes determined by a plasmid are not likely to be discoverable as sequence clusters. Reproduced from reference ( 81 ).

Source: microbiolspec October 2017 vol. 5 no. 5 doi:10.1128/microbiolspec.MTBP-0014-2016
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 4
FIGURE 4

Circles represent different genotypes, and asterisks represent adaptive mutations. (A) Ecotype formation event. A mutation or a recombination event allows the cell to occupy a new ecological niche, founding a new ecotype. A new ecotype can be formed only if the founding organism has undergone a fitness trade-off, whereby it cannot compete successfully with the parental ecotype in the old. (B) Periodic selection event. A periodic selection mutation improves the fitness of an individual such that the mutant and its descendants outcompete all other cells within the ecotype; these mutations do not affect the diversity within other ecotypes because ecological differences between ecotypes prevent direct competition. Periodic selection leads to the distinctness of ecotypes by purging the divergence within but not between ecotypes. Reproduced with permission from reference 193 .

Source: microbiolspec October 2017 vol. 5 no. 5 doi:10.1128/microbiolspec.MTBP-0014-2016
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 5
FIGURE 5

Each row of panels represents a different model of sweep within a metagenome cluster: (A to B) a genome-wide sweep, where the metagenome cluster is populated by only a single ecotype, and where recombination is rare enough to allow a genome-wide sweep within an ecotype ( 28 ); (C to D) a narrow sweep (homogenizing only the chromosomal region near the adaptive mutation), where again the metagenome cluster is populated by a single ecotype, but here recombination (indicated by purple arrows) is frequent enough to prevent a genome-wide sweep within an ecotype (model favored by Bendall et al. [ 188 ]); and (E to H) a narrow sweep, where the metagenome cluster is populated by many ecotypes (in this case, three), and recombination is rare enough to allow genome-wide sweeps within an ecotype but frequent enough to allow an adaptive mutation to recombine (it need happen only once!) between one ecotype and another ( 46 ). In each row, the wide horizontal arrows represent the course of time. In each panel, the rectangle represents one metagenome cluster and each circle represents a single organism. The asterisk represents an adaptive mutation, which allows its carrier to outcompete other organisms in the same ecotype but not organisms from other ecotypes. In panels A to D, the metagenome cluster is ecologically homogeneous, and in panels E to H, the metagenome cluster is ecologically heterogeneous and represents three ecotypes, separated by the vertical dashed lines; the different ecotypes are coded by blue, green, and red. The sequence diversity within an ecotype is represented by different shades of the ecotype color and by different styles of line (dotted, dashed, and solid). In the case of low recombination rates (A to B and E to H), the adaptive mutation causes a genome-wide sweep within the ecotype containing the mutation. In panels E to H, the adaptive mutation is potentially beneficial in different ecotypes and can transfer on a short chromosomal segment to another ecotype, where it precipitates a new genome-wide sweep within its new ecotype. Reproduced with permission from reference ( 156 ).

Source: microbiolspec October 2017 vol. 5 no. 5 doi:10.1128/microbiolspec.MTBP-0014-2016
Permissions and Reprints Request Permissions
Download as Powerpoint

Supplemental Material

No supplementary material available for this content.

This is a required field
Please enter a valid email address
Please check the format of the address you have entered.
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error