Explaining microbial genomic diversity in light of evolutionary ecology (original) (raw)

• Gevers, D. et al. Opinion: re-evaluating prokaryotic species. Nature Rev. Microbiol. 3, 733–739 (2005).
  Article CAS Google Scholar
• Koeppel, A. et al. Identifying the fundamental units of bacterial diversity: a paradigm shift to incorporate ecology into bacterial systematics. Proc. Natl Acad. Sci. USA 105, 2504–2509 (2008).
  Article CAS PubMed PubMed Central Google Scholar
• Achtman, M. & Wagner, M. Microbial diversity and the genetic nature of microbial species. Nature Rev. Microbiol. 6, 431–440 (2008).
  Article CAS Google Scholar
• Fraser, C., Alm, E. J., Polz, M. F., Spratt, B. G. & Hanage, W. P. The bacterial species challenge: making sense of genetic and ecological diversity. Science 323, 741–746 (2009).
  Article CAS PubMed Google Scholar
• Polz, M. F., Alm, E. J. & Hanage, W. P. Horizontal gene transfer and the evolution of bacterial and archaeal population structure. Trends Genet. 29, 170–175 (2013).
  Article CAS PubMed PubMed Central Google Scholar
• Polz, M. F., Hunt, D. E., Preheim, S. P. & Weinreich, D. M. Patterns and mechanisms of genetic and phenotypic differentiation in marine microbes. Phil. Trans. R. Soc. 361, 2009–2021 (2006).
  Article Google Scholar
• Johnson, Z. I. et al. Niche partitioning among Prochlorococcus ecotypes along ocean-scale environmental gradients. Science 311, 1737–1740 (2006).
  Article CAS PubMed Google Scholar
• Hunt, D. E. et al. Resource partitioning and sympatric differentiation among closely related bacterioplankton. Science 320, 1081–1085 (2008). This study shows that the population structure of co-existing Vibrionaceae can be identified using co-clustering of phylogenetic and ecological signals.
  Article CAS PubMed Google Scholar
• Connor, N. et al. Ecology of speciation in the genus Bacillus. Appl. Environ. Microbiol. 76, 1349–1358 (2010).
  Article CAS PubMed PubMed Central Google Scholar
• Whitaker, R. J., Grogan, D. W. & Taylor, J. W. Recombination shapes the natural population structure of the hyperthermophilic archaeon Sulfolobus islandicus. Mol. Biol. Evol. 22, 2354–2361 (2005).
  Article CAS PubMed Google Scholar
• Denef, V. J., Mueller, R. S. & Banfield, J. F. AMD biofilms: using model communities to study microbial evolution and ecological complexity in nature. ISME J. 4, 599–610 (2010).
  Article PubMed Google Scholar
• Oakley, B. B., Carbonero, F., van der Gast, C. J., Hawkins, R. J. & Purdy, K. J. Evolutionary divergence and biogeography of sympatric niche-differentiated bacterial populations. ISME J. 4, 488–497 (2010).
  Article PubMed Google Scholar
• Hahn, M. W. et al. The passive yet successful way of planktonic life: genomic and experimental analysis of the ecology of a free-living polynucleobacter population. PLoS ONE 7, e32772 (2012).
  Article CAS PubMed PubMed Central Google Scholar
• Shapiro, B. J. et al. Population genomics of early events in the ecological differentiation of bacteria. Science 336, 48–51 (2012). This study shows that natural populations of Vibrio cyclitrophicus are highly recombinant and that ecological differentiation between nascent populations is accompanied not by clonal expansions but by the emergence of recombination boundaries owing to microgeographic separation.
  Article CAS PubMed PubMed Central Google Scholar
• Simmons, S. L. et al. Population genomic analysis of strain variation in Leptospirillum group II bacteria involved in acid mine drainage formation. PLoS Biol. 6, e177 (2008).
  Article PubMed PubMed Central CAS Google Scholar
• Cadillo-Quiroz, H. et al. Patterns of gene flow define species of thermophilic archaea. PLoS Biol. 10, e1001265 (2012). This study documents ongoing speciation in two populations of the archaeon Sulpholobus islandicus and suggests that recombination between populations has been gradually decreasing over time with no detectable evidence of loss of diversity owing to genome-wide sweeps.
  Article CAS PubMed PubMed Central Google Scholar
• Whitaker, R. J. Allopatric origins of microbial species. Phil. Trans. R. Soc. 361, 1975–1984 (2006).
  Article Google Scholar
• Fraser, C., Hanage, W. P. & Spratt, B. G. Recombination and the nature of bacterial speciation. Science 315, 476–480 (2007).
  Article CAS PubMed PubMed Central Google Scholar
• Cohan, F. M. Towards a conceptual and operational union of bacterial systematics, ecology, and evolution. Phil. Trans. R. Soc. 361, 1985–1996 (2006).
  Article Google Scholar
• Gudelj, I. et al. An integrative approach to understanding microbial diversity: from intracellular mechanisms to community structure. Ecol. Lett. 13, 1073–1084 (2010).
  Article PubMed PubMed Central Google Scholar
• Thompson, J. R. et al. Genotypic diversity within a natural coastal bacterioplankton population. Science 307, 1311–1313 (2005).
  Article CAS PubMed Google Scholar
• Kettler, G. C. et al. Patterns and implications of gene gain and loss in the evolution of Prochlorococcus. PLoS Genet. 3, e231 (2007).
  Article PubMed PubMed Central CAS Google Scholar
• Tettelin, H., Riley, D., Cattuto, C. & Medini, D. Comparative genomics: the bacterial pan-genome. Curr. Opin. Microbiol. 11, 472–477 (2008). This comparative study provides flexible genome statistics from across different taxonomic groups.
  Article CAS PubMed Google Scholar
• Hejnova, J. et al. Characterization of the flexible genome complement of the commensal Escherichia coli strain A0 34/86 (O83: K24: H31). Microbiology 151, 385–398 (2005).
  Article CAS PubMed Google Scholar
• Genung, M. A. et al. Non-additive effects of genotypic diversity increase floral abundance and abundance of floral visitors. PLoS ONE 5, e8711 (2010).
  Article PubMed PubMed Central CAS Google Scholar
• Cook-Patton, S. C., McArt, S. H., Parachnowitsch, A. L., Thaler, J. S. & Agrawal, A. A. A direct comparison of the consequences of plant genotypic and species diversity on communities and ecosystem function. Ecology 92, 915–923 (2011).
  Article PubMed Google Scholar
• Drummond, E. B. M. & Vellend, M. Genotypic diversity effects on the performance of Taraxacum officinale populations increase with time and environmental favorability. PLoS ONE 7, e30314 (2012).
  Article CAS PubMed PubMed Central Google Scholar
• Crutsinger, G. M. et al. Plant genotypic diversity predicts community structure and governs an ecosystem process. Science 313, 966–968 (2006). This study shows the impact of plant genotypic diversity on net primary productivity above ground as well as on the diversity of associated arthropod communities.
  Article CAS PubMed Google Scholar
• Reusch, T. B. H., Ehlers, A., Hämmerli, A. & Worm, B. Ecosystem recovery after climatic extremes enhanced by genotypic diversity. Proc. Natl Acad. Sci. USA 102, 2826–2831 (2005).
  Article CAS PubMed PubMed Central Google Scholar
• Roger, F., Godhe, A. & Gamfeldt, L. Genetic diversity and ecosystem functioning in the face of multiple stressors. PLoS ONE 7, e45007 (2012).
  Article CAS PubMed PubMed Central Google Scholar
• Eisenhauer, N., Scheu, S. & Jousset, A. Bacterial diversity stabilizes community productivity. PLoS ONE 7, e34517 (2012).
  Article CAS PubMed PubMed Central Google Scholar
• Loreau, M. & Hector, A. Partitioning selection and complementarity in biodiversity experiments. Nature 412, 72–76 (2001).
  Article CAS PubMed Google Scholar
• Hughes, A. R. & Stachowicz, J. J. Ecological impacts of genotypic diversity in the clonal seagrass Zostera marina. Ecology 90, 1412–1419 (2009).
  Article PubMed Google Scholar
• Bolnick, D. I. et al. Why intraspecific trait variation matters in community ecology. Trends Ecol. Evol. 26, 183–192 (2011). This theoretical study discusses the fundamental forms by which genotypic diversity within a species can influence ecological function.
  Article PubMed PubMed Central Google Scholar
• Hughes, A. R., Inouye, B. D., Johnson, M. T. J., Underwood, N. & Vellend, M. Ecological consequences of genetic diversity. Ecol. Lett. 11, 609–623 (2008).
  Article PubMed Google Scholar
• Cordero, O. X. & Hogeweg, P. The impact of long-distance horizontal gene transfer on prokaryotic genome size. Proc. Natl Acad. Sci. USA 106, 21748–21753 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• Cordero, O. X. et al. Ecological populations of bacteria act as socially cohesive units of antibiotic production and resistance. Science 337, 1228–1231 (2012). This study shows asymmetry in the intensity of interference competition between and within bacterioplankton populations. The findings reveal that antagonism occurs more often between, rather than within, populations.
  Article CAS PubMed Google Scholar
• Cordero, O. X., Ventouras, L.-A., DeLong, E. F. & Polz, M. F. Public good games drive the evolution of iron-aquisition strategies in natural bacterioplankton populations. Proc. Natl Acad. Sci. USA 109, 20059–20064 (2012). This study shows that the evolution of cheaters explains the intermediate frequency of siderophore-biosynthesis genes in Vibrio spp. populations.
  Article CAS PubMed PubMed Central Google Scholar
• Figge, F. Bio-folio: applying portfolio theory to biodiversity. Biodivers. Conserv. 13, 827–849 (2004).
  Article Google Scholar
• Schindler, D. E. et al. Population diversity and the portfolio effect in an exploited species. Nature 465, 609–612 (2010). This study shows that the portfolio effect stabilizes salmon populations, despite exploitation by fishing.
  Article CAS PubMed Google Scholar
• Galhardo, R. S., Hastings, P. J. & Rosenberg, S. M. Mutation as a stress response and the regulation of evolvability. Crit. Rev. Biochem. Mol. Biol. 42, 399–435 (2007).
  Article CAS PubMed PubMed Central Google Scholar
• Loh, E., Salk, J. J. & Loeb, L. A. Optimization of DNA polymerase mutation rates during bacterial evolution. Proc. Natl Acad. Sci. USA 107, 1154–1159 (2010).
  Article CAS PubMed Google Scholar
• Palmer, K. L. & Gilmore, M. S. Multidrug-resistant enterococci lack CRISPR–Cas. mBio 1, e00227–00210 (2010). This study shows that some enteroccoci have lost CRISPR–Cas-mediated resistance to foreign DNA, which increases evolvability.
  Article PubMed PubMed Central CAS Google Scholar
• Jousset, A., Schulz, W., Scheu, S. & Eisenhauer, N. Intraspecific genotypic richness and relatedness predict the invasibility of microbial communities. ISME J. 5, 1108–1114 (2011).
  Article PubMed PubMed Central Google Scholar
• Coleman, M. L. & Chisholm, S. W. Ecosystem-specific selection pressures revealed through comparative population genomics. Proc. Natl Acad. Sci. USA 107, 18634–18639 (2010).
  Article CAS PubMed PubMed Central Google Scholar
• Hsiao, W. W. L. et al. Evidence of a large novel gene pool associated with prokaryotic genomic islands. PLoS Genet. 1, e62 (2005).
  Article PubMed PubMed Central CAS Google Scholar
• Smillie, C. S. et al. Ecology drives a global network of gene exchange connecting the human microbiome. Nature 480, 241–244 (2011).
  Article CAS PubMed Google Scholar
• Boucher, Y. et al. Local mobile gene pools rapidly cross species boundaries to create endemicity within global Vibrio cholerae populations. mBio 2, e00335–00310 (2011).
  Article PubMed PubMed Central CAS Google Scholar
• Berg, O. G. & Kurland, C. G. Evolution of microbial genomes: sequence acquisition and loss. Mol. Biol. Evol. 19, 2265–2276 (2002).
  Article CAS PubMed Google Scholar
• Rodriguez-Valera, F. et al. Explaining microbial population genomics through phage predation. Nature Rev. Microbiol. 7, 828–836 (2009).
  Article CAS Google Scholar
• Sinervo, B. & Lively, C. M. The rock–paper–scissors game and the evolution of alternative male strategies. Nature 380, 240–243 (1996).
  Article CAS Google Scholar
• Borghans, J. A. M., Beltman, J. B. & De Boer, R. J. MHC polymorphism under host–pathogen coevolution. Immunogenetics 55, 732–739 (2004).
  Article CAS PubMed Google Scholar
• Gigord, L. D., Macnair, M. R. & Smithson, A. Negative frequency-dependent selection maintains a dramatic flower color polymorphism in the rewardless orchid Dactylorhiza sambucina (L.) Soo. Proc. Natl Acad. Sci. USA 98, 6253–6255 (2001).
  Article CAS PubMed PubMed Central Google Scholar
• Fitzpatrick, B. M., Shook, K. & Izally, R. Frequency-dependent selection by wild birds promotes polymorphism in model salamanders. BMC Ecol. 9, 12 (2009).
  Article PubMed PubMed Central Google Scholar
• Coleman, M. L. et al. Genomic islands and the ecology and evolution of Prochlorococcus. Science 311, 1768–1770 (2006). This study shows that hypervariable regions in the genome (known as genomic islands) are characteristic of an abundant marine cyanobacterial clade.
  Article CAS PubMed Google Scholar
• Wildschutte, H., Preheim, S. P., Hernandez, Y. & Polz, M. F. O-antigen diversity and lateral transfer of the wbe region among Vibrio splendidus isolates. Env. Microbiol. 12, 2977–2987 (2010).
  Article CAS Google Scholar
• Wildschutte, H., Wolfe, D. M., Tamewitz, A. & Lawrence, J. G. Protozoan predation, diversifying selection, and the evolution of antigenic diversity in Salmonella. Proc. Natl Acad. Sci. USA 101, 10644–10649 (2004).
  Article CAS PubMed PubMed Central Google Scholar
• Needham, B. D. & Trent, M. S. Fortifying the barrier: the impact of lipid A remodelling on bacterial pathogenesis. Nature Rev. Microbiol. 11, 467–481 (2013).
  Article CAS Google Scholar
• Van Elsas, J. D. & Bailey, M. J. The ecology of transfer of mobile genetic elements. FEMS Microbiol. Ecol. 42, 187–197 (2002).
  Article CAS PubMed Google Scholar
• Nakamura, Y., Itoh, T., Matsuda, H. & Gojobori, T. Biased biological functions of horizontally transferred genes in prokaryotic genomes. Nature Genet. 36, 760–766 (2004).
  Article CAS PubMed Google Scholar
• Ulrich, L. E., Koonin, E. V. & Zhulin, I. B. One-component systems dominate signal transduction in prokaryotes. Trends Microbiol. 13, 52–56 (2005).
  Article CAS PubMed PubMed Central Google Scholar
• Lang, G. I. et al. Pervasive genetic hitchhiking and clonal interference in forty evolving yeast populations. Nature 500, 571–574 (2013).
  Article CAS PubMed PubMed Central Google Scholar
• Lee, M.-C. & Marx, C. J. Synchronous waves of failed soft sweeps in the laboratory: remarkably rampant clonal interference of alleles at a single locus. Genetics 193, 943–952 (2013).
  Article CAS PubMed PubMed Central Google Scholar
• Winter, C., Bouvier, T., Weinbauer, M. G. & Thingstad, T. F. Trade-offs between competition and defense specialists among unicellular planktonic organisms: the “killing the winner” hypothesis revisited. Microbiol. Mol. Biol. Rev. 74, 42–57 (2010).
  Article CAS PubMed PubMed Central Google Scholar
• Buckling, A. & Rainey, P. B. Antagonistic coevolution between a bacterium and a bacteriophage. Proc. Biol. Sci. 269, 931–936 (2002).
  Article PubMed PubMed Central Google Scholar
• Cuadros-Orellana, S. et al. Genomic plasticity in prokaryotes: the case of the square haloarchaeon. ISME J. 1, 235–245 (2007).
  Article CAS PubMed Google Scholar
• Schaffer, W. M. & Rosenzweig, M. L. Homage to the red queen. I. Coevolution of predators and their victims. Theor. Popul. Biol. 14, 135–157 (1978).
  Article CAS PubMed Google Scholar
• Archetti, M. & Scheuring, I. Coexistence of cooperation and defection in public goods games. Evolution 65, 1140–1148 (2011).
  Article PubMed Google Scholar
• Damore, J. A. & Gore, J. Understanding microbial cooperation. J. Theor. Biol. 299, 31–41 (2012).
  Article PubMed Google Scholar
• Winkelmann, G. Microbial siderophore-mediated transport. Biochem. Soc. Trans. 30, 691–696 (2003).
  Article Google Scholar
• Johnson, J. R., Moseley, S. L., Roberts, P. L. & Stamm, W. E. Aerobactin and other virulence factor genes among strains of Escherichia coli causing urosepsis: association with patient characteristics. Infect. Immun. 56, 405–412 (1988).
  Article CAS PubMed PubMed Central Google Scholar
• Tanabe, T. et al. Identification and characterization of genes required for biosynthesis and transport of the siderophore vibrioferrin in Vibrio parahaemolyticus. J. Bacteriol. 185, 6938–6949 (2003).
  Article CAS PubMed PubMed Central Google Scholar
• West, S. A. & Buckling, A. Cooperation, virulence and siderophore production in bacterial parasites. Proc. Biol. Sci. 270, 37–44 (2003).
  Article PubMed PubMed Central Google Scholar
• D'Onofrio, A. et al. Siderophores from neighboring organisms promote the growth of uncultured bacteria. Chem. Biol. 17, 254–264 (2010).
  Article CAS PubMed PubMed Central Google Scholar
• Griffin, A. S., West, S. A. & Buckling, A. Cooperation and competition in pathogenic bacteria. Nature 430, 1024–1027 (2004).
  Article CAS PubMed Google Scholar
• Majewski, J. & Cohan, F. M. DNA sequence similarity requirements for interspecific recombination in Bacillus. Genetics 153, 1525–1533 (1999).
  Article CAS PubMed PubMed Central Google Scholar
• Koornhof, H. J., Keddy, K. & McGee, L. Clonal expansion of bacterial pathogens across the world. J. Travel Med. 8, 29–40 (2001).
  Article CAS PubMed Google Scholar
• Vos, M. & Velicer, G. J. Social conflict in centimeter- and global-scale populations of the bacterium Myxococcus xanthus. Curr. Biol. 19, 1763–1767 (2009). This study shows that genotypes of Myxococcus xanthus engage in social interactions that depend on fine-scale population structure.
  Article CAS PubMed PubMed Central Google Scholar
• O'Connor, K. A. & Zusman, D. R. Development in Myxococcus xanthus involves differentiation into two cell types, peripheral rods and spores. J. Bacteriol. 173, 3318–3333 (1991).
  Article CAS PubMed PubMed Central Google Scholar
• Stefanic, P. et al. The quorum sensing diversity within and between ecotypes of Bacillus subtilis. Environ. Microbiol. 14, 1378–1389 (2012). This study shows that signalling is more often successful within populations than between populations of Bacillus subtilis.
  Article CAS PubMed Google Scholar
• Tran, L.-S. P., Nagai, T. & Itoh, Y. Divergent structure of the ComQXPA quorum-sensing components: molecular basis of strain-specific communication mechanism in Bacillus subtilis. Mol. Microbiol. 37, 1159–1171 (2000).
  Article CAS PubMed Google Scholar
• Hawlena, H., Bashey, F. & Lively, C. M. Bacteriocin-mediated interactions within and between coexisting species. Ecol. Evol. 2, 2521–2526 (2012).
  Article PubMed PubMed Central Google Scholar
• Riley, M. A. & Wertz, J. E. Bacteriocin diversity: ecological and evolutionary perspectives. Biochimie 84, 357–364 (2002).
  Article CAS PubMed Google Scholar
• Preheim, S. P. et al. Metapopulation structure of Vibrionaceae among coastal marine invertebrates. Environ. Microbiol. 13, 265–275 (2011).
  Article CAS PubMed Google Scholar
• Pérez-Gutiérrez, R.-A. et al. Antagonism influences assembly of a Bacillus guild in a local community and is depicted as a food-chain network. ISME J. 7, 487–497 (2013).
  Article PubMed CAS Google Scholar
• Morris, J. J., Lenski, R. E. & Zinser, E. R. The Black Queen hypothesis: evolution of dependencies through adaptive gene loss. mBio 3, e00036–00012 (2012).
  Article PubMed PubMed Central Google Scholar
• Doolittle, W. F. & Papke, R. T. Genomics and the bacterial species problem. Genome Biol. 7, 116 (2006).
  Article PubMed PubMed Central CAS Google Scholar
• Hanage, W. P., Spratt, B. G., Turner, K. M. E. & Fraser, C. Modelling bacterial speciation. Phil. Trans. R. Soc. 361, 2039–2044 (2006).
  Article Google Scholar
• Ivars-Martinez, E. et al. Comparative genomics of two ecotypes of the marine planktonic copiotroph Alteromonas macleodii suggests alternative lifestyles associated with different kinds of particulate organic matter. ISME J. 2, 1194–1212 (2008).
  Article CAS PubMed Google Scholar
• Croucher, N. J. et al. Rapid pneumococcal evolution in response to clinical interventions. Science 331, 430–434 (2011).
  Article CAS PubMed PubMed Central Google Scholar
• Kurland, C. G., Canback, B. & Berg, O. G. Horizontal gene transfer: a critical view. Proc. Natl Acad. Sci. USA 100, 9658–9662 (2003).
  Article CAS PubMed PubMed Central Google Scholar
• Majewski, J. & Cohan, F. M. Adapt globally, act locally: the effect of selective sweeps on bacterial sequence diversity. Genetics 152, 1459–1474 (1999).
  Article CAS PubMed PubMed Central Google Scholar
• Shapiro, B. J., David, L. A., Friedman, J. & Alm, E. J. Looking for Darwin's footprints in the microbial world. Trends Microbiol. 17, 196–204 (2009).
  Article CAS PubMed Google Scholar
• Hanage, W. P., Fraser, C. & Spratt, B. G. Fuzzy species among recombinogenic bacteria. BMC Biol. 3, 6 (2005).
  Article PubMed PubMed Central CAS Google Scholar
• Guttman, D. S. & Dykhuizen, D. E. Detecting selective sweeps in naturally occurring Escherichia coli. Genetics 138, 993–1003 (1994).
  Article CAS PubMed PubMed Central Google Scholar
• Vos, M. & Didelot, X. A comparison of homologous recombination rates in bacteria and archaea. ISME J. 3, 199–208 (2009).
  Article CAS PubMed Google Scholar
• Azam, F. & Malfatti, F. Microbial structuring of marine ecosystems. Nature Rev. Microbiol. 5, 782–791 (2007).
  Article CAS Google Scholar
• Stocker, R. Marine microbes see a sea of gradients. Science 338, 628–633 (2012).
  Article CAS PubMed Google Scholar
• Burd, A. B. & Jackson, G. A. Particle aggregation. Ann. Rev. Mar. Sci. 1, 65–90 (2009).
  Article PubMed Google Scholar
• Azam, F. & Long, R. A. Sea snow microcosms. Nature 414, 497–498 (2001).
  Article CAS Google Scholar
• Simon, M., Grossart, H. P., Schweitzer, B. & Ploug, H. Microbial ecology of organic aggregates in aquatic ecosystems. Aquat. Microb. Ecol. 28, 175–211 (2002).
  Article Google Scholar
• Grossart, H.-P., Kiørboe, T., Tang, K. & Ploug, H. Bacterial colonization of particles: growth and interactions. Appl. Environ. Microbiol. 69, 3500–3509 (2003).
  Article CAS PubMed PubMed Central Google Scholar
• Labrie, S. J., Samson, J. E. & Moineau, S. Bacteriophage resistance mechanisms. Nature Rev. Microbiol. 8, 317–327 (2010).
  Article CAS Google Scholar