Rapid Evolution of Simple Microbial Communities in the Laboratory

  • Margie Kinnersley
  • Jared W. Wenger
  • Gavin Sherlock
  • Frank R. Rosenzweig
Chapter

Abstract

Classical models predict that asexual populations evolve in simple unstructured environments by clonal replacement, yet laboratory evolutionary studies have uncovered persistent polymorphism, driven either by frequency-dependent selection or mutualistic interactions. We have studied the evolution of microbes in simple unstructured environments as a way to illuminate the evolution of biodiversity. We sought to understand how complexity arises in an Escherichia coli population founded by a single clone and propagated under glucose limitation for >770 generations. When coevolved clones are cultured separately, their transcriptional profiles differ from their common ancestor in ways that are consistent with our understanding of how E. coli adapts to glucose limitation. A majority of the 180 differentially expressed genes shared between coevolved clones is controlled by the global regulators RpoS, Crp, and CpxR. Clone-specific expression differences include upregulation of genes whose products scavenge overflow metabolites such as acetate, enabling cross-feeding. Unexpectedly, we find that when coevolved clones are cultured together, the community expression profile more closely resembles that of minority clones cultured in isolation rather than that of the majority clone cultured in isolation. We attribute this to habitat modification and regulatory feedback arising from consumption of overflow metabolites by niche specialists. Targeted and whole-genome sequencing reveal acs, glpR, and rpoS mutations in the founder that likely predispose evolution of niche specialists. Several mutations bringing about specialization are compensatory rather than gain-of-function. Biocomplexity can therefore arise on a single limiting resource if consumption of that resource results in the creation of others that are differentially accessible to adaptive mutants. These observations highlight the interplay of founder genotype, biotic environment, regulatory mutations, and compensatory changes in the adaptive evolution of asexual species and somatic cells.

Keywords

Phosphorus Glycerol Lactate Recombination Electrophoresis 

Notes

Acknowledgments

The authors gratefully acknowledge fruitful discussions with Dan Kvitek, Evgueny Kroll, and Carla Boulianne-Larsen, and financial support from NIH-NHGRI (HG003328-01) and NASA (NNX07AJ28G) to GS and FR, respectively.

References

  1. Atwood KC, Schneider LK, Ryan FJ (1951) Periodic selection in Escherichia coli. Proc Natl Acad Sci USA 37:146–155PubMedCrossRefGoogle Scholar
  2. 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 176:441–453PubMedCrossRefGoogle Scholar
  3. Boucher D (1985) The biology of mutualism: ecology and evolution. Croom Helm, LondonGoogle Scholar
  4. Carroll SB (2005) Evolution at two levels: on genes and form. PLoS Biol 3:e245PubMedCrossRefGoogle Scholar
  5. de Visser JAGM, Rozen DE (2006) Clonal interference and the periodic selection of new beneficial mutations in Escherichia coli. Genetics 172:2093–2100PubMedCrossRefGoogle Scholar
  6. Denver DR, Morris K, Streelman JT, Kim SK, Lynch M, Thomas WK (2005) The transcriptional consequences of mutation and natural selection in Caenorhabditis elegans. Nat Genet 37:544–548PubMedCrossRefGoogle Scholar
  7. Dobzhansky T, Spassky B (1947) Evolutionary changes in laboratory cultures of Drosophila pseudoobscura. Evolution 1:191–216CrossRefGoogle Scholar
  8. Dobzhansky T, Wright S (1947) Genetics of natural populations. Xv. rate of diffusion of a mutant gene through a population of Drosophila pseudoobscura. Genetics 32:303–324Google Scholar
  9. Dykhuizen DE, Dean AM (1994) Predicted fitness changes along an environmental gradient. Evol Ecol 8:541CrossRefGoogle Scholar
  10. Estes S, Lynch M (2003) Rapid fitness recovery in mutationally degraded lines of Caenorhabditis elegans. Evolution Int J Org Evolution 57:1022–1030Google Scholar
  11. Estes S, Phillips PC, Denver DR, Thomas WK, Lynch M (2004) Mutation accumulation in populations of varying size: the distribution of mutational effects for fitness correlates in Caenorhabditis elegans. Genetics 166:1269–1279PubMedCrossRefGoogle Scholar
  12. Friesen ML, Saxer G, Travisano M, Doebeli M (2004) Experimental evidence for sympatric ecological diversification due to frequency-dependent competition in Escherichia coli. Evolution Int J Org Evolution 58:245–260Google Scholar
  13. Gause GF (1934) Experimental analysis of Vito Volterra’s mathematical theory of the struggle for existence. Science 79:16–17PubMedCrossRefGoogle Scholar
  14. Gerrish PJ, Lenski RE (1998) The fate of competing beneficial mutations in an asexual population. Genetica 102–103:127–144PubMedCrossRefGoogle Scholar
  15. Hardin G (1960) The competitive exclusion principle. Science 131:1292–1297PubMedCrossRefGoogle Scholar
  16. Helling RB, Vargas CN, Adams J (1987) Evolution of Escherichia coli during growth in a constant environment. Genetics 116:349–358PubMedGoogle Scholar
  17. Hoekstra HE, Coyne JA (2007) The locus of evolution: evo devo and the genetics of adaptation. Evolution Int J Org Evolution 61:995–1016CrossRefGoogle Scholar
  18. Jacob F (1977) Evolution and tinkering. Science 196:1161–1166PubMedCrossRefGoogle Scholar
  19. Kao KC, Sherlock G (2008) Molecular characterization of clonal interference during adaptive evolution in asexual populations of Saccharomyces cerevisiae. Nat Genet 40:1499–1504PubMedCrossRefGoogle Scholar
  20. Kinnersley MA, Holben WE, Rosenzweig F (2009) E unibus plurum: genomic analysis of an experimentally evolved polymorphism in Escherichia coli. PLoS Genet 5:e1000713PubMedCrossRefGoogle Scholar
  21. Kvitek DJ, Sherlock G (2011) Reciprocal sign epistasis between frequently experimentally evolved adaptive mutations causes a rugged fitness landscape. PloS Genetics 2011 April; 7(4): e100256 PMCID: PMC3084205Google Scholar
  22. Kubitschek HE (1970) Introduction to research with continuous cultures. Prentice-Hall, Englewood CliffsGoogle Scholar
  23. Kurlandzka A, Rosenzweig RF, Adams J (1991) Identification of adaptive changes in an evolving population of Escherichia coli: the role of changes with regulatory and highly pleiotropic effects. Mol Biol Evol 8:261–281PubMedGoogle Scholar
  24. Le Gac M, Brazas MD, Bertrand M, Tyerman JG, Spencer CC, Hancock REW, Doebeli M (2008) Metabolic changes associated with adaptive diversification in Escherichia coli. Genetics 178:1049–1060PubMedCrossRefGoogle Scholar
  25. Monod J (1942) Recherche sur la croissance des cultures bactériennes. Hermann et Cie, ParisGoogle Scholar
  26. Muller HJ (1932) Some genetic aspects of sex. Am Nat 66:118–138CrossRefGoogle Scholar
  27. Novick A, Szilard L (1950) Experiments with the chemostat on spontaneous mutations of bacteria. Proc Natl Acad Sci USA 36:708–719PubMedCrossRefGoogle Scholar
  28. Rainey PB, Travisano M (1998) Adaptive radiation in a heterogeneous environment. Nature 394:69–72PubMedCrossRefGoogle Scholar
  29. Rainey PB, Buckling A, Kassen R, Travisano M (2000) The emergence and maintenance of diversity: insights from experimental bacterial populations. Trends Ecol Evol 15:243–247PubMedCrossRefGoogle Scholar
  30. Rosenzweig F, Sherlock G (2009) Through a glass, clearly: experimental evolution as a window on genome evolution. In: Garland T, Rose M (eds) Experimental evolution: applications and methods. University of California Press, Berkeley, pp 353–388Google Scholar
  31. Rosenzweig RF, Sharp RR, Treves DS, Adams J (1994) Microbial evolution in a simple unstructured environment: genetic differentiation in Escherichia coli. Genetics 137:903–917PubMedGoogle Scholar
  32. Rozen DE, Lenski RE (2000) Long-term experimental evolution in Escherichia coli, VIII, dynamics of a balanced polymorphism. Am Nat 155:24–35PubMedCrossRefGoogle Scholar
  33. Rozen DE, Philippe N, de Visser JA, Lenski RE, Schneider D (2009) Death and cannibalism in a seasonal environment facilitate bacterial coexistence. Ecol Lett 12:34–44PubMedCrossRefGoogle Scholar
  34. Sniegowski PD, Gerrish PJ (2010) Beneficial mutations and the dynamics of adaptation in asexual populations. Philos Trans R Soc Lond B Biol Sci 365:1255–1263PubMedCrossRefGoogle Scholar
  35. Spencer CC, Bertrand M, Travisano M, Doebeli M (2007) Adaptive diversification in genes that regulate resource use in Escherichia coli. PLoS Genet 3:e15PubMedCrossRefGoogle Scholar
  36. Thompson J (2005) The geographic mosaic of coevolution. University of Chicago Press, ChicagoGoogle Scholar
  37. Treves DS, Manning S, Adams J (1998) Repeated evolution of an acetate crossfeeding polymorphism in long-term populations of Escherichia coli. Mol Biol Evol 15:789–797PubMedCrossRefGoogle Scholar
  38. Turner PE, Souza V, Lenski RE (1996) Tests of ecological mechanisms promoting the stable coexistence of two bacterial genotypes. Ecology 77:2119CrossRefGoogle Scholar
  39. Wray GA (2007) The evolutionary significance of cis-regulatory mutations. Nat Rev Genet 8:206–216PubMedCrossRefGoogle Scholar
  40. Wright S, Dobzhansky T (1946) Genetics of natural populations. Xii. Experimental reproduction of some of the changes caused by natural selection in certain populations of Drosophila pseudoobscura. Genetics 31:125–156Google Scholar
  41. Zeyl C (2006) Experimental evolution with yeast. FEMS Yeast Res 6:685–691PubMedCrossRefGoogle Scholar
  42. Zhong S, Khodursky A, Dykhuizen DE, Dean AM (2004) Evolutionary genomics of ecological specialization. Proc Natl Acad Sci USA 101:11719–11724PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2011

Authors and Affiliations

  • Margie Kinnersley
    • 1
  • Jared W. Wenger
    • 2
  • Gavin Sherlock
    • 2
  • Frank R. Rosenzweig
    • 1
  1. 1.Division of Biological SciencesUniversity of MontanaMissoulaUSA
  2. 2.Department of GeneticsStanford University School of MedicineStanfordUSA

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