Evolutionary insight from whole-genome sequencing of experimentally evolved microbes

Molecular Ecology

Volumn 21, Issue 9, 2012, Pages 2058-2077

  Dettman, Jeremy R ^a   Rodrigue, Nicolas ^b   Melnyk, Anita H ^a   Wong, Alex ^c   Bailey, Susan F ^a   Kassen, Rees ^a  

^a UNIVERSITY OF OTTAWA   (Canada)

^b OTTAWA RESEARCH AND DEVELOPMENT CENTRE   (Canada)

^c CARLETON UNIVERSITY   (Canada)

Author keywords

adaptive evolution; evolutionary genomics; experimental evolution; next generation sequencing

Indexed keywords

BACTERIAL CHROMOSOME; BACTERIAL GENOME; BACTERIUM; CHROMOSOME; CHROMOSOME MAP; DIRECTED MOLECULAR EVOLUTION; DNA SEQUENCE; FUNGAL GENOME; FUNGUS; GENETICS; HIGH THROUGHPUT SEQUENCING; MOLECULAR EVOLUTION; REVIEW;

BACTERIA; CHROMOSOME MAPPING; CHROMOSOMES, BACTERIAL; CHROMOSOMES, FUNGAL; DIRECTED MOLECULAR EVOLUTION; EVOLUTION, MOLECULAR; FUNGI; GENOME, BACTERIAL; GENOME, FUNGAL; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; SEQUENCE ANALYSIS, DNA;

EID: 84860663163     PISSN: 09621083     EISSN: 1365294X     Source Type: Journal    
DOI: 10.1111/j.1365-294X.2012.05484.x     Document Type: Review

References (120)

1. Anderson JB, Funt J, Thompson DA, et al. (2010) Determinants of divergent adaptation and Dobzhansky-Muller interaction in experimental yeast populations. Current Biology, 20, 1383-1388.
2. Applebee MK, Herrgard MJ, Palsson BO, (2008) Impact of individual mutations on increased fitness in adaptively evolved strains of Escherichia coli. Journal of Bacteriology, 190, 5087-5094.
3. Araya CL, Payen C, Dunham MJ, Fields S, (2010) Whole-genome sequencing of a laboratory-evolved yeast strain. BMC Genomics, 11, 88.
4. Atsumi S, Wu TY, Machado IMP, et al. (2010) Evolution, genomic analysis, and reconstruction of isobutanol tolerance in Escherichia coli. Molecular Systems Biology, 6, 449.
5. Bao H, Guo H, Wang JW, et al. (2009) MapView: visualization of short reads alignment on a desktop computer. Bioinformatics, 25, 1554-1555.
6. Barrick JE, Lenski RE, (2009) Genome-wide mutational diversity in an evolving population of Escherichia coli. Cold Spring Harbor Symposia on Quantitative Biology, 74, 119-129.
7. Barrick JE, Yu DS, Yoon SH, et al. (2009) Genome evolution and adaptation in a long-term experiment with Escherichia coli. Nature, 461, 1243-1247.
8. Beaumont HJE, Gallie J, Kost C, Ferguson GC, Rainey PB, (2009) Experimental evolution of bet hedging. Nature, 462, 90-93.
9. Bell G, Collins S, (2008) Adaptation, extinction and global change. Evolutionary Applications, 1, 3-16.
10. Betancourt AJ, (2009) Genomewide patterns of substitution in adaptively evolving populations of the RNA Bacteriophage MS2. Genetics, 181, 1535-1544.
11. Blankenberg D, Von Kuster G, Coraor N, et al. (2010) Galaxy: a web-based genome analysis tool for experimentalists. Current Protocols in Molecular Biology, Chapter 19, 1-21.
12. Brockhurst MA, Colegrave N, Rozen DE, (2011) Next-generation sequencing as a tool to study microbial evolution. Molecular Ecology, 20, 972-980.
13. Brown CJ, Todd KM, Rosenzweig RF, (1998) Multiple duplications of yeast hexose transport genes in response to selection in a glucose-limited environment. Molecular Biology and Evolution, 15, 931-942.
14. Buckling A, Maclean RC, Brockhurst MA, Colegrave N, (2009) The Beagle in a bottle. Nature, 457, 824-829.
15. Burke MK, Dunham JP, Shahrestani P, et al. (2010) Genome-wide analysis of a long-term evolution experiment with Drosophila. Nature, 467, 587-590.
16. Chou HH, Chiu HC, Delaney NF, Segre D, Marx CJ, (2011) Diminishing returns epistasis among beneficial mutations decelerates adaptation. Science, 332, 1190-1192.
17. Conrad TM, Joyce AR, Applebee MK, et al. (2009) Whole-genome resequencing of Escherichia coli K-12 MG1655 undergoing short-term laboratory evolution in lactate minimal media reveals flexible selection of adaptive mutations. Genome Biology, 10, R118.
18. Conrad TM, Frazier M, Joyce AR, et al. (2010) RNA polymerase mutants found through adaptive evolution reprogram Escherichia coli for optimal growth in minimal media. Proceedings of the National Academy of Sciences of the United States of America, 107, 20500-20505.
19. Cooper VS, Schneider D, Blot M, Lenski RE, (2001) Mechanisms causing rapid and parallel losses of ribose catabolism in evolving populations of Escherichia coli B. Journal of Bacteriology, 183, 2834-2841.
20. Cooper TF, Rozen DE, Lenski RE, (2003) Parallel changes in qene expression after 20,000 generations of evolution in Escherichia coli. Proceedings of the National Academy of Sciences of the United States of America, 100, 1072-1077.
21. Costanzo M, Baryshnikova A, Bellay J, et al. (2010) The genetic landscape of a cell. Science, 327, 425-431.
22. Croucher NJ, Harris SR, Fraser C, et al. (2011) Rapid pneumococcal evolution in response to clinical interventions. Science, 331, 430-434.
23. Crozat E, Philippe N, Lenski RE, Geiselmann J, Schneider D, (2005) Long-term experimental evolution in Escherichia coli. XII. DNA topology as a key target of selection. Genetics, 169, 523-532.
24. Crozat E, Winkworth C, Gaffe J, et al. (2010) Parallel genetic and phenotypic evolution of DNA superhelicity in experimental populations of Escherichia coli. Molecular Biology and Evolution, 27, 2113-2128.
25. Dallinger WH, (1887) The President's address. Journal of the Royal Microscopic Society, 7, 184-199.
26. De Vecchi E, Nicola L, Ossola F, Drago L, (2009) In vitro selection of resistance in Streptococcus pneumoniae at in vivo fluoroquinolone concentrations. Journal of Antimicrobial Chemotherapy, 63, 721-727.
27. Denver DR, Howe DK, Wilhelm LJ, et al. (2010) Selective sweeps and parallel mutation in the adaptive recovery from deleterious mutation in Caenorhabditis elegans. Genome Research, 20, 1663-1671.
28. Deutschbauer AM, Davis RW, (2005) Quantitative trait loci mapped to single-nucleotide resolution in yeast. Nature Genetics, 37, 1333-1340.
29. Dong T, Chiang SM, Joyce C, Yu R, Schellhorn HE, (2009) Polymorphism and selection of rpoS in pathogenic Escherichia coli. BMC Microbiology, 9, 119.
30. Drago L, Nicola L, Mattina R, De Vecchi E, (2010) In vitro selection of resistance in Escherichia coli and Klebsiella spp. at in vivo fluoroquinolone concentrations. BMC Microbiology, 10, 119.
31. Dunham MJ, Badrane H, Ferea T, et al. (2002) Characteristic genome rearrangements in experimental evolution of Saccharomyces cerevisiae. Proceedings of the National Academy of Sciences of the United States of America, 99, 16144-16149.
32. Elena SF, Lenski RE, (2003) Evolution experiments with microorganisms: the dynamics and genetic bases of adaptation. Nature Reviews Genetics, 4, 457-469.
33. Ferea TL, Botstein D, Brown PO, Rosenzweig RF, (1999) Systematic changes in gene expression patterns following adaptive evolution in yeast. Proceedings of the National Academy of Sciences of the United States of America, 96, 9721-9726.
34. Fisher RA, (1930) The Genetical Theory of Natural Selection. Oxford University Press, Oxford, UK.
35. Fong SS, Joyce AR, Palsson BO, (2005) Parallel adaptive evolution cultures of Escherichia coli lead to convergent growth phenotypes with different gene expression states. Genome Research, 15, 1365-1372.
36. Friesen ML, Saxer G, Travisano M, Doebeli M, (2004) Experimental evidence for sympatric ecological diversification due to frequency-dependent competition in Escherichia coli. Evolution, 58, 245-260.
37. Gifford DR, Schoustra SE, Kassen R, (2011) The length of adaptive walks is insensitive to starting fitness in Aspergillus nidulans. Evolution, 65, 3070-3078.
38. Gnerre S, MacCallum I, Przybylski D, et al. (2011) High-quality draft assemblies of mammalian genomes from massively parallel sequence data. Proceedings of the National Academy of Sciences of the United States of America, 108, 1513-1518.
39. Goecks J, Nekrutenko A, Taylor J, (2010) Galaxy: a comprehensive approach for supporting accessible, reproducible, and transparent computational research in the life sciences. Genome Biology, 11, R86.
40. Gresham D, Ruderfer DM, Pratt SC, et al. (2006) Genome-wide detection of polymorphisms at nucleotide resolution with a single DNA microarray. Science, 311, 1932-1936.
41. Gresham D, Desai MM, Tucker CM, et al. (2008) The repertoire and dynamics of evolutionary adaptations to controlled nutrient-limited environments in yeast. PLoS Genetics, 4, e1000303.
42. Gresham D, Curry B, Ward A, et al. (2010) Optimized detection of sequence variation in heterozygous genomes using DNA microarrays with isothermal-melting probes. Proceedings of the National Academy of Sciences of the United States of America, 107, 1482-1487.
43. Harismendy O, Ng PC, Strausberg RL, et al. (2009) Evaluation of next generation sequencing platforms for population targeted sequencing studies. Genome Biology, 10, R32.
44. He XL, Qian WF, Wang Z, Li Y, Zhang JZ, (2010) Prevalent positive epistasis in Escherichia coli and Saccharomyces cerevisiae metabolic networks. Nature Genetics, 42, 272-276.
45. Hegreness M, Kishony R, (2007) Analysis of genetic systems using experimental evolution and whole-genome sequencing. Genome Biology, 8, 201.
46. Herring CD, Palsson BO, (2007) An evaluation of comparative genome sequencing (CGS) by comparing two previously-sequenced bacterial genomes. BMC Genomics, 8, 274.
47. Herring CD, Raghunathan A, Honisch C, et al. (2006) Comparative genome sequencing of Escherichia coli allows observation of bacterial evolution on a laboratory timescale. Nature Genetics, 38, 1406-1412.
48. Hoekstra HE, Coyne JA, (2007) The locus of evolution: evo devo and the genetics of adaptation. Evolution, 61, 995-1016.
49. Homer N, Nelson SF, (2010) Improved variant discovery through local re-alignment of short-read next-generation sequencing data using SRMA. Genome Biology, 11, R99.
50. Hou HB, Zhao FQ, Zhou LL, et al. (2010) MagicViewer: integrated solution for next-generation sequencing data visualization and genetic variation detection and annotation. Nucleic Acids Research, 38, W732-W736.
51. Huang WC, Marth G, (2008) EagleView: a genome assembly viewer for next-generation sequencing technologies. Genome Research, 18, 1538-1543.
52. Huisinga KL, Pugh BF, (2004) A genome-wide housekeeping role for TFIID and a highly regulated stress-related role for SAGA in Saccharomyces cerevisiae. Molecular Cell, 13, 573-585.
53. Kao KC, Sherlock G, (2008) Molecular characterization of clonal interference during adaptive evolution in asexual populations of Saccharomyces cerevisiae. Nature Genetics, 40, 1499-1504.
54. Khan AI, Dinh DM, Schneider D, Lenski RE, Cooper TF, (2011) Negative epistasis between beneficial mutations in an evolving bacterial population. Science, 332, 1193-1196.
55. Kinnersley MA, Holben WE, Rosenzweig F, (2009) E Unibus Plurum: genomic analysis of an experimentally evolved polymorphism in Escherichia coli. PLoS Genetics, 5, e1000713.
56. Kvitek DJ, Sherlock G, (2011) Reciprocal sign epistasis between frequently experimentally evolved adaptive mutations causes a rugged fitness landscape. PLoS Genetics, 7, e1002056.
57. Lang GI, Botstein D, Desai MM, (2011) Genetic variation and the fate of beneficial mutations in asexual populations. Genetics, 188, 647-661.
58. Langmead B, Trapnell C, Pop M, Salzberg SL, (2009) Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biology, 10, R25.
59. Lee DH, Palsson BO, (2010) Adaptive evolution of Escherichia coli K-12 MG1655 during growth on a nonnative carbon source, L-1,2-propanediol. Applied and Environmental Microbiology, 76, 4158-4168.
60. Lee SI, Dudley AM, Drubin D, et al. (2009) Learning a prior on regulatory potential from eQTL data. PLoS Genetics, 5, e1000358.
61. Lenski RE, Travisano M, (1994) Dynamics of adaptation and diversification-a 10,000-generation experiment with bacterial populations. Proceedings of the National Academy of Sciences of the United States of America, 91, 6808-6814.
62. Lenski RE, Winkworth CL, Riley MA, (2003) Rates of DNA sequence evolution in experimental populations of Escherichia coli during 20,000 generations. Journal of Molecular Evolution, 56, 498-508.
63. Li H, Durbin R, (2010) Fast and accurate long-read alignment with Burrows-Wheeler transform. Bioinformatics, 26, 589-595.
64. Li H, Homer N, (2010) A survey of sequence alignment algorithms for next-generation sequencing. Briefings in Bioinformatics, 11, 473-483.
65. Li H, Ruan J, Durbin R, (2008) Mapping short DNA sequencing reads and calling variants using mapping quality scores. Genome Research, 18, 1851-1858.
66. Li H, Handsaker B, Wysoker A, et al. (2009a) The Sequence Alignment/Map format and SAMtools. Bioinformatics, 25, 2078-2079.
67. Li RQ, Yu C, Li YR, et al. (2009b) SOAP2: an improved ultrafast tool for short read alignment. Bioinformatics, 25, 1966-1967.
68. Liti G, Carter DM, Moses AM, et al. (2009) Population genomics of domestic and wild yeasts. Nature, 458, 337-341.
69. Luo CW, Walk ST, Gordon DM, et al. (2011) Genome sequencing of environmental Escherichia coli expands understanding of the ecology and speciation of the model bacterial species. Proceedings of the National Academy of Sciences of the United States of America, 108, 7200-7205.
70. Maharjan R, Seeto S, Notley-McRobb L, Ferenci T, (2006) Clonal adaptive radiation in a constant environment. Science, 313, 514-517.
71. Maharjan R, Zhou ZM, Ren Y, et al. (2010) Genomic identification of a novel mutation in hfq that provides multiple benefits in evolving glucose-limited populations of Escherichia coli. Journal of Bacteriology, 192, 4517-4521.
72. McKenna A, Hanna M, Banks E, et al. (2010) The genome analysis toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Research, 20, 1297-1303.
73. Melnyk AH, Kassen R, (2011) Adaptive landscapes in evolving populations of Pseudomonas fluorescens. Evolution, 65, 3048-3059.
74. Miller CR, Joyce P, Wichman HA, (2011) Mutational effects and population dynamics during viral adaptation challenge current models. Genetics, 187, 185-202.
75. Minty JJ, Lesnefsky AA, Lin FM, et al. (2011) Evolution combined with genomic study elucidates genetic bases of isobutanol tolerance in Escherichia coli. Microbial Cell Factories, 10, 18.
76. Notley-McRobb L, Ferenci T, (1999) Adaptive mgl-regulatory mutations and genetic diversity evolving in glucose-limited Escherichia coli populations. Environmental Microbiology, 1, 33-43.
77. Notley-McRobb L, King T, Ferenci T, (2002) rpoS mutations and loss of general stress resistance in Escherichia coli populations as a consequence of conflict between competing stress responses. Journal of Bacteriology, 184, 806-811.
78. Orr HA, (2005a) The genetic theory of adaptation: a brief history. Nature Reviews Genetics, 6, 119-127.
79. Orr HA, (2005b) The probability of parallel evolution. Evolution, 59, 216-220.
80. Ostrowski EA, Woods RJ, Lenski RE, (2008) The genetic basis of parallel and divergent phenotypic responses in evolving populations of Escherichia coli. Proceedings of the Royal Society B-Biological Sciences, 275, 277-284.
81. Papp B, Notebaart RA, Pál C, (2011) Systems-biology approaches for predicting genomic evolution. Nature Reviews Genetics, 12, 591-602.
82. Paquin CE, Adams J, (1983) Relative fitness can decrease in evolving asexual populations of S. cerevisiae. Nature, 306, 368-371.
83. Paterson S, Vogwill T, Buckling A, et al. (2010) Antagonistic coevolution accelerates molecular evolution. Nature, 464, 275-278.
84. Pelosi L, Kuhn L, Guetta D, et al. (2006) Parallel changes in global protein profiles during long-term experimental evolution in Escherichia coli. Genetics, 173, 1851-1869.
85. Philippe N, Crozat E, Lenski RE, Schneider D, (2007) Evolution of global regulatory networks during a long-term experiment with Escherichia coli. Bioessays, 29, 846-860.
86. Phillips PC, (2008) Epistasis-the essential role of gene interactions in the structure and evolution of genetic systems. Nature Reviews Genetics, 9, 855-867.
87. Piddock LJV, (1999) Mechanisms of fluoroquinolone resistance: an update 1994-1998. Drugs, 58, 11-18.
88. Rainey PB, Travisano M, (1998) Adaptive radiation in a heterogeneous environment. Nature, 394, 69-72.
89. Rozen DE, Lenski RE, (2000) Long-term experimental evolution in Escherichia coli. VIII. Dynamics of a balanced polymorphism. American Naturalist, 155, 24-35.
90. Rozen DE, Philippe N, de Visser JA, Lenski RE, Schneider D, (2009) Death and cannibalism in a seasonal environment facilitate bacterial coexistence. Ecology Letters, 12, 34-44.
91. Sanjuan R, Elena SF, (2006) Epistasis correlates to genomic complexity. Proceedings of the National Academy of Sciences of the United States of America, 103, 14402-14405.
92. Sanjuan R, Nebot MR, (2008) A network model for the correlation between epistasis and genomic complexity. PLoS ONE, 3, e2663.
93. Schacherer J, Shapiro JA, Ruderfer DM, Kruglyak L, (2009) Comprehensive polymorphism survey elucidates population structure of Saccharomyces cerevisiae. Nature, 458, 342-345.
94. Schoustra SE, Bataillon T, Gifford DR, Kassen R, (2009) The properties of adaptive walks in evolving populations of fungus. PLoS Biology, 7, e1000250.
95. Segre D, DeLuna A, Church GM, Kishony R, (2005) Modular epistasis in yeast metabolism. Nature Genetics, 37, 77-83.
96. Shen YF, Wan ZZ, Coarfa C, et al. (2010) A SNP discovery method to assess variant allele probability from next-generation resequencing data. Genome Research, 20, 273-280.
97. Shendure J, Porreca GJ, Reppas NB, et al. (2005) Accurate multiplex polony sequencing of an evolved bacterial genome. Science, 309, 1728-1732.
98. Sinha H, Nicholson BP, Steinmetz LM, McCusker JH, (2006) Complex genetic interactions in a quantitative trait locus. PLoS Genetics, 2, e13.
99. Smith EE, Buckley DG, Wu ZN, et al. (2006) Genetic adaptation by Pseudomonas aeruginosa to the airways of cystic fibrosis patients. Proceedings of the National Academy of Sciences of the United States of America, 103, 8487-8492.
100. Smith DR, Quinlan AR, Peckham HE, et al. (2008) Rapid whole-genome mutational profiling using next-generation sequencing technologies. Genome Research, 18, 1638-1642.
101. Spigaglia P, Barbanti F, Louie T, Barbut F, Mastrantonio P, (2009) Molecular analysis of the gyrA and gyrB quinolone resistance-determining regions of fluoroquinolone-resistant Clostridium difficile mutants selected in vitro. Antimicrobial Agents and Chemotherapy, 53, 2463-2468.
102. Stern DL, Orgogozo V, (2008) The loci of evolution: how predictable is genetic evolution? Evolution, 62, 2155-2177.
103. Szappanos B, Kovacs K, Szamecz B, et al. (2011) An integrated approach to characterize genetic interaction networks in yeast metabolism. Nature Genetics, 43, 656-662.
104. Travisano M, Vasi F, Lenski RE, (1995) Long-term experimental evolution in Escherichia coli. 3. Variation among replicate populations in correlated responses to novel environments. Evolution, 49, 189-200.
105. Treves DS, Manning S, Adams J, (1998) Repeated evolution of an acetate-crossfeeding polymorphism in long-term populations of Escherichia coli. Molecular Biology and Evolution, 15, 789-797.
106. Turner TL, Stewart AD, Fields AT, Rice WR, Tarone AM, (2011) Population-based resequencing of experimentally evolved populations reveals the genetic basis of body size variation in Drosophila melanogaster. PLoS Genetics, 7, e1001336.
107. Velicer GJ, Raddatz G, Keller H, et al. (2006) Comprehensive mutation identification in an evolved bacterial cooperator and its cheating ancestor. Proceedings of the National Academy of Sciences of the United States of America, 103, 8107-8112.
108. Wagner A, (2008) Robustness and evolvability: a paradox resolved. Proceedings of the Royal Society B-Biological Sciences, 275, 91-100.
109. Wang L, Spira B, Zhou ZM, et al. (2010) Divergence involving global regulatory gene mutations in an Escherichia coli population evolving under phosphate limitation. Genome Biology and Evolution, 2, 478-487.
110. Weber H, Polen T, Heuveling J, Wendisch VF, Hengge R, (2005) Genome-wide analysis of the general stress response network in Escherichia coli: sigma(S)-dependent genes, promoters, and sigma factor selectivity. Journal of Bacteriology, 187, 1591-1603.
111. Wichman HA, Brown CJ, (2010) Experimental evolution of viruses: Microviridae as a model system. Philosophical Transactions of the Royal Society B-Biological Sciences, 365, 2495-2501.
112. Wong A, Kassen R, (2011) Parallel evolution and local differentiation in quinolone resistance in Pseudomonas aeruginosa. Microbiology, 157, 937-944.
113. Woods R, Schneider D, Winkworth CL, Riley MA, Lenski RE, (2006) Tests of parallel molecular evolution in a long-term experiment with Escherichia coli. Proceedings of the National Academy of Sciences of the United States of America, 103, 9107-9112.
114. Woods RJ, Barrick JE, Cooper TF, et al. (2011) Second-order selection for evolvability in a large Escherichia coli population. Science, 331, 1433-1436.
115. Wray GA, (2007) The evolutionary significance of cis-regulatory mutations. Nature Reviews Genetics, 8, 206-216.
116. Yang L, Jelsbak L, Marvig RL, et al. (2011) Evolutionary dynamics of bacteria in a human host environment. Proceedings of the National Academy of Sciences of the United States of America, 108, 7481-7486.
117. Zambrano MM, Siegele DA, Almiron M, Tormo A, Kolter R, (1993) Microbial competition-Escherichia coli mutants that take over stationary phase cultures. Science, 259, 1757-1760.
118. Zeyl C, (2005) The number of mutations selected during adaptation in a laboratory population of Saccharomyces cerevisiae. Genetics, 169, 1825-1831.
119. Zhang QC, Lambert G, Liao D, et al. (2011) Acceleration of emergence of bacterial antibiotic resistance in connected microenvironments. Science, 333, 1764-1767.
120. Zhu J, Zhang B, Smith EN, et al. (2008) Integrating large-scale functional genomic data to dissect the complexity of yeast regulatory networks. Nature Genetics, 40, 854-861.