A decade of genome sequencing has revolutionized studies of experimental evolution

Current Opinion in Microbiology

Volumn 45, Issue , 2018, Pages 149-155

  Bruger, Eric L ^a   Marx, Christopher J ^a  

^a UNIVERSITY OF IDAHO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GENOME; HUMAN; NATURAL POPULATION; REVIEW; BACTERIAL GENOME; BACTERIUM; GENETICS; HIGH THROUGHPUT SEQUENCING; METABOLISM; MOLECULAR EVOLUTION; WHOLE GENOME SEQUENCING;

BACTERIA; EVOLUTION, MOLECULAR; GENOME, BACTERIAL; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; WHOLE GENOME SEQUENCING;

EID: 85048499014     PISSN: 13695274     EISSN: 18790364     Source Type: Journal    
DOI: 10.1016/j.mib.2018.03.002     Document Type: Review

References (67)

1. Hass, J.W., The Reverend Dr William Henry Dallinger, FRS (1839–1909). Notes Rec Roy Soc 54 (2000), 53–65.
2. Haas, J.W., The Rev. Dr. William H. Dallinger FRS: early advocate of theistic evolution and foe of spontaneous generation’. Perspect Sci Christian Faith 52 (2000), 107–117.
3. Monod, J., Recherches sur la croissance des cultures bactériennes. 1942, Hermann & Cie.
4. Monod, J., La technique de culture continue: théorie et applications. Ann Inst Pasteur 79 (1950), 390–410.
5. Levin, B.R., Stewart, F.M., Chao, L., Resource-limited growth, competition, and predation: a model and experimental studies with bacteria and bacteriophage. Am Natural 111 (1977), 3–24.
6. Dykhuizen, D., Hartl, D., Evolution of competitive ability in Escherichia coli. Evolution 35 (1981), 581–594.
7. Hall, B.G., Zuzel, T., Evolution of a new enzymatic function by recombination within a gene. Proc Natl Acad Sci U S A 77 (1980), 3529–3533.
8. Horne, M.T., Coevolution of Escherichia coli and bacteriophage in chemostat culture. Science 168 (1970), 992–993.
9. Elena, S.F., Lenski, R.E., Evolution experiments with microorganisms: the dynamics and genetic bases of adaptation. Nature Rev Genet 4 (2003), 457–469 Review encapsulating major ideas about the dynamics and genetics of adaptive changes gleaned from experimental evolution studies predating major recent advances in sequencing technologies.
10. Lenski, R.E., Rose, M.R., Simpson, S.C., Tadler, S.C., Long-term experimental evolution in Escherichia coli. I. Adaptation and divergence during 2,000 generations. Am Natural 138 (1991), 1315–1341 A fundamental study examining the adaptive changes of multiple bacterial populations in parallel over a non-trivially long time period.
11. Lenski, R.E., Travisano, M., Dynamics of adaptation and diversification: a 10,000-generation experiment with bacterial populations. Proc Natl Acad Sci U S A 91 (1994), 6808–6814.
12. Kassen, R., The experimental evolution of specialists, generalists, and the maintenance of diversity. J Evol Biol 15 (2002), 173–190.
13. Pardo-Diaz, C., Salazar, C., Jiggins, C.D., Towards the identification of the loci of adaptive evolution. Meth Ecol Evol 6 (2015), 445–464.
14. Marx, C.J., Evolution as an experimental tool in microbiology: ‘bacterium, improve thyself!’. Environ Microbiol Rep 3 (2011), 12–14.
15. Velicer, G.J., Raddatz, G., Keller, H., Deiss, S., Lanz, C., Dinkelacker, I., Schuster, S.C., Comprehensive mutation identification in an evolved bacterial cooperator and its cheating ancestor. Proc Natl Acad Sci U S A 103 (2006), 8107–8112 First study to utilize whole-genome sequencing to investigate adaptive changes in clonal isolates from evolved Myxococcus xanthus popuations.
16. Barrick, J.E., Lenski, R.E., Genome dynamics during experimental evolution. Nature Rev Genet 14 (2013), 827–839 Important review that covers many concepts related to evolutionary and ecological forces driving genome adaptation that have been illuminated by genome sequencing approaches.
17. Bull, J.J., Badgett, M.R., Wichman, H.A., Huelsenbeck, J.P., Hillis, D.M., Gulati, A., Ho, C., Molineux, I.J., Exceptional convergent evolution in a virus. Genetics 147 (1997), 1497–1507.
18. Wichman, H.A., Badgett, M.R., Scott, L.A., Boulianne, C.M., Bull, J.J., Different trajectories of parallel evolution during viral adaptation. Science 285 (1999), 422–424.
19. Herring, C.D., Raghunathan, A., Honisch, C., Patel, T., Applebee, M.K., Joyce, A.R., Albert, T.J., Blattner, F.R., Van den Boom, D., Cantor, C.R., Palsson, B.Ø., Comparative genome sequencing of Escherichia coli allows observation of bacterial evolution on a laboratory timescale. Nature Genet 38 (2006), 1406–1412.
20. Chou, H.H., Chiu, H.C., Delaney, N.F., Segrè D., Marx, C.J., Diminishing returns epistasis among beneficial mutations decelerates adaptation. Science 332 (2011), 1190–1192.
21. Khan, A.I., Dinh, D.M., Schneider, D., Lenski, R.E., Cooper, T.F., Negative epistasis between beneficial mutations in an evolving bacterial population. Science 332 (2011), 1193–1196.
22. Tenaillon, O., Rodríguez-Verdugo, A., Gaut, R.L., McDonald, P., Bennett, A.F., Long, A.D., Gaut, B.S., The molecular diversity of adaptive convergence. Science 335 (2012), 457–461 A prominent example of the power of applying genome sequencing of isolates at a deep level to investigate fundamental biological questions, using statistical patterns from many independent populations to uncover epistasis and its effect on constraining adaptive trajectories, in this case in E. coli populations in response to temperature stress.
23. Maddamsetti, R., Lenski, R.E., Barrick, J.E., Adaptation, clonal interference, and frequency-dependent interactions in a long-term evolution experiment with Escherichia coli. Genetics 200 (2015), 619–631 The application of isolate sequencing over the time course in a particular evolved population of E. coli reveals critical information on phenomena affecting the adaptive dynamics of this population.
24. Atwood, K.C., Schneider, L.K., Ryan, F.J., Periodic selection in Escherichia coli. Proc Natl Acad Sci 37 (1951), 146–155.
25. Gerrish, P.J., Lenski, R.E., The fate of competing beneficial mutations in an asexual population. Genetica 102 (1998), 127–144.
26. Michener, J.K., Neves, A.A., Vuilleumier, S., Bringel, F., Marx, C.J., Effective use of a horizontally-transferred pathway for dichloromethane catabolism requires post-transfer refinement. Elife, 3, 2014, e04279.
27. Nayak, D.D., Agashe, D., Lee, M.C., Marx, C.J., Selection maintains apparently degenerate metabolic pathways due to tradeoffs in using methylamine for carbon versus nitrogen. Curr Biol 26 (2016), 1416–1426.
28. Koren, S., Phillippy, A.M., One chromosome, one contig: complete microbial genomes from long-read sequencing and assembly. Curr Opin Microbiol 23 (2015), 110–120.
29. Levy, S.E., Myers, R.M., Advancements in next-generation sequencing. Ann Rev Genom Hum Genet 17 (2016), 95–115.
30. Ning, L., Liu, G., Li, G., Hou, Y., Tong, Y., He, J., Current challenges in the bioinformatics of single cell genomics. Front Oncol, 4, 2014.
31. Gawad, C., Koh, W., Quake, S.R., Single-cell genome sequencing: current state of the science. Nature Rev Genet 17 (2016), 175–188.
32. Barrick, J.E., Lenski, R.E., Genome-wide mutational diversity in an evolving population of Escherichia coli. Cold Spring Harb Symp Quant Biol 74 (2009), 119–129.
33. Good, B.H., McDonald, M.J., Barrick, J.E., Lenski, R.E., Desai, M.M., The dynamics of molecular evolution over 60,000 generations. Nature 551 (2017), 45–50 Exceptional temporal metagenomic sequencing depth is applied to LTEE E. coli populations to produce detailed trajectories of genetic changes occurring within these populations.
34. Lang, G.I., Rice, D.P., Hickman, M.J., Sodergren, E., Weinstock, G.M., Botstein, D., Desai, M.M., Pervasive genetic hitchhiking and clonal interference in forty evolving yeast populations. Nature 500 (2013), 571–574 A principal example of the potential behind using of metagenomic sequencing for detecting within population changes, this paper revealed that lineages that selectively sweep populations are often composed of cohorts of beneficial mutations rather than alternating sweeps by single mutational changes.
35. Herron, M.D., Doebeli, M., Parallel evolutionary dynamics of adaptive diversification in Escherichia coli. PLoS Biol, 11, 2013, e1001490.
36. Marx, C.J., Can you sequence ecology? Metagenomics of adaptive diversification. PLoS Biol, 11, 2013, e1001487.
37. Cohan, F.M., Bacterial species and speciation. Syst Biol 50 (2001), 513–524.
38. Chubiz, L.M., Lee, M.C., Delaney, N.F., Marx, C.J., FREQ-Seq: a rapid, cost-effective, sequencing-based method to determine allele frequencies directly from mixed populations. PLoS One, 7, 2012, e47959.
39. Levy, S.F., Blundell, J.R., Venkataram, S., Petrov, D.A., Fisher, D.S., Sherlock, G., Quantitative evolutionary dynamics using high-resolution lineage tracking. Nature 519 (2015), 181–186 Demonstration of the utility of applying massively parallel barcoding to track early evolutionary dynamics, thereby uncovering the initial distribution of fitness effects of beneficial mutations in that environment.
40. Orr, H.A., The distribution of fitness effects among beneficial mutations. Genetics 163 (2003), 1519–1526.
41. Venkataram, S., Dunn, B., Li, Y., Agarwala, A., Chang, J., Ebel, E.R., Geiler-Samerotte, K., Hérissant, L., Blundell, J.R., Levy, S.F., Fisher, D.S., Development of a comprehensive genotype-to-fitness map of adaptation-driving mutations in yeast. Cell 166 (2016), 1585–1596.
42. Araya, C.L., Fowler, D.M., Deep mutational scanning: assessing protein function on a massive scale. Trends Biotechnol 29 (2011), 435–442.
43. Wrenbeck, E.E., Klesmith, J.R., Stapleton, J.A., Adeniran, A., Tyo, K.E., Whitehead, T.A., Plasmid-based one-pot saturation mutagenesis. Nature Meth 13 (2016), 928–930.
44. Wang, H.H., Isaacs, F.J., Carr, P.A., Sun, Z.Z., Xu, G., Forest, C.R., Church, G.M., Programming cells by multiplex genome engineering and accelerated evolution. Nature 460 (2009), 894–898 Herein, multiplexed gene editing using MAGE approach in E. coli is used to rapidly introduce variation pertinent to the 1-deoxy-D-xylulose-5-phosphate (DXP) biosynthesis pathway.
45. Wang, H.H., Kim, H., Cong, L., Jeong, J., Bang, D., Church, G.M., Genome-scale promoter engineering by coselection MAGE. Nature Meth 9 (2012), 591–593 Further demonstration of the use of MAGE to quickly introduce variation on the genome scale to introduce promoter changes at multiple operons.
46. Dalia, A.B., McDonough, E., Camilli, A., Multiplex genome editing by natural transformation. Proc Natl Acad Sci U S A 111 (2014), 8937–8942 Another multiplexed genome editing technique that depends on natural competence, MuGENT, is introduced to rapidly introduce multiple mutational changes into the genome of Vibrio cholerae.
47. Dalia, T.N., Hayes, C.A., Stolyar, S., Marx, C.J., McKinlay, J.B., Dalia, A.B., Multiplex genome editing by natural transformation (MuGENT) for synthetic biology in Vibrio natriegens. ACS Synth Biol 6 (2017), 1650–1655.
48. Nayak, D.D., Metcalf, W.W., Cas9-mediated genome editing in the methanogenic archaeon Methanosarcina acetivorans. Proc Natl Acad Sci U S A 114 (2017), 2976–2981.
49. Jiang, W., Bikard, D., Cox, D., Zhang, F., Marraffini, L.A., RNA-guided editing of bacterial genomes using CRISPR-Cas systems. Nature Biotechnol 31 (2013), 233–239.
50. Garst, A.D., Bassalo, M.C., Pines, G., Lynch, S.A., Halweg-Edwards, A.L., Liu, R., Liang, L., Wang, Z., Zeitoun, R., Alexander, W.G., Gill, R.T., Genome-wide mapping of mutations at single-nucleotide resolution for protein, metabolic and genome engineering. Nature Biotechnol 35 (2017), 48–55.
51. Isaacs, F.J., Carr, P.A., Wang, H.H., Lajoie, M.J., Sterling, B., Kraal, L., Tolonen, A.C., Gianoulis, T.A., Goodman, D.B., Reppas, N.B., Emig, C.J., Precise manipulation of chromosomes in vivo enables genome-wide codon replacement. Science 333 (2011), 348–353.
52. Zeitoun, R.I., Pines, G., Grau, W.C., Gill, R.T., Quantitative tracking of combinatorially engineered populations with multiplexed binary assemblies. ACS Synth Biol 6 (2017), 619–627.
53. Orgogozo, V., Morizot, B., Martin, A., The differential view of genotype–phenotype relationships. Front Genet, 6, 2015.
54. De Visser, J.A., Krug, J., Empirical fitness landscapes and the predictability of evolution. Nature Rev Genet 15 (2014), 480–490.
55. Lässig, M., Mustonen, V., Walczak, A.M., Predicting evolution. Nature Ecol Evol, 1, 2017, 0077.
56. Datta, M.S., Sliwerska, E., Gore, J., Polz, M.F., Cordero, O.X., Microbial interactions lead to rapid micro-scale successions on model marine particles. Nature Commun, 7, 2016, 11965.
57. Cordero, O.X., Ventouras, L.A., DeLong, E.F., Polz, M.F., Public good dynamics drive evolution of iron acquisition strategies in natural bacterioplankton populations. Proc Natl Acad Sci U S A 109 (2012), 20059–20064.
58. Lieberman, T.D., Michel, J.B., Aingaran, M., Potter-Bynoe, G., Roux, D., Davis, M.R. Jr., Skurnik, D., Leiby, N., LiPuma, J.J., Goldberg, J.B., McAdam, A.J., Parallel bacterial evolution within multiple patients identifies candidate pathogenicity genes. Nature Genet 43 (2011), 1275–1280 A premier example of how sequencing approaches can be leveraged to yield information about the evolution of bacterial infections within patients.
59. Xue, K.S., Stevens-Ayers, T., Campbell, A.P., Englund, J.A., Pergam, S.A., Boeckh, M., Bloom, J.D., Parallel evolution of influenza across multiple spatiotemporal scales. Elife, 6, 2017.
60. Silva, I.N., Santos, P.M., Santos, M.R., Zlosnik, J.E., Speert, D.P., Buskirk, S.W., Bruger, E.L., Waters, C.M., Cooper, V.S., Moreira, L.M., Long-term evolution of Burkholderia multivorans during a chronic cystic fibrosis infection reveals shifting forces of selection. mSystems, 1, 2016 e00029-16.
61. Zhao, S., Lieberman, T.D., Poyet, M., Groussin, M., Gibbons, S.M., Xavier, R.J., Alm, E.J., Adaptive evolution within the gut microbiome of individual people. bioRxiv, 2017, 208009.
62. Marvig, R.L., Sommer, L.M., Molin, S., Johansen, H.K., Convergent evolution and adaptation of Pseudomonas aeruginosa within patients with cystic fibrosis. Nature Genet 47 (2015), 57–64.
63. Levade, I., Terrat, Y., Leducq, J.B., Weil, A.A., Mayo-Smith, L.M., Chowdhury, F., Khan, A.I., Boncy, J., Buteau, J., Ivers, L.C., Ryan, E.T., Charles, R.C., Calderwood, S.B., Qadri, F., Harris, J.B., LaRocque, R.C., Shapiro, B.J., Vibrio cholerae genomic diversity within and between patients. Microb Genom, 3, 2017.
64. Blundell, J.R., Levy, S.F., Beyond genome sequencing: lineage tracking with barcodes to study the dynamics of evolution, infection, and cancer. Genomics 104 (2014), 417–430.
65. Van Opijnen, T., Camilli, A., Transposon insertion sequencing: a new tool for systems-level analysis of microorganisms. Nature Rev Microbiol 11 (2013), 435–442.
66. Barrick, J.E., Yu, D.S., Yoon, S.H., Jeong, H., Oh, T.K., Schneider, D., Lenski, R.E., Kim, J.F., Genome evolution and adaptation in a long-term experiment with Escherichia coli. Nature 461 (2009), 1243–1247 First detailed application of genomic sequencing of isolates to a long-term experimentally evolved population. The study also provides a detailed accounting of the adaptive changes encountered by the examined experimental population over the course of 40,000 generations.
67. Lieberman, T.D., Seven billion microcosms: evolution within human microbiomes. mSystems 3 (2018), e00171–17.