Simple phenotypic sweeps hide complex genetic changes in populations

Genome Biology and Evolution

Volumn 7, Issue 2, 2015, Pages 531-544

  Maharjan, Ram P ^a   Liu, Bin ^b,c   Feng, Lu ^b,c   Ferenci, Thomas ^a   Wang, Lei ^b,c  

^a UNIVERSITY OF SYDNEY   (Australia)

^b NANKAI UNIVERSITY   (China)

^c BEIJING UNIVERSITY OF POSTS AND TELECOMMUNICATIONS   (China)

Author keywords

E. coli genome; experimental evolution; metagenomics; mutational sweeps; periodic selection

Indexed keywords

BACTERIA (MICROORGANISMS);

ADAPTATION; BACTERIAL GENE; CYTOLOGY; DNA SEQUENCE; ESCHERICHIA COLI K 12; EVOLUTION; GENE DUPLICATION; GENE FREQUENCY; GENETICS; GENOTYPE; INDEL MUTATION; PHENOTYPE;

ADAPTATION, PHYSIOLOGICAL; BIOLOGICAL EVOLUTION; ESCHERICHIA COLI K12; GENE DUPLICATION; GENE FREQUENCY; GENES, BACTERIAL; GENOTYPE; INDEL MUTATION; PHENOTYPE; SEQUENCE ANALYSIS, DNA;

EID: 84928258832     PISSN: None     EISSN: 17596653     Source Type: Journal    
DOI: 10.1093/gbe/evv004     Document Type: Article

References (54)

1. Armstrong RA, McGehee R. 1980. Competitive exclusion. Am Nat. 115: 151-170.
2. Atwood K, Schneider LK, Ryan FJ. 1951a. Periodic selection in Escherichia coli. Proc Natl Acad Sci U S A. 37:146.
3. Atwood KC, Schneider LK, Ryan FJ. 1951b. Selective mechanisms in bacteria. Cold Spring Harb Symp Quant Biol. 16:345-355.
4. Barrick JE, Lenski RE. 2009. Genome-wide mutational diversity in an evolving population of Escherichia coli. Cold Spring Harb Symp Quant Biol. 74:119-129.
5. Barrick JE, Lenski RE. 2013. Genome dynamics during experimental evolution. Nat Rev Genet. 14:827-839.
6. Barroso-Batista J, et al. 2014. The first steps of adaptation of Escherichia coli to the gut are dominated by soft sweeps. PLoS Genet. 10: e1004182.
7. Berg OG. 1995. Periodic selection and hitchhiking in a bacterial population. J Theor Biol. 173:307-320.
8. Cox M, Peterson D, Biggs P. 2010. SolexaQA: at-a-glance quality assessment of Illumina second-generation sequencing data. BMC Bioinformatics 11:485.
9. de Visser JAGM, Rozen DE. 2006. Clonal interference and the periodic selection of new beneficialmutations in Escherichia coli. Genetics 172: 2093-2100.
10. de Visser JAGM, Zeyl CW, Gerrish PJ, Blanchard JL, Lenski RE. 1999. Diminishing returns from mutation supply rate in asexual populations. Science 283:404-406.
11. Death A, Notley L, Ferenci T. 1993. Derepression of LamB protein facilitates outer membrane permeation of carbohydrates into Escherichia coli under conditions of nutrient stress. J Bacteriol. 175:1475-1483.
12. Dykhuizen DE, Hartl DE. 1983. Selection in chemostats. Microbiol Rev. 47: 150-168.
13. Ferenci T. 2008a. Bacterial physiology, regulation and mutational adaptation in a chemostat environment. Adv Microb Physiol. 53:169-229.
14. Ferenci T. 2008b. The spread of a beneficial mutation in experimental bacterial populations: the influence of the environment and genotype on the fixation of rpoS mutations. Heredity 100:446-452.
15. Ferenci T, et al. 2009. Genomic sequencing reveals regulatory mutations and recombinational events in the widely used MC4100 lineage of Escherichia coli K-12. J Bacteriol. 191:4025-4029.
16. Fischer E, Sauer U. 2003. A novel metabolic cycle catalyzes glucose oxidation and anaplerosis in hungry Escherichia coli. J Biol Chem. 278: 46446-46451.
17. Gaffe J, et al. 2011. Insertion sequence-driven evolution of Escherichia coli in Chemostats. J Mol Evol. 72:398-412.
18. Garrison E, Marth G. 2012. Haplotype-based variant detection from shortread sequencing. arXiv 1207; 3907v2 [q-bio.GN].
19. Gerrish PJ, Lenski RE. 1998. The fate of competing beneficial mutations in an asexual population. Genetica 103:127-144.
20. Gresham D, et al. 2008. The repertoire and dynamics of evolutionary adaptations to controlled nutrient-limited environments in yeast. PLoS Genet. 4:e1000303.
21. Hermisson J, Pennings PS. 2005. Soft sweeps: molecular population genetics of adaptation from standing genetic variation. Genetics 169: 2335-2352.
22. Herron MD, Doebeli M. 2013. Parallel evolutionary dynamics of adaptive diversification in Escherichia coli. PLoS Biol. 11:e1001490.
23. Hove-Jensen B, Rosenkrantz TJ, Haldimann A, Wanner BL. 2003. Escherichia coli phnN, encoding ribose 1,5-bisphosphokinase activity (phosphoribosyl diphosphate forming): dual role in phosphonate degradation and NAD biosynthesis pathways. J Bacteriol. 185: 2793-2801.
24. Kellermann OK, Ferenci T. 1982. Maltose-binding protein fromEscherichia coli. Methods Enzymol. 90:459-463.
25. Kinnersley MA, Holben WE, Rosenzweig F. 2009. E Unibus Plurum: genomic analysis of an experimentally evolved polymorphism in Escherichia coli. PLoS Genet. 5:e1000713.
26. Koch AL. 1974. The pertinence of the periodic selection phenomenon to prokaryote evolution. Genetics 77:127-142.
27. Kubitschek HE. 1970. Introduction to research with continuous cultures. Englewood Cliffs (NJ): Prentice-Hall Inc.
28. Kvitek DJ, Sherlock G. 2013. Whole genome, whole population sequencing reveals that loss of signaling networks is the major adaptive strategy in a constant environment. PLoS Genet. 9: e1003972-3972.
29. Lang GI, et al. 2013. Pervasive genetic hitchhiking and clonal interference in forty evolving yeast populations. Nature 500:571-574.
30. Levert M, et al. 2010. Molecular and evolutionary bases of within-patient genotypic and phenotypic diversity in Escherichia coli extraintestinal infections. PLoS Pathog. 6:e1001125.
31. Li H, Durbin R. 2009. Fast and accurate short read alignment with burrows- wheeler transform. Bioinformatics 25:1754-1760.
32. Li H, et al. 2009. The Sequence Alignment/Map format and SAMtools. Bioinformatics 25:2078-2079.
33. Maharjan R, et al. 2010. Genomic identification of a novel mutation in hfq that provides multiple benefits in evolving glucose-limited populations of Escherichia coli. J Bacteriol. 192:4517-4521.
34. Maharjan R, et al. 2012. The multiplicity of divergence mechanisms in a single evolving population. Genome Biol. 13:R41.
35. Maharjan R, McKenzie C, Yeung A, Ferenci T. 2013. The basis of antagonistic pleiotropy in hfq mutations that have opposite effects on fitness at slow and fast growth rates. Heredity 110:10-18.
36. Maharjan R, Nilsson S, et al. 2013. The form of a trade-off determines the response to competition. Ecol Lett. 16:1267-1276.
37. Maharjan R, Seeto S, Notley-McRobb L, Ferenci T. 2006. Clonal adaptive radiation in a constant environment. Science 313:514-517.
38. Maharjan RP, Ferenci T. 2013. Epistatic interactions determine the mutational pathways and coexistence of lineages in clonal Escherichia coli populations. Evolution 67:2762-2768.
39. Maharjan RP, Yu PL, Seeto S, Ferenci T. 2005. The role of isocitrate lyase and the glyoxylate cycle in Escherichia coli growing under glucose limitation. Res Microbiol. 156:178-183.
40. Messer PW, Petrov DA. 2013. Population genomics of rapid adaptation by soft selective sweeps. Trends Ecol Evol. 28:659-669.
41. Misra R, Peterson A, Ferenci T, Silhavy TJ. 1991. A genetic approach for analyzing the pathway of LamB assembly into the outer membrane of Escherichia coli. J Biol Chem. 266:13592-13597.
42. Notley L, Ferenci T. 1995. Differential expression of mal genes under cAMP and endogenous inducer control in nutrient stressed Escherichia coli. Mol Microbiol. 16:121-129.
43. Notley-McRobb L, Ferenci T. 1999a. Adaptive mgl-regulatory mutations and genetic diversity evolving in glucose-limited Escherichia coli populations. Environ Microbiol. 1:33-43.
44. Notley-McRobb L, Ferenci T. 1999b. The generation of multiple coexisting mal-regulatory mutations through polygenic evolution in glucose- limited populations of Escherichia coli. Environ Microbiol. 1:45-52.
45. Notley-McRobb L, Ferenci T. 2000. Experimental analysis of molecular events during mutational periodic selections in bacterial evolution. Genetics 156:1493-1501.
46. 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. J Bacteriol. 184:806-811.
47. Notley-McRobb L, Seeto S, Ferenci T. 2002. Enrichment and elimination of mutY mutators in Escherichia coli populations. Genetics 162: 1055-1062.
48. Notley-McRobb L, Seeto S, Ferenci T. 2003. The influence of cellular physiology on the initiation of mutational pathways in Escherichia coli populations. Proc Natl Acad Sci U S A. 270:843-848.
49. Pennings PS, Hermisson J. 2006. Soft Sweeps II - molecular population genetics of adaptation from recurrent mutation or migration. Mol Biol Evol. 23:1076-1084.
50. Phan K, Ferenci T. 2013. A design-constraint trade-off underpins the diversity in ecologically important traits in species Escherichia coli. ISME J. 7:2034-2043.
51. Rosenzweig RF, Adams J. 1994. Microbial adaptation to a changeable environment: cell-cell interactions mediate physiological and genetic differentiation. Bioessays 16:715-717.
52. Tomar A, Eiteman MA, Altman E. 2003. The effect of acetate pathway mutations on the production of pyruvate in Escherichia coli. Appl Microbiol Biotechnol. 62:76-82.
53. Wang L, et al. 2010. Divergence involving global regulatory gene mutations in an Escherichia coli population evolving under phosphate limitation. Genome Biol Evol. 2:478-487.
54. Ye K, Schulz MH, Long Q, Apweiler R, Ning Z. 2009. Pindel: a pattern growth approach to detect break points of large deletions and medium sized insertions from paired-end short reads. Bioinformatics 25:2865-2871.