Evolution after Introduction of a Novel Metabolic Pathway Consistently Leads to Restoration of Wild-Type Physiology

PLoS Genetics

Volumn 9, Issue 4, 2013, Pages

  Carroll, Sean Michael ^a   Marx, Christopher J ^a,b  

^a HARVARD UNIVERSITY   (United States)

^b HARVARD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACCLIMATIZATION; ARTICLE; BACTERIAL STRAIN; BIOENGINEERING; CONTROLLED STUDY; EVOLUTIONARY ADAPTATION; GENE; GENE EXPRESSION; GENE MUTATION; GENE REPLICATION; GROWTH RATE; METABOLISM; METHYLOBACTERIUM EXTORQUENS; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYSIOLOGY; PNTAB GENE; WILD TYPE;

ACCLIMATIZATION; BIOLOGICAL EVOLUTION; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GENE DELETION; GENE EXPRESSION REGULATION, BACTERIAL; METABOLIC NETWORKS AND PATHWAYS; METHYLOBACTERIUM EXTORQUENS; MUTATION; NADP TRANSHYDROGENASES; STRESS, PHYSIOLOGICAL; TRANSCRIPTION, GENETIC;

METHYLOBACTERIUM EXTORQUENS;

EID: 84876838057     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1003427     Document Type: Article

References (48)

1. Cooper TF, Rozen DE, Lenski RE, (2003) Parallel changes in gene expression after 20,000 generations of evolution in Escherichia coli. P Natl Acad Sci Usa 100: 1072-1077 doi:10.1073/pnas.0334340100.
2. Cooper TF, Remold SK, Lenski RE, Schneider D, (2008) Expression profiles reveal parallel evolution of epistatic interactions involving the CRP regulon in Escherichia coli. PLoS Genet 4: e35 doi:10.1371/journal.pgen.0040035.
3. Gresham D, Desai MM, Tucker CM, Jenq HT, Pai DA, et al. (2008) The repertoire and dynamics of evolutionary adaptations to controlled nutrient-limited environments in yeast. PLoS Genet 4: e1000303 doi:10.1371/journal.pgen.1000303.
4. McDonald MJ, Gehrig SM, Meintjes PL, Zhang X-X, Rainey PB, (2009) Adaptive divergence in experimental populations of Pseudomonas fluorescens. IV. Genetic constraints guide evolutionary trajectories in a parallel adaptive radiation. Genetics 183: 1041-1053 doi:10.1534/genetics.109.107110.
5. Kvitek DJ, Sherlock G, (2011) Reciprocal sign epistasis between frequently experimentally evolved adaptive mutations causes a rugged fitness landscape. PLoS Genet 7: e1002056 doi:10.1371/journal.pgen.1002056.
6. Toprak E, Veres A, Michel J-B, Chait R, Hartl DL, et al. (2012) Evolutionary paths to antibiotic resistance under dynamically sustained drug selection. Nat Genet 44: 101-105 doi:10.1038/ng.1034.
7. Maharjan R, Seeto S, Notley-McRobb L, Ferenci T, (2006) Clonal adaptive radiation in a constant environment. Science 313: 514-517 doi:10.1126/science.1129865.
8. Woods R, Schneider D, Winkworth CL, Riley MA, Lenski RE, (2006) Tests of parallel molecular evolution in a long-term experiment with Escherichia coli. P Natl Acad Sci Usa 103: 9107-9112 doi:10.1073/pnas.0602917103.
9. Wood TE, Burke JM, Rieseberg LH, (2005) Parallel genotypic adaptation: when evolution repeats itself. Genetica 123: 157-170.
10. Chou H-H, Berthet J, Marx CJ, (2009) Fast growth increases the selective advantage of a mutation arising recurrently during evolution under metal limitation. PLoS Genet 5: e1000652 doi:10.1371/journal.pgen.1000652.
11. Cooper VS, Lenski RE, (2000) The population genetics of ecological specialization in evolving Escherichia coli populations. Nature 407: 736-739 doi:10.1038/35037572.
12. Fong SS, Joyce AR, Palsson BØ, (2005) Parallel adaptive evolution cultures of Escherichia coli lead to convergent growth phenotypes with different gene expression states. Genome Res 15: 1365-1372 doi:10.1101/gr.3832305.
13. Peel D, Quayle J, (1961) Microbial growth on C1 compounds. I. Isolation and characterization of Pseudomonas AM 1. Biochem J 81: 465-469.
14. Chistoserdova L, Chen S-W, Lapidus A, Lidstrom ME, (2003) Methylotrophy in Methylobacterium extorquens AM1 from a genomic point of view. J Bacteriol 185: 2980-2987.
15. Chistoserdova L, Vorholt JA, Thauer RK, Lidstrom ME, (1998) C1 transfer enzymes and coenzymes linking methylotrophic bacteria and methanogenic Archaea. Science 281: 99-102.
16. Vorholt JA, Chistoserdova L, Stolyar SM, Thauer RK, Lidstrom ME, (1999) Distribution of tetrahydromethanopterin-dependent enzymes in methylotrophic bacteria and phylogeny of methenyl tetrahydromethanopterin cyclohydrolases. J Bacteriol 181: 5750-5757.
17. Marx CJ, Chistoserdova L, Lidstrom ME, (2003) Formaldehyde-detoxifying role of the tetrahydromethanopterin-linked pathway in Methylobacterium extorquens AM1. J Bacteriol 185: 7160-7168.
18. Marx CJ, Van Dien SJ, Lidstrom ME, (2005) Flux analysis uncovers key role of functional redundancy in formaldehyde metabolism. PLoS Biol 3: e16 doi:10.1371/journal.pbio.0030016.
19. Crowther GJ, Kosály G, Lidstrom ME, (2008) Formate as the main branch point for methylotrophic metabolism in Methylobacterium extorquens AM1. J Bacteriol 190: 5057-5062 doi:10.1128/JB.00228-08.
20. Chou H-H, Chiu H-C, Delaney NF, Segrè D, Marx CJ, (2011) Diminishing returns epistasis among beneficial mutations decelerates adaptation. Science 332: 1190-1192 doi:10.1126/science.1203799.
21. Sauer U, Canonaco F, Heri S, Perrenoud A, Fischer E, (2004) The soluble and membrane-bound transhydrogenases UdhA and PntAB have divergent functions in NADPH metabolism of Escherichia coli. J Biol Chem 279: 6613-6619 doi:10.1074/jbc.M311657200.
22. Masip L, Veeravalli K, Georgiou G, (2006) The many faces of glutathione in bacteria. Antioxid Redox Signal 8: 753-762 doi:10.1089/ars.2006.8.753.
23. Chou H-H, Marx CJ (2012) Optimization of gene expression through divergent mutational paths. Cell Reports: 1-15. doi:10.1016/j.celrep.2011.12.003.
24. Park C, Zhang J, (2012) High expression hampers horizontal gene transfer. Genome Biol Evol 4: 523-532 doi:10.1093/gbe/evs030.
25. Dekel E, Alon U, (2005) Optimality and evolutionary tuning of the expression level of a protein. Nature 436: 588-592 doi:10.1038/nature03842.
26. Delaney NF, Rojas Echenique JI, Marx CJ, (2012) Clarity: an open-source manager for laboratory automation. J Lab Autom doi:10.1177/2211068212460237.
27. Delaney NF, Kaczmarek ME, Ward LM, Swanson PK, Lee MC, et al. (n.d.) Development of an optimized medium, strain and high-throughput culturing methods for Methylobacterium extorquens. Submitted.
28. Delaney NF, Kaczmarek ME, Marx CJ, (n.d.) Evaluating sources of bias when estimating microbial growth rates in microtiter plates and development of the open-source program Curve Fitter. Submitted.
29. Lee M-C, Chou H-H, Marx CJ, (2009) Asymmetric, bimodal trade-offs during adaptation of Methylobacterium to distinct growth substrates. Evolution 63: 2816-2830 doi:10.1111/j.1558-5646.2009.00757.x.
30. Eady RR, Large PJ, (1968) Purification and properties of an amine dehydrogenase from Pseudomonas AM1 and its role in growth on methylamine. Biochem J 106: 245-255.
31. Vuilleumier S, Chistoserdova L, Lee M-C, Bringel F, Lajus A, et al. (2009) Methylobacterium genome sequences: a reference blueprint to investigate microbial metabolism of C1 compounds from natural and industrial sources. PLoS ONE 4: e5584 doi:10.1371/journal.pone.0005584.t004.
32. Lee M-C, Marx CJ, (2012) Repeated, selection-driven genome reduction of accessory genes in experimental populations. PLoS Genet 8: e1002651 doi:10.1371/journal.pgen.1002651.
33. Kayser A, Weber J, Hecht V, Rinas U, (2005) Metabolic flux analysis of Escherichia coli in glucose-limited continuous culture. I. Growth-rate-dependent metabolic efficiency at steady state. Microbiology (Reading, Engl) 151: 693-706 doi:10.1099/mic.0.27481-0.
34. Lahtvee P-J, Adamberg K, Arike L, Nahku R, Aller K, et al. (2011) Multi-omics approach to study the growth efficiency and amino acid metabolism in Lactococcus lactis at various specific growth rates. Microb Cell Fact 10: 12 doi:10.1186/1475-2859-10-12.
35. Marx CJ, (2012) Recovering from a bad start: rapid adaptation and tradeoffs to growth below a threshold density. BMC Evol Biol 12: 109 doi:10.1186/1471-2148-12-109.
36. Skovran E, Crowther GJ, Guo X, Yang S, Lidstrom ME, (2010) A systems biology approach uncovers cellular strategies used by Methylobacterium extorquens AM1 during the switch from multi- to single-carbon growth. PLoS ONE 5: e14091 doi:10.1371/journal.pone.0014091.
37. Waddington CH, (1953) Genetic assimilation of an acquired character. Evolution pp. 118-126.
38. West-Eberhard MJ (2003) Developmental plasticity and evolution. Oxford, UK: Oxford University Press. 816 p.
39. Braendle C, Flatt T, (2006) A role for genetic accommodation in evolution? Bioessays 28: 868-873 doi:10.1002/bies.20456.
40. Gibson G, Dworkin I, (2004) Uncovering cryptic genetic variation. Nat Rev Genet 5: 681-U11 doi:10.1038/nrg1426.
41. Marx CJ, (2008) Development of a broad-host-range sacB-based vector for unmarked allelic exchange. BMC Res Notes 1: 1 doi:10.1186/1756-0500-1-1.
42. Scott JW, Rasche ME, (2002) Purification, overproduction, and partial characterization of beta-RFAP synthase, a key enzyme in the methanopterin biosynthesis pathway. J Bacteriol 184: 4442-4448.
43. Okubo Y, Skovran E, Guo X, Sivam D, Lidstrom ME, (2007) Implementation of microarrays for Methylobacterium extorquens AM1. OMICS 11: 325-340 doi:10.1089/omi.2007.0027.
44. Smyth GK, (2004) Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol 3: Article3 doi:10.2202/1544-6115.1027.
45. Ritchie ME, Silver J, Oshlack A, Holmes M, Diyagama D, et al. (2007) A comparison of background correction methods for two-colour microarrays. Bioinformatics 23: 2700-2707 doi:10.1093/bioinformatics/btm412.
46. Gentleman RC, Carey VJ, Bates DM, Bolstad B, Dettling M, et al. (2004) Bioconductor: open software development for computational biology and bioinformatics. Genome Biol 5: R80 doi:10.1186/gb-2004-5-10-r80.
47. R Core Team (2012) R: A Language and Environment for Statistical Computing. Vienna, Austria.
48. Thompson LR, Zeng Q, Kelly L, Huang KH, Singer AU, et al. (2011) Phage auxiliary metabolic genes and the redirection of cyanobacterial host carbon metabolism. P Natl Acad Sci Usa 108: E757-E764 doi:10.1073/pnas.1102164108/-/DCSupplemental.