Fast growth increases the selective advantage of a mutation arising recurrently during evolution under metal limitation

PLoS Genetics

Volumn 5, Issue 9, 2009, Pages

  Chou, Hsin Hung ^a   Berthet, Julia ^a,b   Marx, Christopher J ^a  

^a HARVARD UNIVERSITY   (United States)

^b SWARTHMORE COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARBON; COBALT; CYANOCOBALAMIN; METAL; METHANOL; SUCCINIC ACID; ACYL COENZYME A; CHELATING AGENT; EDETIC ACID; ETHYLMALONYL COENZYME A; ETHYLMALONYL-COENZYME A;

ANIMAL CELL; ARTICLE; CARBON METABOLISM; CONTROLLED STUDY; GENE; GENE MUTATION; GENETIC VARIABILITY; GENOTYPE ENVIRONMENT INTERACTION; GROWTH RATE; ICUAB GENE; INCUBATION TIME; METHYLOBACTERIUM EXTORQUENS; METHYLOBACTERIUM EXTORQUENS AM1; MOLECULAR EVOLUTION; MOLECULAR MECHANICS; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYTOPLANKTON; ALLELE; BACTERIAL GENE; CONFORMATION; CULTURE MEDIUM; DRUG EFFECT; EVOLUTION; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MOLECULAR GENETICS; MUTATION; PHENOTYPE; PROMOTER REGION; TRANSPOSON;

METHYLOBACTERIUM EXTORQUENS;

ACYL COENZYME A; ALLELES; BASE SEQUENCE; CARBON; CHELATING AGENTS; COBALT; CULTURE MEDIA; DNA TRANSPOSABLE ELEMENTS; EDETIC ACID; EVOLUTION; GENE EXPRESSION REGULATION, BACTERIAL; GENES, BACTERIAL; METALS; METHANOL; METHYLOBACTERIUM EXTORQUENS; MOLECULAR SEQUENCE DATA; MUTAGENESIS, INSERTIONAL; MUTATION; NUCLEIC ACID CONFORMATION; PHENOTYPE; PROMOTER REGIONS, GENETIC; TRANSCRIPTION, GENETIC;

EID: 70349690200     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1000652     Document Type: Article

References (80)

1. Colosimo PF, Hosemann KE, Balabhadra S, Villarreal G Jr, Dickson M, et al. (2005) Widespread parallel evolution in sticklebacks by repeated fixation of Ectodysplasin alleles. Science 307: 1928-1933. (Pubitemid 40404697)
2. Bradshaw HD, Schemske DW (2003) Allele substitution at a flower colour locus produces a pollinator shift in monkeyflowers. Nature 426: 176-178.
3. Herring CD, Raghunathan A, Honisch C, Patel T, Applebee MK, et al. (2006) Comparative genome sequencing of Escherichia coli allows observation of bacterial evolution on a laboratory timescale. Nat Genet 38: 1406-1412. (Pubitemid 44837562)
4. Burch CL, Chao L (1999) Evolution by small steps and rugged landscapes in the RNA virus Q6. Genetics 151: 921-927.
5. Sanjuan R, Elena SF (2006) Epistasis correlates to genomic complexity. Proc Natl Acad Sci U S A 103: 14402-14405.
6. Weinreich DM, Delaney NF, Depristo MA, Hartl DL (2006) Darwinian evolution can follow only very few mutational paths to fitter proteins. Science 312: 111-114.
7. Jasnos L, Korona R (2007) Epistatic buffering of fitness loss in yeast double deletion strains. Nat Genet 39: 550-554. (Pubitemid 46514769)
8. Bjorkman J, Nagaev I, Berg OG, Hughes D, Andersson DI (2000) Effects of environment on compensatory mutations to ameliorate costs of antibiotic resistance. Science 287: 1479-1482. (Pubitemid 30127140)
9. Ostrowski EA, Rozen DE, Lenski RE (2005) Pleiotropic effects of beneficial mutations in Escherichia coli. Evolution 59: 2343-2352. (Pubitemid 41752648)
10. Manch K, Notley-McRobb L, Ferenci T (1999) Mutational adaptation of Escherichia coli to glucose limitation involves distinct evolutionary pathways in aerobic and oxygen-limited environments. Genetics 153: 5-12. (Pubitemid 29434763)
11. 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.
12. Applebee MK, Herrgard MJ, Palsson BO (2008) Impact of individual mutations on increased fitness in adaptively evolved strains of Escherichia coli. J Bacteriol 190: 5087-5094.
13. Fiegna F, Yu YT, Kadam SV, Velicer GJ (2006) Evolution of an obligate social cheater to a superior cooperator. Nature 441: 310-314. (Pubitemid 44050190)
14. Elena SF, Lenski RE (2003) Evolution experiments with microorganisms: the dynamics and genetic bases of adaptation. Nat Rev Genet 4: 457-469.
15. Zhong SB, Khodursky A, Dykhuizen DE, Dean AM (2004) Evolutionary genomics of ecological specialization. Proc Natl Acad Sci USA 101: 11719-11724.
16. Brown CJ, Todd KM, Rosenzweig RF (1998) Multiple duplications of yeast hexose transport genes in response to selection in a glucose-limited environment. Mol Biol Evol 15: 931-942.
17. Wood TE, Burke JM, Rieseberg LH (2005) Parallel genotypic adaptation: when evolution repeats itself. Genetica 123: 157-170.
18. Stern DL, Orgogozo V (2009) Is genetic evolution predictable? Science 323: 746-751.
19. Yu FH, Yarov-Yarovoy V, Gutman GA, Catterall WA (2005) Overview of molecular relationships in the voltage-gated ion channel superfamily. Pharmacol Rev 57: 387-395. (Pubitemid 43036430)
20. Voet D, Voet J (2004) Metal ion catalysis. In: Biochemistry. Hoboken: John Wiley & Sons, Inc. pp 501-503.
21. Stumm W, Morgan JJ (1996) Metal ions in aqueous solution: aspects of coordination chemistry. In: Aquatic chemistry: chemical equilibria and rates in natural waters. New York: John Wiley & Sons, Inc. pp 252-348.
22. Hayes KF, Traina SJ (1998) Metal ion speciation and its significance in ecosystem health. In: Huang PM, Adriano DC, Logan TJ, Checkai RT, eds. Soil chemistry and ecosystem health. Madison: Soil Science Society of America, Inc. pp 45-84.
23. Morel FMM, Hudson RJM, Price NM (1991) Limitation of productivity by trace metals in the sea. Limnol Oceanogr 36: 1742-1755.
24. Vlek PLG (1985) Micronutrients in tropical food crop production. Dordrecht: Martinus Nijhoff/Dr W. Junk Publishers. 260 p.
25. Otto BR, Verweij-van Vught AM, MacLaren DM (1992) Transferrins and heme-compounds as iron sources for pathogenic bacteria. Crit Rev Microbiol 18: 217-233.
26. Expert D (1999) Withholding and exchanging iron: interactions between Erwinia spp. and their plant hosts. Annu Rev Phytopathol 37: 307-334.
27. Haas H, Eisendle M, Turgeon BG (2008) Siderophores in fungal physiology and virulence. Annu Rev Phytopathol 46: 149-187.
28. Ferguson AD, Deisenhofer J (2004) Metal import through microbial membranes. Cell 116: 15-24.
29. O'Halloran TV (1993) Transition metals in control of gene expression. Science 261: 715-725. (Pubitemid 23278386)
30. Chistoserdova L, Chen SW, Lapidus A, Lidstrom ME (2003) Methylotrophy in Methylobacterium extorquens AM1 from a genomic point of view. J Bacteriol 185: 2980-2987. (Pubitemid 36539093)
31. Okubo Y, Skovran E, Guo X, Sivam D, Lidstrom ME (2007) Implementation of microarrays for Methylobacterium extorquens AM1. OMICS 11: 325-340. (Pubitemid 350293821)
32. Van Dien SJ, Strovas T, Lidstrom ME (2003) Quantification of central metabolic fluxes in the facultative methylotroph Methylobacterium extorquens AM1 using 13C-label tracing and mass spectrometry. Biotech Bioeng 84: 45-55. (Pubitemid 37075619)
33. Guo X, Lidstrom ME (2006) Physiological analysis of Methylobacterium extorquens AM1 grown in continuous and batch cultures. Arch Microbiol 186: 139-149. (Pubitemid 44127154)
34. Kiefer P, Portais JC, Vorholt JA (2008) Quantitative metabolome analysis using liquid chromatography-high-resolution mass spectrometry. Anal Biochem 382: 94-100.
35. Lee MC, Chou HH, Marx CJ (2009) Asymmetric, bi-modal tradeoffs during adaptation of Methylobacterium to distinct growth substrates. Evolution. In press. doi:10.1111/j.1558-5646.2009.00757.x.
36. Marx CJ, Chistoserdova L, Lidstrom ME (2003) Formaldehyde-detoxifying role of the tetrahydromethanopterin-linked pathway in Methylobacterium extorquens AM1. J Bacteriol 185: 7160-7168. (Pubitemid 37509832)
37. Marchler-Bauer A, Bryant SH (2004) CD-Search: protein domain annotations on the fly. Nucleic Acids Res 32: W327-W331. (Pubitemid 38997352)
38. Mahillon J, Chandler M (1998) Insertion sequences. Microbiol Mol Biol Rev 62: 725-774.
39. Vuilleumier S, Chistoserdova L, Lee MC, 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.
40. Crooks GE, Hon G, Chandonia JM, Brenner SE (2004) WebLogo: a sequence logo generator. Genome Res 14: 1188-1190.
41. Zuker M (2003) Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res 31: 3406-3415.
42. Domingo JL (1998) Developmental toxicity of metal chelating agents. Reprod Toxicol 12: 499-510.
43. Laurie SH, Tancock NP, Mcgrath SP, Sanders JR (1991) Influence of complexation on the uptake by plants of iron, manganese, copper and zinc. 1. Effect of EDTA in a multi-metal and computer-simulation study. J Exp Bot 42: 509-513.
44. Sunda W, Huntsman S (2003) Effect of pH, light, and temperature on Fe-EDTA chelation and Fe hydrolysis in seawater. Mar Chem 84: 35-47. (Pubitemid 37545900)
45. Korotkova N, Chistoserdova L, Kuksa V, Lidstrom ME (2002) Glyoxylate regeneration pathway in the methylotroph Methylobacterium extorquens AM1. J Bacteriol 184: 1750-1758. (Pubitemid 34188227)
46. Korotkova N, Lidstrom ME (2004) MeaB is a component of the methylmalonyl-CoA mutase complex required for protection of the enzyme from inactivation. J Biol Chem 279: 13652-13658. (Pubitemid 38468893)
47. 2-units involving crotonyl-CoA carboxylase/reductase: the ethylmalonyl-CoA pathway. Proc Natl Acad Sci USA 104: 10631-10636.
48. Chistoserdova LV, Lidstrom ME (1996) Molecular characterization of a chromosomal region involved in the oxidation of acetyl-CoA to glyoxylate in the isocitrate-lyase-negative methylotroph Methylobacterium extorquens AM1. Microbiology 142: 1459-1468.
49. 2 compounds in the methylotroph Methylobacterium extorquens AM1. J Bacteriol 183: 1038-1046.
50. Zhang M, Lidstrom ME (2003) Promoters and transcripts for genes involved in methanol oxidation in Methylobacterium extorquens AM 1. Microbiology 149: 1033-1040. (Pubitemid 36553372)
51. Marx CJ, Lidstrom ME (2001) Development of improved versatile broad-hostrange vectors for use in methylotrophs and other Gram-negative bacteria. Microbiology 147: 2065-2075. (Pubitemid 32785488)
52. Wagner S, Baars L, Ytterberg AJ, Klussmeier A, Wagner CS, et al. (2007) Consequences of membrane protein overexpression in Escherichia coli. Mol Cell Proteomics 6: 1527-1550. (Pubitemid 47506165)
53. Weinreich DM, Watson RA, Chao L (2005) Perspective: Sign epistasis and genetic constraint on evolutionary trajectories. Evolution 59: 1165-1174.
54. Tiffany ME, Fellner V, Spears JW (2006) Influence of cobalt concentration on vitamin B12 production and fermentation of mixed ruminal microorganisms grown in continuous culture flow-through fermentors. J Anim Sci 84: 635-640. (Pubitemid 44405677)
55. Rao SS, Washington DR (1964) Influence of cobalt on Propionibacterium freudenreichii. Nature 202: 212-213.
56. 12 production by Pseudomonas denitrificans. Can J Microbiol 16: 809-815.
57. Mertz W (1987) Trace elements in human and animal. San Diego: Academic Press, Inc. 480 p.
58. 12 synthesis in the North Atlantic Ocean. Global Biogeochem Cycles 22: GB2029.
59. 12. Nat Chem Biol 4: 194-196.
60. Knief C, Frances L, Cantet F, Vorholt JA (2008) Cultivation-independent characterization of methylobacterium populations in the plant phyllosphere by automated ribosomal intergenic spacer analysis. Appl Environ Microbiol 74: 2218-2228.
61. Sy A, Timmers AC, Knief C, Vorholt JA (2005) Methylotrophic metabolism is advantageous for Methylobacterium extorquens during colonization of Medicago truncatula under competitive conditions. Appl Environ Microbiol 71: 7245-7252. (Pubitemid 43194218)
62. Kabata-Pendias A, Pendias H (1984) Cobalt. In: Trace elements in soils and plants. Boca Raton: CRC Press, Inc. pp 239-246.
63. Sy A, Giraud E, Jourand P, Garcia N, Willems A, et al. (2001) Methylotrophic Methylobacterium bacteria nodulate and fix nitrogen in symbiosis with legumes. J Bacteriol 183: 214-220. (Pubitemid 32003126)
64. Hewitt EJ, Bond G (1966) The cobalt requirement of non-legume root nodule plants. J Exp Bot 17: 480-491.
65. Kobayashi M, Suzuki T, Fujita T, Masuda M, Shimizu S (1995) Occurrence of enzymes Involved in biosynthesis of indole-3-acetic-acid from indole-3-acetonitrile in plant-associated bacteria, Agrobacterium and Rhizobium. Proc Natl Acad Sci USA 92: 714-718.
66. 12: Catalysis by cobalamin-dependent enzymes. Annual Review of Biochemistry 72: 209-247.
67. Saito MA, Moffett JW, Chisholm SW, Waterbury JB (2002) Cobalt limitation and uptake in Prochlorococcus. Limnol Oceanogr 47: 1629-1636.
68. Saito MA, Rocap G, Moffett JW (2005) Production of cobalt binding ligands in a Synechococcus feature at the Costa Rica upwelling dome. Limnol Oceanogr 50: 279-290. (Pubitemid 40199048)
69. Craig NL (1997) Target site selection in transposition. Annu Rev Biochem 66: 437-474.
70. Jasnos L, Tomala K, Paczesniak D, Korona R (2008) Interactions between stressful environment and gene deletions alleviate the expected average loss of fitness in yeast. Genetics 178: 2105-2111.
71. Kishony R, Leibler S (2003) Environmental stress can alleviate the average deleterious effect of mutations. J Biol 2: 14. (Pubitemid 36992713)
72. Marx CJ (2008) Development of a broad-host-range sacB-based vector for unmarked allelic exchange. BMC Res Notes 1: 1.
73. Zhang M, FitzGerald KA, Lidstrom ME (2005) Identification of an upstream regulatory sequence that mediates the transcription of mox genes in Methylobacterium extorquens AM1. Microbiology 151: 3723-3728. (Pubitemid 41632082)
74. Vorholt JA, Marx CJ, Lidstrom ME, Thauer RK (2000) Novel formaldehyde-activating enzyme in Methylobacterium extorquens AM1 required for growth on methanol. J Bacteriol 182: 6645-6650.
75. cott JW, Rasche ME (2002) Purification, overproduction, and partial characterization of β-RFAP synthase, a key enzyme in the methanopterin biosynthesis pathway. J Bacteriol 184: 4442-4448.
76. Chistoserdov AY, Chistoserdova LV, McIntire WS, Lidstrom ME (1994) Genetic organization of the mau gene cluster in Methylobacterium extorquens AM1: complete nucleotide sequence and generation and characteristics of mau mutants. J Bacteriol 176: 4052-4065.
77. Palumbo AV, Lee SY, Boerman P (1994) The effect of media composition on EDTA degradation by Agrobacterium sp. Appl Biochem Biotechnol 45-46: 811-822.
78. Giraud A, Arous S, De PM, Gaboriau-Routhiau V, Bambou JC, et al. (2008) Dissecting the genetic components of adaptation of Escherichia coli to the mouse gut. PLoS Genet 4: e2. doi:10.1371/journal.pgen.0040002. (Pubitemid 351230873)
79. Lee CL, Ow DS, Oh SK (2006) Quantitative real-time polymerase chain reaction for determination of plasmid copy number in bacteria. J Microbiol Methods 65: 258-267. (Pubitemid 43670487)
80. Crameri A, Whitehorn EA, Tate E, Stemmer WP (1996) Improved green fluorescent protein by molecular evolution using DNA shuffling. Nat Biotechnol 14: 315-319. (Pubitemid 26150145)