Multiple long-term, experimentally-evolved populations of Escherichia coli acquire dependence upon citrate as an iron chelator for optimal growth on glucose

BMC Evolutionary Biology

Volumn 12, Issue 1, 2012, Pages

  Leiby, Nicholas ^a   Harcombe, William R ^a   Marx, Christopher J ^a,b  

^a HARVARD UNIVERSITY   (United States)

^b HARVARD UNIVERSITY   (United States)

Author keywords

Citrate; Iron limitation; Specialization; Tradeoffs

Indexed keywords

ACCUMULATION; CHELATION; CITRIC ACID; COLIFORM BACTERIUM; GLUCOSE; IRON; SPECIALIZATION; TRADE-OFF;

ESCHERICHIA COLI;

CARBON; CHELATING AGENT; CITRATE SODIUM; CITRIC ACID; GLUCOSE; IRON;

ADAPTATION; ARTICLE; ESCHERICHIA COLI; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MOLECULAR EVOLUTION;

ADAPTATION, PHYSIOLOGICAL; CARBON ISOTOPES; CHELATING AGENTS; CITRATES; ESCHERICHIA COLI; EVOLUTION, MOLECULAR; GLUCOSE; IRON;

EID: 84865287298     PISSN: None     EISSN: 14712148     Source Type: Journal    
DOI: 10.1186/1471-2148-12-151     Document Type: Article

References (38)

1. The evolution of ecological specialization. Futuyma D, Annu Rev Ecol Syst 1988 19 207 233 10.1146/annurev.es.19.110188.001231
2. Optimal life histories under age-specific predation. Law R, Am Nat 1979 114 399 417 10.1086/283488
3. The experimental evolution of specialists, generalists, and the maintenance of diversity. Kassen R, J Evol Biol 2002 15 173 190 10.1046/j.1420-9101.2002.00377.x
4. An experimental test of evolutionary trade-offs during temperature adaptation. Bennett AF, Lenski RE, Proc Natl Acad Sci 2007 104 Suppl 8649 54 10.1073/pnas.0702117104 17494741
5. The population genetics of ecological specialization in evolving Escherichia coli populations. Cooper VS, Lenski RE, Nature 2000 407 736 9 10.1038/35037572 11048718
6. Asymmetric, bimodal trade-offs during adaptation of Methylobacterium to distinct growth substrates. Lee M-C, Chou H-H, Marx CJ, Evolution 2009 63 2816 30 10.1111/j.1558-5646.2009.00757.x 19545267
7. Evolutionary reversals during viral adaptation to alternating hosts. Crill WD, Wichman HA, Bull JJ, Genetics 2000 154 27 37 10628966
8. Laboratory-dependent bacterial ecology: a cautionary tale. O'Keefe KJ, Morales NM, Ernstberger H, Benoit G, Turner PE, Appl Environ Microbiol 2006 72 3032 3035 10.1128/AEM.72.4.3032-3035.2006 16598013
9. Microbial minimalism: genome reduction in bacterial pathogens. Moran NA, Cell 2002 108 583 6 10.1016/S0092-8674(02)00665-7 11893328
10. Costs and benefits of high mutation rates: adaptive evolution of bacteria in the mouse gut. Giraud A, Matic I, Tenaillon O, Clara A, Radman M, Fons M, Taddei F, Science 2001 291 2606 8 10.1126/science.1056421 11283373
11. Long-term experimental evolution in Escherichia coli. I. Adaptation and divergence during 2,000 generations. Lenski RE, Rose MR, Simpson SC, Tadler SC, Am Nat 1991 138 1315 10.1086/285289
12. The isolation of biochemically deficient mutants of bacteria by means of penicillin. Davis B, Proc Natl Acad Sci 1949 35 1 10 10.1073/pnas.35.1.1 16588845
13. Genome evolution and adaptation in a long-term experiment with Escherichia coli. Barrick J, Yu D, Yoon S, Jeong H, Oh T, Nature 2009 461 1243 7 10.1038/nature08480 19838166
14. Experimental tests of the roles of adaptation, chance, and history in evolution. Travisano M, Mongold JA, Bennett AF, Lenski RE, Science 1995 267 87 10.1126/science.7809610 7809610
15. Mechanisms causing rapid and parallel losses of ribose catabolism in evolving populations of Escherichia coli B. Cooper VS, Schneider D, Blot M, Lenski RE, J Bacteriol 2001 183 2834 10.1128/JB.183.9.2834-2841.2001 11292803
16. Pleiotropic effects of beneficial mutations in Escherichia coli. Ostrowski EA, Rozen DE, Lenski RE, Evolution 2005 59 2343 52 16396175
17. Mutants of Escherichia coli requiring methionine or vitamin B12. Davis B, Mingioli E, J Bacteriol 1950 60 17 28 15436457
18. Historical contingency and the evolution of a key innovation in an experimental population of Escherichia coli. Blount ZD, Borland CZ, Lenski RE, Proc Natl Acad Sci 2008 105 7899 906 10.1073/pnas.0803151105 18524956
19. Chromosomal mutation for citrate utilization by Escherichia coli K-12. Hall BG, J Bacteriol 1982 151 269 73 7045076
20. The Escherichia coli citrate carrier CitT: a member of a novel eubacterial transporter family related to the 2-oxoglutarate/malate translocator from spinach chloroplasts. Pos KM, Dimroth P, Bott M, J Bacteriol 1998 180 4160 5 9696764
21. Iron limitation across chlorophyll gradients in the southern Drake Passage: Phytoplankton responses to iron addition and photosynthetic indicators of iron stress. Hopkinson BM, Mitchell BG, Reynolds RA, Wang H, Selph KE, Measures CI, Hewes CD, Holm-Hansen O, Barbeau KA, Limnol Oceanogr 2007 52 2540 2554 10.4319/lo.2007.52.6.2540
22. Cooperation, virulence and siderophore production in bacterial parasites. West SA, Buckling A, Proceedings of the Royal Society: Biological Sciences 2003 270 37 44 10.1098/rspb.2002.2209
23. Molecular mechanism of regulation of siderophore-mediated iron assimilation. Bagg A, Neilands JB, Microbiol Rev 1987 51 509 18 2963952
24. Global iron-dependent gene regulation in Escherichia coli. A new mechanism for iron homeostasis. McHugh JP, Rodríguez-Quinoñes F, Abdul-Tehrani H, Svistunenko DA, Poole RK, Cooper CE, Andrews SC, J Biol Chem 2003 278 29478 86 10.1074/jbc.M303381200 12746439
25. Bacterial solutions to the iron-supply problem. Braun V, Killmann H, Trends in Biochemical Sciences 1999 24 104 9 10.1016/S0968-0004(99)01359-6 10203757
26. Fast growth increases the selective advantage of a mutation arising recurrently during evolution under metal limitation. Chou H-H, Berthet J, Marx CJ, PLoS Genetics 2009 5 1000652 10.1371/journal.pgen.1000652 19763169
27. High relatedness selects against hypermutability in bacterial metapopulations. Harrison F, Buckling A, Proceedings of the Royal Society: Biological Sciences 2007 274 1341 7 10.1098/rspb.2006.0408
28. Study of pyoverdine type and production by Pseudomonas aeruginosa isolated from cystic fibrosis patients: prevalence of type II pyoverdine isolates and accumulation of pyoverdine-negative mutations. De Vos D, De Chial M, Cochez C, Jansen S, Tümmler B, Meyer JM, Cornelis P, Arch Microbiol 2001 175 384 388 10.1007/s002030100278 11409549
29. Cooperation and competition in pathogenic bacteria. Griffin AS, West SA, Buckling A, Nature 2004 430 1024 1027 10.1038/nature02744 15329720
30. Long-term experimental evolution in Escherichia coli. II. Changes in life-history traits during adaptation to a seasonal environment. Vasi F, Travisano M, Lenski RE, Am Nat 1994 144 432 456 10.1086/285685
31. Long-term experimental evolution in Escherichia coli. VIII. Dynamics of a balanced polymorphism. Rozen D, Lenski R, Am Nat 2000 155 24 35 10.1086/303299 10657174
32. Role of siderophore in iron uptake in cowpea Rhizobium GN1 (peanut isolate): Possible involvement of iron repressible outer membrane proteins. Jadhav RS, Desai A, FEMS Microbiol Lett 1994 115 185 190 10.1111/j.1574-6968. 1994.tb06635.x
33. Role of siderophore biosynthesis in virulence of Staphylococcus aureus: Identification and characterization of genes involved in production of a siderophore. Dale S, Doherty-Kirby A, Lajoie G, Heinrichs DE, Infect Immun 2004 72 29 37 10.1128/IAI.72.1.29-37.2004 14688077
34. The EcoCyc database. Karp PD, Riley M, Saier M, Paulsen IT, Collado-Vides J, Paley SM, Pellegrini-Toole A, Bonavides C, Gama-Castro S, Nucleic Acids Res 2002 30 56 8 10.1093/nar/30.1.56 11752253
35. Evolution of high mutation rates in experimental populations of E. coli. Sniegowski PD, Gerrish PJ, Lenski RE, Nature 1997 387 703 705 10.1038/42701 9192894
36. Gene Mutation. Carlton B, Brown B, Manual of Methods for General Bacteriology Washington DC: American Society for Microbiology, Gerhardt P, 1981 222 242
37. Death and cannibalism in a seasonal environment facilitate bacterial coexistence. Rozen DE, Philippe N, de Visser JA, Lenski RE, Schneider D, Ecol Lett 2009 12 34 44 10.1111/j.1461-0248.2008.01257.x 19019196
38. (13)C-based metabolic flux analysis. Zamboni N, Fendt S-M, Rühl M, Sauer U, Nat Protoc 2009 4 878 92 10.1038/nprot.2009.58 19478804