Ex Uno Plures: Clonal Reinforcement Drives Evolution of a Simple Microbial Community

PLoS Genetics

Volumn 10, Issue 6, 2014, Pages

  Kinnersley, Margie ^a   Wenger, Jared ^b   Kroll, Evgueny ^a   Adams, Julian ^c   Sherlock, Gavin ^b   Rosenzweig, Frank ^a  

^a UNIVERSITY OF MONTANA   (United States)

^b STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF MICHIGAN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACETIC ACID; ACETYL COENZYME A; FRUCTOSE 1,6 BISPHOSPHATE; FRUCTOSE 6 PHOSPHATE; GLUCOSE; PYRUVIC ACID; GLYCEROL; STOP CODON;

ARTICLE; CONTROLLED STUDY; DNA SEQUENCE; ESCHERICHIA COLI; GENE MUTATION; GENE SEQUENCE; GENETIC PREDISPOSITION; GENOME ANALYSIS; GLUCOSE TRANSPORT; METABOLITE; MICROBIAL COMMUNITY; MICROBIAL DIVERSITY; MOLECULAR CLONING; MOLECULAR EVOLUTION; MUTATION RATE; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATION REDUCTION STATE; PHENOTYPE; PHYLOGENETIC TREE; SINGLE NUCLEOTIDE POLYMORPHISM; AMINO ACID SUBSTITUTION; BACTERIAL GENOME; DIRECTED MOLECULAR EVOLUTION; GENETIC SELECTION; GENETIC VARIABILITY; GENETICS; METABOLISM; PHYLOGENY; STOP CODON;

AMINO ACID SUBSTITUTION; CODON, NONSENSE; DIRECTED MOLECULAR EVOLUTION; ESCHERICHIA COLI; GENETIC VARIATION; GENOME, BACTERIAL; GLUCOSE; GLYCEROL; PHYLOGENY; POLYMORPHISM, SINGLE NUCLEOTIDE; SELECTION, GENETIC;

EID: 84903464880     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1004430     Document Type: Article

References (149)

1. Muller HJ, (1932) Some genetic aspects of sex. Am Naturalist 66: 118-138.
2. Williams GC (1975) Sex and Evolution. Princeton, NJ: Princeton University Press.
3. Helling RB, Vargas CN, Adams J, (1987) Evolution of Escherichia coli during growth in a constant environment. Genetics 116: 349-358.
4. Ferenci T, (2008) Bacterial physiology, regulation and mutational adaptation in a chemostat environment. Adv Microb Physiol 53: 169-229.
5. Lang GI, Rice DP, Hickman MJ, Sodergren E, Weinstock GM, et al. (2013) Pervasive genetic hitchhiking and clonal interference in forty evolving yeast populations. Nature 500: 571-574.
6. Le Gac M, Brazas MD, Bertrand M, Tyerman JG, Spencer CC, et al. (2008) Metabolic changes associated with adaptive diversification in Escherichia coli. Genetics 178: 1049-1060.
7. Spencer CC, Bertrand M, Travisano M, Doebeli M, (2007) Adaptive diversification in genes that regulate resource use in Escherichia coli. PLoS Genet 3: e15.
8. Rozen DE, Lenski RE, (2000) Long-Term Experimental Evolution in Escherichia coli. VIII. Dynamics of a Balanced Polymorphism. Am Nat 155: 24-35.
9. Turner PE, Souza V, Lenski RE, (1996) Tests of Ecological Mechanisms Promoting the Stable Coexistence of Two Bacterial Genotypes. Ecology 77: 2119-2129.
10. Rainey PB, Travisano M, (1998) Adaptive radiation in a heterogeneous environment. Nature 394: 69-72.
11. Herron MD, Doebeli M, (2013) Parallel evolutionary dynamics of adaptive diversification in Escherichia coli. PLoS Biol 11: e1001490.
12. Zhong S, Khodursky A, Dykhuizen DE, Dean AM, (2004) Evolutionary genomics of ecological specialization. Proc Natl Acad Sci U S A 101: 11719-11724.
13. Rainey PB, Buckling A, Kassen R, Travisano M, (2000) The emergence and maintenance of diversity: insights from experimental bacterial populations. Trends Ecol Evol 15: 243-247.
14. Rosenzweig F, Sherlock G (2011) Through a Glass, Clearly: Experimental Evolution as a Window on Adaptive Genome Evolution. In: Garland JT, Rose MR, editors. EXPERIMENTAL EVOLUTION: Concepts, Methods, and Applications of Selection Experiments: University of California Press.
15. Novak M, Pfeiffer T, Lenski RE, Sauer U, Bonhoeffer S, (2006) Experimental tests for an evolutionary trade-off between growth rate and yield in E. coli. Am Nat 168: 242-251.
16. Le Gac M, Plucain J, Hindre T, Lenski RE, Schneider D, (2012) Ecological and evolutionary dynamics of coexisting lineages during a long-term experiment with Escherichia coli. Proc Natl Acad Sci U S A 109: 9487-9492.
17. Rozen DE, Philippe N, Arjan de Visser J, Lenski RE, Schneider D, (2009) Death and cannibalism in a seasonal environment facilitate bacterial coexistence. Ecol Lett 12: 34-44.
18. Monod J (1942) Recherche sur la croissance des cultures bacteriennes. Paris: Hermann et Cie.
19. Kubitschek HE (1970) Introduction to Research with Continuous Cultures. Englewood Cliffs, N.J: Prentice-Hall.
20. Hutchinson GE (1965) The Ecological Theater and the Evolutionary Play: Yale University Press.
21. Wenger JW, Piotrowski J, Nagarajan S, Chiotti K, Sherlock G, et al. (2011) Hunger artists: yeast adapted to carbon limitation show trade-offs under carbon sufficiency. PLoS Genet 7: e1002202.
22. Kvitek DJ, Sherlock G, (2011) Reciprocal sign epistasis between frequently experimentally evolved adaptive mutations causes a rugged fitness landscape. PLoS Genet 7: e1002056.
23. Novick A, Szilard L, (1950) Experiments with the Chemostat on spontaneous mutations of bacteria. Proc Natl Acad Sci U S A 36: 708-719.
24. Atwood KC, Schneider LK, Ryan FJ, (1951) Periodic Selection in Escherichia coli. Proc Natl Acad Sci U S A 37: 146-155.
25. Kao KC, Sherlock G, (2008) Molecular characterization of clonal interference during adaptive evolution in asexual populations of Saccharomyces cerevisiae. Nat Genet 40: 1499-1504.
26. de Visser JA, Rozen DE, (2006) Clonal interference and the periodic selection of new beneficial mutations in Escherichia coli. Genetics 172: 2093-2100.
27. Gerrish PJ, Lenski RE, (1998) The fate of competing beneficial mutations in an asexual population. Genetica 102-103: 127-144.
28. Boucher DH, ed. (1985) The Biology of Mutualism. NY: Oxford University Press.
29. Thompson JN (2005) The geographic mosaic of coevolution. Chicago, Illinois: University of Chicago Press.
30. Kinnersley MA, Holben WE, Rosenzweig F, (2009) E Unibus Plurum: genomic analysis of an experimentally evolved polymorphism in Escherichia coli. PLoS Genet 5: e1000713.
31. Rosenzweig RF, Sharp RR, Treves DS, Adams J, (1994) Microbial evolution in a simple unstructured environment: genetic differentiation in Escherichia coli. Genetics 137: 903-917.
32. Barrick JE, Yu DS, Yoon SH, Jeong H, Oh TK, et al. (2009) Genome evolution and adaptation in a long-term experiment with Escherichia coli. Nature 461: 1243-1247.
33. Nghiem Y, Cabrera M, Cupples CG, Miller JH, (1988) The mutY gene: a mutator locus in Escherichia coli that generates G.C----T.A transversions. Proc Natl Acad Sci U S A 85: 2709-2713.
34. Ferenci T, (2003) What is driving the acquisition of mutS and rpoS polymorphisms in Escherichia coli? Trends Microbiol 11: 457-461.
35. Notley-McRobb L, Ferenci T, (1999) The generation of multiple co-existing mal-regulatory mutations through polygenic evolution in glucose-limited populations of Escherichia coli. Environ Microbiol 1: 45-52.
36. Treves DS, Manning S, Adams J, (1998) Repeated evolution of an acetate-crossfeeding polymorphism in long-term populations of Escherichia coli. Mol Biol Evol 15: 789-797.
37. Maharjan RP, Gaffe J, Plucain J, Schliep M, Wang L, et al. (2013) A case of adaptation through a mutation in a tandem duplication during experimental evolution in Escherichia coli. BMC Genomics 14: 441.
38. Maharjan R, Seeto S, Notley-McRobb L, Ferenci T, (2006) Clonal adaptive radiation in a constant environment. Science 313: 514-517.
39. Lin JC, Singh RR, Cox DL, (2008) Theoretical study of DNA damage recognition via electron transfer from the [4Fe-4S] complex of MutY. Biophysical journal 95: 3259-3268.
40. 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.
41. Notley-McRobb L, Pinto R, Seeto S, Ferenci T, (2002) Regulation of mutY and nature of mutator mutations in Escherichia coli populations under nutrient limitation. J Bacteriol 184: 739-745.
42. Cox EC, (1976) Bacterial mutator genes and the control of spontaneous mutation. Annu Rev Genet 10: 135-156.
43. Cox EC, Gibson TC, (1974) Selection for high mutation rates in chemostats. Genetics 77: 169-184.
44. Desai MM, Fisher DS, (2011) The balance between mutators and nonmutators in asexual populations. Genetics 188: 997-1014.
45. Gibson TC, Scheppe ML, Cox EC, (1970) Fitness of an Escherichia coli mutator gene. Science 169: 686-688.
46. de Visser JA, (2002) The fate of microbial mutators. Microbiology 148: 1247-1252.
47. Maharjan RP, Liu B, Li Y, Reeves PR, Wang L, et al. (2013) Mutation accumulation and fitness in mutator subpopulations of Escherichia coli. Biol Lett 9: 20120961.
48. Maloy SR, Stewart VJ, Taylor RK (1996) Genetic analysis of pathogenic bacteria: A laboratory manual: Cold Spring Harbor Laboratory Press.
49. Raghavan R, Groisman EA, Ochman H, (2011) Genome-wide detection of novel regulatory RNAs in E. coli. Genome Res 21: 1487-1497.
50. Zhang A, Wassarman KM, Rosenow C, Tjaden BC, Storz G, et al. (2003) Global analysis of small RNA and mRNA targets of Hfq. Mol Microbiol 50: 1111-1124.
51. Kurlandzka A, Rosenzweig RF, Adams J, (1991) Identification of adaptive changes in an evolving population of Escherichia coli: the role of changes with regulatory and highly pleiotropic effects. Mol Biol Evol 8: 261-281.
52. Notley-McRobb L, Ferenci T, (1999) Adaptive mgl-regulatory mutations and genetic diversity evolving in glucose-limited Escherichia coli populations. Environ Microbiol 1: 33-43.
53. Joly N, Bohm A, Boos W, Richet E, (2004) MalK, the ATP-binding cassette component of the Escherichia coli maltodextrin transporter, inhibits the transcriptional activator malt by antagonizing inducer binding. J Biol Chem 279: 33123-33130.
54. Kuhnau S, Reyes M, Sievertsen A, Shuman HA, Boos W, (1991) The activities of the Escherichia coli MalK protein in maltose transport, regulation, and inducer exclusion can be separated by mutations. J Bacteriol 173: 2180-2186.
55. Bukau B, Ehrmann M, Boos W, (1986) Osmoregulation of the maltose regulon in Escherichia coli. J Bacteriol 166: 884-891.
56. Bohm A, Diez J, Diederichs K, Welte W, Boos W, (2002) Structural model of MalK, the ABC subunit of the maltose transporter of Escherichia coli: implications for mal gene regulation, inducer exclusion, and subunit assembly. J Biol Chem 277: 3708-3717.
57. 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.
58. Decker K, Peist R, Reidl J, Kossmann M, Brand B, et al. (1993) Maltose and maltotriose can be formed endogenously in Escherichia coli from glucose and glucose-1-phosphate independently of enzymes of the maltose system. J Bacteriol 175: 5655-5665.
59. Raibaud O, Vidal-Ingigliardi D, Richet E, (1989) A complex nucleoprotein structure involved in activation of transcription of two divergent Escherichia coli promoters. J Mol Biol 205: 471-485.
60. Raibaud O, Richet E, (1987) Maltotriose is the inducer of the maltose regulon of Escherichia coli. J Bacteriol 169: 3059-3061.
61. Vogel J, Luisi BF, (2011) Hfq and its constellation of RNA. Nat Rev Microbiol 9: 578-589.
62. Valentin-Hansen P, Eriksen M, Udesen C, (2004) The bacterial Sm-like protein Hfq: a key player in RNA transactions. Mol Microbiol 51: 1525-1533.
63. Sobrero P, Valverde C, (2012) The bacterial protein Hfq: much more than a mere RNA-binding factor. Crit Rev Microbiol 38: 276-299.
64. Muffler A, Fischer D, Hengge-Aronis R, (1996) The RNA-binding protein HF-I, known as a host factor for phage Qbeta RNA replication, is essential for rpoS translation in Escherichia coli. Genes Dev 10: 1143-1151.
65. Seeto S, Notley-McRobb L, Ferenci T, (2004) The multifactorial influences of RpoS, Mlc and cAMP on ptsG expression under glucose-limited and anaerobic conditions. Res Microbiol 155: 211-215.
66. Notley-McRobb L, Seeto S, Ferenci T, (2003) The influence of cellular physiology on the initiation of mutational pathways in Escherichia coli populations. Proc Biol Sci 270: 843-848.
67. Maharjan R, Zhou Z, Ren Y, Li Y, Gaffe J, 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.
68. Maharjan RP, Ferenci T, (2013) Epistatic interactions determine the mutational pathways and coexistence of lineages in clonal Escherichia coli populations. Evolution 67: 2762-2768.
69. Patel HV, Vyas KA, Mattoo RL, Southworth M, Perler FB, et al. (2006) Properties of the C-terminal domain of enzyme I of the Escherichia coli phosphotransferase system. J Biol Chem 281: 17579-17587.
70. Postma PW, Lengeler JW, Jacobson GR, (1993) Phosphoenolpyruvate:carbohydrate phosphotransferase systems of bacteria. Microbiol Rev 57: 543-594.
71. Chauvin F, Fomenkov A, Johnson CR, Roseman S, (1996) The N-terminal domain of Escherichia coli enzyme I of the phosphoenolpyruvate/glycose phosphotransferase system: molecular cloning and characterization. Proc Natl Acad Sci U S A 93: 7028-7031.
72. Seok YJ, Lee BR, Zhu PP, Peterkofsky A, (1996) Importance of the carboxyl-terminal domain of enzyme I of the Escherichia coli phosphoenolpyruvate: sugar phosphotransferase system for phosphoryl donor specificity. Proc Natl Acad Sci U S A 93: 347-351.
73. Teplyakov A, Lim K, Zhu PP, Kapadia G, Chen CC, et al. (2006) Structure of phosphorylated enzyme I, the phosphoenolpyruvate:sugar phosphotransferase system sugar translocation signal protein. Proc Natl Acad Sci U S A 103: 16218-16223.
74. Garcia-Alles LF, Alfonso I, Erni B, (2003) Enzyme I of the phosphotransferase system: induced-fit protonation of the reaction transition state by Cys-502. Biochemistry 42: 4744-4750.
75. Nam TW, Cho SH, Shin D, Kim JH, Jeong JY, et al. (2001) The Escherichia coli glucose transporter enzyme IICB(Glc) recruits the global repressor Mlc. Embo J 20: 491-498.
76. Lee SJ, Boos W, Bouche JP, Plumbridge J, (2000) Signal transduction between a membrane-bound transporter, PtsG, and a soluble transcription factor, Mlc, of Escherichia coli. Embo J 19: 5353-5361.
77. Zeppenfeld T, Larisch C, Lengeler JW, Jahreis K, (2000) Glucose transporter mutants of Escherichia coli K-12 with changes in substrate recognition of IICB(Glc) and induction behavior of the ptsG gene. J Bacteriol 182: 4443-4452.
78. Decker K, Plumbridge J, Boos W, (1998) Negative transcriptional regulation of a positive regulator: the expression of malT, encoding the transcriptional activator of the maltose regulon of Escherichia coli, is negatively controlled by Mlc. Mol Microbiol 27: 381-390.
79. Fox DK, Meadow ND, Roseman S, (1986) Phosphate transfer between acetate kinase and enzyme I of the bacterial phosphotransferase system. J Biol Chem 261: 13498-13503.
80. Ferea TL, Botstein D, Brown PO, Rosenzweig RF, (1999) Systematic changes in gene expression patterns following adaptive evolution in yeast. Proc Natl Acad Sci U S A 96: 9721-9726.
81. Kotlarz D, Garreau H, Buc H, (1975) Regulation of the amount and of the activity of phosphofructokinases and pyruvate kinases in Escherichia coli. Biochim Biophys Acta 381: 257-268.
82. Babul J, (1978) Phosphofructokinases from Escherichia coli. Purification and characterization of the nonallosteric isozyme. J Biol Chem 253: 4350-4355.
83. Nobelmann B, Lengeler JW, (1996) Molecular analysis of the gat genes from Escherichia coli and of their roles in galactitol transport and metabolism. J Bacteriol 178: 6790-6795.
84. Zhong S, Miller SP, Dykhuizen DE, Dean AM, (2009) Transcription, translation, and the evolution of specialists and generalists. Mol Biol Evol 26: 2661-2678.
85. Zhong S, Khodursky A, Dykhuizen DE, Dean AM, (2004) Evolutionary genomics of ecological specialization. Proc Natl Acad Sci U S A 101: 11719-11724.
86. Morita T, Kawamoto H, Mizota T, Inada T, Aiba H, (2004) Enolase in the RNA degradosome plays a crucial role in the rapid decay of glucose transporter mRNA in the response to phosphosugar stress in Escherichia coli. Mol Microbiol 54: 1063-1075.
87. Vanderpool CK, (2007) Physiological consequences of small RNA-mediated regulation of glucose-phosphate stress. Curr Opin Microbiol 10: 146-151.
88. Morita T, Maki K, Aiba H, (2005) RNase E-based ribonucleoprotein complexes: mechanical basis of mRNA destabilization mediated by bacterial noncoding RNAs. Genes Dev 19: 2176-2186.
89. Vanderpool CK, Gottesman S, (2004) Involvement of a novel transcriptional activator and small RNA in post-transcriptional regulation of the glucose phosphoenolpyruvate phosphotransferase system. Mol Microbiol 54: 1076-1089.
90. Ikeda Y, Yagi M, Morita T, Aiba H, (2011) Hfq binding at RhlB-recognition region of RNase E is crucial for the rapid degradation of target mRNAs mediated by sRNAs in Escherichia coli. Mol Microbiol 79: 419-432.
91. Gonidakis S, Finkel SE, Longo VD, (2010) Genome-wide screen identifies Escherichia coli TCA-cycle-related mutants with extended chronological lifespan dependent on acetate metabolism and the hypoxia-inducible transcription factor ArcA. Aging Cell 9: 868-881.
92. Li M, Ho PY, Yao S, Shimizu K, (2006) Effect of lpdA gene knockout on the metabolism in Escherichia coli based on enzyme activities, intracellular metabolite concentrations and metabolic flux analysis by 13C-labeling experiments. J Biotechnol 122: 254-266.
93. Abdel-Hamid AM, Attwood MM, Guest JR, (2001) Pyruvate oxidase contributes to the aerobic growth efficiency of Escherichia coli. Microbiology 147: 1483-1498.
94. Blaschkowski HP, Neuer G, Ludwig-Festl M, Knappe J, (1982) Routes of flavodoxin and ferredoxin reduction in Escherichia coli. CoA-acylating pyruvate: flavodoxin and NADPH: flavodoxin oxidoreductases participating in the activation of pyruvate formate-lyase. Eur J Biochem 123: 563-569.
95. Eremina NS, Yampolskaya TA, Altman IB, Mashko SV, Stoynova NV, (2010) Overexpression of ydbK-encoding Putative Pyruvate Synthase Improves L-valine Production and Aerobic Growth on Ethanol Media by an Escherichia coli Strain Carrying an Oxygen-Resistant Alcohol Dehydrogenase. J Microbial Biochem Technol 2: 077-083.
96. Akhtar MK, Jones PR, (2009) Construction of a synthetic YdbK-dependent pyruvate:H2 pathway in Escherichia coli BL21(DE3). Metab Eng 11: 139-147.
97. Sawers G, Hesslinger C, Muller N, Kaiser M, (1998) The glycyl radical enzyme TdcE can replace pyruvate formate-lyase in glucose fermentation. J Bacteriol 180: 3509-3516.
98. Reizer J, Reizer A, Saier MH Jr, (1995) Novel phosphotransferase system genes revealed by bacterial genome analysis-a gene cluster encoding a unique Enzyme I and the proteins of a fructose-like permease system. Microbiology 141 (Pt 4):: 961-971.
99. Pecher A, Blaschkowski HP, Knappe K, Bock A, (1982) Expression of pyruvate formate-lyase of Escherichia coli from the cloned structural gene. Arch Microbiol 132: 365-371.
100. de Graef MR, Alexeeva S, Snoep JL, Teixeira de Mattos MJ, (1999) The steady-state internal redox state (NADH/NAD) reflects the external redox state and is correlated with catabolic adaptation in Escherichia coli. J Bacteriol 181: 2351-2357.
101. Knappe J, Sawers G, (1990) A radical-chemical route to acetyl-CoA: the anaerobically induced pyruvate formate-lyase system of Escherichia coli. FEMS Microbiol Rev 6: 383-398.
102. Sawers G, Bock A, (1989) Novel transcriptional control of the pyruvate formate-lyase gene: upstream regulatory sequences and multiple promoters regulate anaerobic expression. J Bacteriol 171: 2485-2498.
103. Alexeeva S, de Kort B, Sawers G, Hellingwerf KJ, de Mattos MJ, (2000) Effects of limited aeration and of the ArcAB system on intermediary pyruvate catabolism in Escherichia coli. J Bacteriol 182: 4934-4940.
104. Carlson RP, (2007) Metabolic systems cost-benefit analysis for interpreting network structure and regulation. Bioinformatics 23: 1258-1264.
105. Sawers G, Watson G, (1998) A glycyl radical solution: oxygen-dependent interconversion of pyruvate formate-lyase. Mol Microbiol 29: 945-954.
106. Vemuri GN, Altman E, Sangurdekar DP, Khodursky AB, Eiteman MA, (2006) Overflow metabolism in Escherichia coli during steady-state growth: transcriptional regulation and effect of the redox ratio. Appl Environ Microbiol 72: 3653-3661.
107. Cozzone AJ, El-Mansi M, (2005) Control of isocitrate dehydrogenase catalytic activity by protein phosphorylation in Escherichia coli. J Mol Microbiol Biotechnol 9: 132-146.
108. El-Mansi M, Cozzone AJ, Shiloach J, Eikmanns BJ, (2006) Control of carbon flux through enzymes of central and intermediary metabolism during growth of Escherichia coli on acetate. Curr Opin Microbiol 9: 173-179.
109. el-Mansi EM, Nimmo HG, Holms WH, (1986) Pyruvate metabolism and the phosphorylation state of isocitrate dehydrogenase in Escherichia coli. J Gen Microbiol 132: 797-806.
110. Li M, Yao S, Shimizu K, (2007) Effect of poxB gene knockout on metabolism in Escherichia coli based on growth characteristics and enzyme activities. World Journal of Microbiology and Biotechnology 23: 573-580.
111. Carlson RP, (2009) Decomposition of complex microbial behaviors into resource-based stress responses. Bioinformatics 25: 90-97.
112. Weidner U, Geier S, Ptock A, Friedrich T, Leif H, et al. (1993) The gene locus of the proton-translocating NADH: ubiquinone oxidoreductase in Escherichia coli. Organization of the 14 genes and relationship between the derived proteins and subunits of mitochondrial complex I. J Mol Biol 233: 109-122.
113. Elvin CM, Hardy CM, Rosenberg H, (1985) Pi exchange mediated by the GlpT-dependent sn-glycerol-3-phosphate transport system in Escherichia coli. J Bacteriol 161: 1054-1058.
114. Deutscher J, Francke C, Postma PW, (2006) How phosphotransferase system-related protein phosphorylation regulates carbohydrate metabolism in bacteria. Microbiol Mol Biol Rev 70: 939-1031.
115. Novotny MJ, Frederickson WL, Waygood EB, Saier MH Jr, (1985) Allosteric regulation of glycerol kinase by enzyme IIIglc of the phosphotransferase system in Escherichia coli and Salmonella typhimurium. J Bacteriol 162: 810-816.
116. Zwaig N, Lin EC, (1966) Feedback inhibition of glycerol kinase, a catabolic enzyme in Escherichia coli. Science 153: 755-757.
117. de Boer M, Broekhuizen CP, Postma PW, (1986) Regulation of glycerol kinase by enzyme IIIGlc of the phosphoenolpyruvate:carbohydrate phosphotransferase system. J Bacteriol 167: 393-395.
118. Lin EC, (1976) Glycerol dissimilation and its regulation in bacteria. Annu Rev Microbiol 30: 535-578.
119. Subedi KP, Kim I, Kim J, Min B, Park C, (2008) Role of GldA in dihydroxyacetone and methylglyoxal metabolism of Escherichia coli K12. FEMS Microbiol Lett 279: 180-187.
120. Applebee MK, Joyce AR, Conrad TM, Pettigrew DW, Palsson BO, (2011) Functional and metabolic effects of adaptive glycerol kinase (GLPK) mutants in Escherichia coli. J Biol Chem 286: 23150-23159.
121. Lindner SN, Meiswinkel TM, Panhorst M, Youn JW, Wiefel L, et al. (2012) Glycerol-3-phosphatase of Corynebacterium glutamicum. J Biotechnol 159: 216-224.
122. Rozen DE, Schneider D, Lenski RE, (2005) Long-term experimental evolution in Escherichia coli. XIII. Phylogenetic history of a balanced polymorphism. J Mol Evol 61: 171-180.
123. Levine JM, HilleRisLambers J, (2009) The importance of niches for the maintenance of species diversity. Nature 461: 254-257.
124. Maharjan RP, Ferenci T, Reeves PR, Li Y, Liu B, et al. (2012) The multiplicity of divergence mechanisms in a single evolving population. Genome Biol 13: R41.
125. de Mazancourt C, Schwartz MW, (2010) A resource ratio theory of cooperation. Ecol Lett 13: 349-359.
126. Updegrove TB, Wartell RM, (2011) The influence of Escherichia coli Hfq mutations on RNA binding and sRNA*mRNA duplex formation in rpoS riboregulation. Biochim Biophys Acta 1809: 532-540.
127. Updegrove T, Wilf N, Sun X, Wartell RM, (2008) Effect of Hfq on RprA-rpoS mRNA pairing: Hfq-RNA binding and the influence of the 5′ rpoS mRNA leader region. Biochemistry 47: 11184-11195.
128. Ko YF, Bentley WE, Weigand WA, (1994) A metabolic model of cellular energetics and carbon flux during aerobic Escherichia coli fermentation. Biotechnol Bioeng 43: 847-855.
129. van Hoek MJ, Merks RM, (2012) Redox balance is key to explaining full vs. partial switching to low-yield metabolism. BMC Syst Biol 6: 22.
130. Tempest D, Neijssel O (1987) Growth Yield and Energy Distribution. In: Neidhardt F, editor. Escherichia coli and Salmonella typhimurium Washington DC: American Society for Microbiology. pp. 797-806.
131. Negrete A, Majdalani N, Phue JN, Shiloach J, (2013) Reducing acetate excretion from E. coli K-12 by over-expressing the small RNA SgrS. N Biotechnol 30: 269-273.
132. Kawamoto H, Koide Y, Morita T, Aiba H, (2006) Base-pairing requirement for RNA silencing by a bacterial small RNA and acceleration of duplex formation by Hfq. Mol Microbiol 61: 1013-1022.
133. Piotrowski JS, Nagarajan S, Kroll E, Stanbery A, Chiotti KE, et al. (2012) Different selective pressures lead to different genomic outcomes as newly-formed hybrid yeasts evolve. BMC Evol Biol 12: 46.
134. Gause GF, (1932) Experimental studies on the struggle for existence: 1. Mixed population of two species of yeast. Journal of Experimental Biology 9: 389-402.
135. Hardin G, (1960) The competitive exclusion principle. Science 131: 1292-1297.
136. Crow JF, Kimura K, (1965) Evolution in asexual populations. Am Nat 99: 439-450.
137. Jezequel N, Lagomarsino MC, Heslot F, Thomen P, (2013) Long-term diversity and genome adaptation of Acinetobacter baylyi in a minimal-medium chemostat. Genome Biol Evol 5: 87-97.
138. Morris BE, Henneberger R, Huber H, Moissl-Eichinger C, (2013) Microbial syntrophy: interaction for the common good. FEMS Microbiol Rev 37: 384-406.
139. Seyfried TN, Shelton LM, (2010) Cancer as a metabolic disease. Nutrition & metabolism 7: 7.
140. Vaughan RA, Garcia-Smith R, Trujillo KA, Bisoffi M, (2013) Tumor necrosis factor alpha increases aerobic glycolysis and reduces oxidative metabolism in prostate epithelial cells. Prostate 73: 1538-1546.
141. Ciofu O, Mandsberg LF, Bjarnsholt T, Wassermann T, Hoiby N, (2010) Genetic adaptation of Pseudomonas aeruginosa during chronic lung infection of patients with cystic fibrosis: strong and weak mutators with heterogeneous genetic backgrounds emerge in mucA and/or lasR mutants. Microbiology 156: 1108-1119.
142. Qin X, Zerr DM, McNutt MA, Berry JE, Burns JL, et al. (2012) Pseudomonas aeruginosa syntrophy in chronically colonized airways of cystic fibrosis patients. Antimicrob Agents Chemother 56: 5971-5981.
143. Helling RB, Kinney T, Adams J, (1981) The maintenance of Plasmid-containing organisms in populations of Escherichia coli. J Gen Microbiol 123: 129-141.
144. Sarkar S, Ma WT, Sandri GH, (1992) On fluctuation analysis: a new, simple and efficient method for computing the expected number of mutants. Genetica 85: 173-179.
145. Tusher VG, Tibshirani R, Chu G, (2001) Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci U S A 98: 5116-5121.
146. Syn CK, Swarup S, (2000) A scalable protocol for the isolation of large-sized genomic DNA within an hour from several bacteria. Anal Biochem 278: 86-90.
147. Li H, Durbin R, (2009) Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25: 1754-1760.
148. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, et al. (2009) The Sequence Alignment/Map format and SAMtools. Bioinformatics 25: 2078-2079.
149. Adams J, Kinney T, Thompson S, Rubin L, Helling RB, (1979) Frequency-Dependent Selection for Plasmid-Containing Cells of ESCHERICHIA COLI. Genetics 91: 627-637.