Global gene expression in Escherichia coli K-12 during short-term and long-term adaptation to glucose-limited continuous culture conditions

Microbiology

Volumn 152, Issue 7, 2006, Pages 2111-2127

  Franchini, Alessandro G ^a   Egli, Thomas ^a  

^a SWISS FEDERAL INSTITUTE OF AQUATIC SCIENCE AND TECHNOLOGY   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

CARBON; CITRIC ACID; GALACTOSE; GLUCOSE; GLYOXYLIC ACID; MALTOSE; MESSENGER RNA; PERIPLASMIC BINDING PROTEIN; PROTEOME; TRANSCRIPTOME;

ARTICLE; BACTERIUM CULTURE; BINDING AFFINITY; CARBON SOURCE; CELL GROWTH; CITRIC ACID CYCLE; CONTINUOUS CULTURE; CONTROLLED STUDY; DILUTION; ESCHERICHIA COLI K 12; EVOLUTIONARY ADAPTATION; GENE EXPRESSION; GENE NUMBER; GENE TECHNOLOGY; GENETIC CODE; MICROARRAY ANALYSIS; NONHUMAN; NUTRIENT SUPPLY; OPERON; PRIORITY JOURNAL; PROTEIN ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA ISOLATION; TRANSCRIPTION REGULATION; UPREGULATION;

ADAPTATION, PHYSIOLOGICAL; ENERGY METABOLISM; ESCHERICHIA COLI K12; GLUCOSE; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; TRANSCRIPTION, GENETIC;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI K12;

EID: 33746061277     PISSN: 13500872     EISSN: None     Source Type: Journal    
DOI: 10.1099/mic.0.28939-0     Document Type: Article

References (61)

1. Cecchini, G., Schroder, I., Gunsalus, R. P. & Maklashina, E. (2002). Succinate dehydrogenase and fumarate reductase from Escherichia coli. Biochim Biophys Acta 1553, 140-157.
2. Conway, P. L. (1995). Microbial ecology of the human large intestine. In Human Colonic Bacteria: Role in Nutrition, Physiology, and Pathology, pp. 1-24. Edited by G. R. Gibson & G. T. MacFarlane. Boca Raton, FL: CRC Press.
3. Cronan, J. E., Jr & LaPorte, D. (1996). Tricarboxylic acid cycle and glyoxylate bypass. In Escherichia coli and Salmonella typhimurium: Cellular and Molecular Biology, 2nd edn, pp. 206-216. Edited by F. C. Neidhardt and others. Washington, DC: American Society for Microbiology.
4. Death, A. & Ferenci, T. (1993b). The importance of the binding-protein dependent Mgl system to the transport of glucose in Escherichia coli growing on low sugar concentrations. Res Microbiol 144, 529-537.
5. Death, A., Notley, L. & Ferenci, T. (1993a). Derepression of LamB protein faciliates outer membrane permeation of carbohydrates into Escherichia coli under conditions of nutrient stress. J Bacteriol 175, 1475-1483.
6. Egli, T. (1995). The ecological and physiological significance of the growth of heterotrophic microorganisms with mixtures of substrates. Adv Microb Ecol 14, 305-386.
7. Farrell, M. J. & Finkel, S. E. (2003). The growth advantage in stationary-phase phenotype conferred by rpoS mutations is dependent on the pH and nutrient environment. J Bacteriol 185, 7044-7052.
8. Ferenci, T. (1996). Adaptation to life at micromolar nutrient levels: regulation of Escherichia coli glucose transport by endoinduction and cAMP. FEMS Microbiol Rev 18, 301-317.
9. Ferenci, T. (1999a). Regulation by nutrient limitation. Curr Opin Microbiol 2, 208-213.
10. Ferenci, T. (2003). What is driving the acquisition of mutS and rpoS polymorphisms in Escherichia coli? Trends Microbiol 11, 457-461.
11. Fischer, E. & Sauer, U. (2003). A novel metabolic cycle catalyzes glucose oxidation and anaplerosis in hungry Escherichia coli. J Biol Chem 278, 46446-46451.
12. Garcia-Armisen, T. & Servais, P. (2004). Enumeration of viable E. coli in rivers and wastewaters by fluorescent in situ hybridization. J Microbiol Methods 58, 269-279.
13. Gosset, G., Zhang, Z., Nayyar, S., Cuevas, W. A. & Saier, M. H., Jr (2004). Transcriptome analysis of Crp-dependent catabolite control of gene expression in Escherichia coli. J Bacteriol 186, 3516-3524.
14. Gourse, R. L., de Boer, H. A. & Nomura, M. (1986). DNA determinants of rRNA synthesis in E. coli: growth rate dependent regulation, feedback inhibition, upstream activation, antitermination. Cell 44, 197-205.
15. Guest, J. R. (1981). Partial replacement of succinate dehydrogenase function by phage- and plasmid-specified fumarate reductase in Escherichia coli. J Gen Microbial 122, 171-179.
16. Hazen, T. C. & Toranzos, G. A. (1990). Tropical source water. In Drinking Water Microbiology, pp. 32-54. Edited by G. A. McFeters. New York: Springer.
17. S (RpoS) subunit of RNA polymerase. Microbiol Mol Biol Rev 66, 373-395.
18. Ho, K. K. & Weiner, H. (2005). Isolation and characterization of an aldehyde dehydrogenase encoded by the aldB gene of Escherichia coli. J Bacteriol 187, 1067-1073.
19. Hua, Q., Yang, C., Baba, T., Mori, H. & Shimizu, K. (2003). Responses of the central metabolism in Escherichia coli to phosphoglucose isomerase and glucose-6-phosphate dehydrogenase knockouts. J Bacteriol 185, 7053-7067.
20. Hua, Q., Yang, C., Oshima, T., Mori, H. & Shimizu, K. (2004). Analysis of gene expression in Escherichia coli in response to changes of growth-limiting nutrient in chemostat cultures. Appl Environ Microbiol 70, 2354-2366.
21. Ihssen, J. & Egli, T. (2004). Specific growth rate and not cell density controls the general stress response in Escherichia coli. Microbiology 150, 1637-1648.
22. Ihssen, J. & Egli, T. (2005). Global physiological analysis of carbon-and energy-limited growing Escherichia coli confirms a high degree of catabolic flexibility and preparedness for mixed substrate utilization. Environ Microbiol 7, 1568-1581.
23. King, T., Ishihama, A., Kori, A. & Ferenci, T. (2004). A regulatory trade-off as a source of strain variation in the species Escherichia coli. J Bacteriol 186, 5614-5620.
24. Koshland, D. E., Jr, Walsh, K. & LaPorte, D. C. (1985). Sensitivity of metabolic fluxes to covalent control. Curr Top Cell Regul 27, 13-22.
25. Kurland, C. G. & Maaloe, O. (1962). Regulation of ribosomal and transfer RNA synthesis. J Mol Biol 4, 193-210.
26. Lacour, S. & Landini, P. (2004). SigmaS -dependent gene expression at the onset of stationary phase in Escherichia coli: function of sigmaS -dependent genes and identification of their promoter sequences. J Bacteriol 186, 7186-7195.
27. Lee, S. K., Newman, J. D. & Keasling, J. D. (2005). Catabolite repression of the propionate catabolic genes in Escherichia coli and Salmonella enterica: evidence for involvement of the cyclic AMP receptor protein. J Bacteriol 187, 2793-2800.
28. Limon, A., Hidalgo, E. & Aguilar, J. (1997). The aldA gene of Escherichia coli is under the control of at least three transcriptional regulators. Microbiology 143, 2085-2095.
29. Liu, M., Durfee, T., Cabrera, J. E., Zhao, K., Jin, D. J. & Blattner, F. R. (2005). Global transcriptional programs reveal a carbon source foraging strategy by Escherichia coli. J Biol Chem 280, 15921-15927.
30. Macfarlane, G. T. & Macfarlane, S. (1997). Human colonic microbiota: ecology, physiology and metabolic potential of intestinal bacteria. Scand J Gastroenterol Suppl 222, 3-9.
31. Macfarlane, S. & Macfarlane, G. T. (2004). Bacterial diversity in the human gut. Adv Appl Microbiol 54, 261-289.
32. Macfarlane, G. T., Macfarlane, S. & Gibson, G. R. (1998). Validation of a three-stage compound continuous culture system for investigating the effect of retention time on the ecology and metabolism of bacteria in the human colon. Microb Ecol 35, 180-187.
33. Makinoshima, H., Aizawa, S., Hayashi, H., Miki, T., Nishimura, A. & Ishihama, A. (2003). Growth phase-coupled alterations in cell structure and function of Escherichia coli. J Bacteriol 185, 1338-1345.
34. Matin, A., Auger, E. A., Blum, P. H. & Schultz, J. E. (1989). Genetic basis of starvation survival in nondifferentiating bacteria. Annu Rev Microbiol 43, 293-316.
35. McFeters, G. A. (1990). Drinking Water Microbiology. New York: Springer.
36. Miura, A., Krueger, J. H., Itoh, S., de Boer, H. A. & Nomura, M. (1981). Growth-rate-dependent regulation of ribosome synthesis in E. coli: expression of the lacZ and galK genes fused to ribosomal promoters. Cell 25, 773-782.
37. Morita, R. Y. (1993). Bioavailability of energy and the starvation state. In Starvation in Bacteria, pp. 1-23. Edited by S. Kjelleberg. New York: Plenum.
38. Münster, U. (1993). Concentrations and fluxes of organic carbon substrates in the aquatic environment. Antonie van Leeuwenhoek 63, 243-274.
39. Notley, L. & Ferenci, T. (1995). Differential expression of mal genes under cAMP and enclogenous inducer control in nutrient-stressed Escherichia coli. Mol Microbiol 16, 121-129.
40. 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.
41. 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.
42. Notley-McRobb, L., Death, A. & Ferenci, T. (1997). The relationship between external glucose concentration and cAMP levels inside Escherichia coli: implications for model of phosphotransferase-mediated regulation of adenylate cyclase. Microbiology 143, 1909-1918.
43. 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.
44. Nyström, T. (2004). Growth versus maintenance: a trade-off dictated by RNA polymerase availability and sigma factor competition? Mol Microbiol 54, 855-862.
45. Patten, C. L., Kirchhof, M. G., Schertzberg, M. R., Morton, R. A. & Schellhorn, H. E. (2004). Microarray analysis of RpoS-mediated gene expression in Escherichia coli K-12. Mol Genet Genomics; 272, 580-591.
46. Rozen, Y. & Belkin, S. (2001). Survival of enteric bacteria in seawater. FEMS Microbial Rev 25, 513-529.
47. Salgado, H., Gama-Castro, S., Martinez-Antonio, A. & 8 other authors (2004). RegulonDB (version 4.0): transcriptional regulation, operon organization and growth conditions in Escherichia coli K-12. Nucleic Acids Res 32, D303-D306.
48. Sambrook, J., Fritsch, E. F. & Maniatis, T. (1989). Molecular Cloning. a Laboratory Manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
49. Savageau, M. A. (1983). Escherichia coli habitats, cell types, and molecular mechanisms of gene control. Am Nat 122, 732-744.
50. Senn, H., Lendenmann, U., Snozzi, M., Hamer, G. & Egli, T. (1994). The growth of Escherichia coli in glucose-limited chemostat cultures: a re-examination of the kinetics. Biochim Biophys Acta 1201, 424-436.
51. Tan, K., Moreno-Hagelsieb, G., Collado-Vides, J. & Stormo, G. D. (2001). A comparative genomics approach to prediction of new members of regulons. Genome Res 11, 566-584.
52. Tweeddale, H., Notley-McRobb, L. & Ferenci, T. (1998). Effect of slow growth on metabolism of Escherichia coli, as revealed by global metabolite pool ("metabolome") analysis. J Bacteriol 180, 5109-5116.
53. Visick, J. E. & Clarke, S. (1997). RpoS- and OxyR-independent induction of HPI catalase at stationary phase in Escherichia coli and identification of rpoS mutations in common laboratory strains. J Bacteriol 179, 4158-4163.
54. Wang, L., Hashimoto, Y., Tsao, C. Y., Valdes, J. J. & Bentley, W. E. (2005). Cyclic AMP (cAMP) and cAMP receptor protein influence both synthesis and uptake of extracellular autoinducer 2 in Escherichia coli. J Bacteriol 187, 2066-2076.
55. Weber, H., Polen, T., Heuveling, J., Wendisch, V. F. & Hengge, R. (2005). Genome-wide analysis of the general stress response network in Escherichia coli: sigmaS-dependent genes, promoters, and sigma factor selectivity. J Bacteriol 187, 1591-1603.
56. WHO (1996). Guideline for Drinking-Water Quality, vol. 2, Health Criteria and Other Supporting Information, 2nd edn. Geneva, Switzerland: World Health Organization.
57. Wick, L. M., Quadroni, M. & Egli, T. (2001). Short- and long-term changes in proteome composition and kinetic properties in a culture of Escherichia coli during transition from glucose-excess to glucose-limited growth conditions in continuous culture and vice versa. Environ Microbiol 3, 588-599.
58. Wick, L. M., Weilenmann, H.-U. & Egli, T. (2002). The apparent clock-like evolution of Escherichia coli in glucose-limited chemostats is reproducible at large but not at small population sizes and can be explained with Monod kinetics. Microbiology 148, 2889-2902.
59. Williams, S. T. (1985). Oligotrophy in soil: fact or fiction? In Bacteria in the Natural Environment, pp. 81-110. Edited by M. Fletcher & G. D. Floodgate. London: Academic Press.
60. Yoon, S. H., Han, M. J., Lee, S. Y., Jeong, K. J. & Yoo, J. S. (2003). Combined transcriptome and proteome analysis of Escherichia coli during high cell density culture. Biotechnol Bioeng 81, 753-767.
61. Zambrano, M. M. & Kolter, R. (1996). GASPing for life in stationary phase. Cell 86, 181-184.