1887

Abstract

Microarray technology was used to study the cellular events that take place at the transcription level during short-term (physiological) and long-term (genetic) adaptation of the faecal indicator bacterium K-12 to slow growth under limited nutrient supply. Short-term and long-term adaptation were assessed by comparing the mRNA levels isolated after 40 or 500 h of glucose-limited continuous culture at a dilution rate of 0.3 h with those from batch culture with glucose excess. A large number of genes encoding periplasmic binding proteins were upregulated, indicating that the cells are prepared for high-affinity uptake of all types of carbon sources during glucose-limited growth in continuous culture. All the genes belonging to the maltose (/) and galactose (/) operons were upregulated. A similar transcription pattern was observed for long-term cultures except that the expression factors were lower than in the short-term adaptation. The patterns of upregulation were confirmed by real-time RT-PCR. A switch from a fully operational citric acid cycle to the PEP-glyoxylate cycle was clearly observed in cells grown in glucose-limited continuous culture when compared to batch-grown cells and this was confirmed by transcriptome analysis. This transcriptome analysis confirms and extends the observations from previous proteome and catabolome studies in the authors' laboratory.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.28939-0
2006-07-01
2019-10-21
Loading full text...

Full text loading...

/deliver/fulltext/micro/152/7/2111.html?itemId=/content/journal/micro/10.1099/mic.0.28939-0&mimeType=html&fmt=ahah

References

  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.[CrossRef]
    [Google Scholar]
  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.[CrossRef]
    [Google Scholar]
  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.
    [Google Scholar]
  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.
    [Google Scholar]
  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.[CrossRef]
    [Google Scholar]
  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.[CrossRef]
    [Google Scholar]
  9. Ferenci, T. ( 1999a; ). Regulation by nutrient limitation. Curr Opin Microbiol 2, 208–213.[CrossRef]
    [Google Scholar]
  10. Ferenci, T. ( 2003; ). What is driving the acquisition of mutS and rpoS polymorphisms in Escherichia coli? Trends Microbiol 11, 457–461.[CrossRef]
    [Google Scholar]
  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.[CrossRef]
    [Google Scholar]
  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.[CrossRef]
    [Google Scholar]
  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.[CrossRef]
    [Google Scholar]
  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.[CrossRef]
    [Google Scholar]
  15. Guest, J. R. ( 1981; ). Partial replacement of succinate dehydrogenase function by phage- and plasmid-specified fumarate reductase in Escherichia coli. J Gen Microbiol 122, 171–179.
    [Google Scholar]
  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. Hengge-Aronis, R. ( 2002; ). Signal transduction and regulatory mechanisms involved in control of the σ S (RpoS) subunit of RNA polymerase. Microbiol Mol Biol Rev 66, 373–395.[CrossRef]
    [Google Scholar]
  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.[CrossRef]
    [Google Scholar]
  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.[CrossRef]
    [Google Scholar]
  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.[CrossRef]
    [Google Scholar]
  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.[CrossRef]
    [Google Scholar]
  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.[CrossRef]
    [Google Scholar]
  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.[CrossRef]
    [Google Scholar]
  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.
    [Google Scholar]
  25. Kurland, C. G. & Maaloe, O. ( 1962; ). Regulation of ribosomal and transfer RNA synthesis. J Mol Biol 4, 193–210.[CrossRef]
    [Google Scholar]
  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.[CrossRef]
    [Google Scholar]
  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.[CrossRef]
    [Google Scholar]
  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.[CrossRef]
    [Google Scholar]
  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.[CrossRef]
    [Google Scholar]
  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.
    [Google Scholar]
  31. Macfarlane, S. & Macfarlane, G. T. ( 2004; ). Bacterial diversity in the human gut. Adv Appl Microbiol 54, 261–289.
    [Google Scholar]
  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.[CrossRef]
    [Google Scholar]
  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.[CrossRef]
    [Google Scholar]
  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.[CrossRef]
    [Google Scholar]
  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.[CrossRef]
    [Google Scholar]
  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.[CrossRef]
    [Google Scholar]
  39. 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.[CrossRef]
    [Google Scholar]
  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.[CrossRef]
    [Google Scholar]
  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.[CrossRef]
    [Google Scholar]
  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.[CrossRef]
    [Google Scholar]
  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.[CrossRef]
    [Google Scholar]
  44. Nyström, T. ( 2004; ). Growth versus maintenance: a trade-off dictated by RNA polymerase availability and sigma factor competition? Mol Microbiol 54, 855–862.[CrossRef]
    [Google Scholar]
  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.[CrossRef]
    [Google Scholar]
  46. Rozen, Y. & Belkin, S. ( 2001; ). Survival of enteric bacteria in seawater. FEMS Microbiol Rev 25, 513–529.[CrossRef]
    [Google Scholar]
  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.[CrossRef]
    [Google Scholar]
  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.[CrossRef]
    [Google Scholar]
  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.[CrossRef]
    [Google Scholar]
  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.[CrossRef]
    [Google Scholar]
  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.
    [Google Scholar]
  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.
    [Google Scholar]
  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.[CrossRef]
    [Google Scholar]
  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.[CrossRef]
    [Google Scholar]
  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.[CrossRef]
    [Google Scholar]
  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.
    [Google Scholar]
  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.[CrossRef]
    [Google Scholar]
  61. Zambrano, M. M. & Kolter, R. ( 1996; ). GASPing for life in stationary phase. Cell 86, 181–184.[CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.28939-0
Loading
/content/journal/micro/10.1099/mic.0.28939-0
Loading

Data & Media loading...

Supplements

genes whose expression levels were increased by a factor ≥2 in cultures exposed for 40 h to glucose-limited growth conditions in continuous culture at =0.3 h . [PDF](185 kb) genes whose expression levels were increased by a factor ≥2 in cultures exposed for 500 h to glucose-limited growth conditions in continuous culture at =0.3 h . [PDF](57 kb) genes whose expression levels were decreased by a factor ≤-2 in cultures exposed for 40 h to glucose-limited growth conditions in continuous culture at =0.3 h . [PDF](265 kb) genes whose expression levels were decreased by a factor ≤-2 in cultures exposed for 500 h to glucose-limited growth conditions in continuous culture at =0.3 h . [PDF](132 kb)

PDF

genes whose expression levels were increased by a factor ≥2 in cultures exposed for 40 h to glucose-limited growth conditions in continuous culture at =0.3 h . [PDF](185 kb) genes whose expression levels were increased by a factor ≥2 in cultures exposed for 500 h to glucose-limited growth conditions in continuous culture at =0.3 h . [PDF](57 kb) genes whose expression levels were decreased by a factor ≤-2 in cultures exposed for 40 h to glucose-limited growth conditions in continuous culture at =0.3 h . [PDF](265 kb) genes whose expression levels were decreased by a factor ≤-2 in cultures exposed for 500 h to glucose-limited growth conditions in continuous culture at =0.3 h . [PDF](132 kb)

PDF

genes whose expression levels were increased by a factor ≥2 in cultures exposed for 40 h to glucose-limited growth conditions in continuous culture at =0.3 h . [PDF](185 kb) genes whose expression levels were increased by a factor ≥2 in cultures exposed for 500 h to glucose-limited growth conditions in continuous culture at =0.3 h . [PDF](57 kb) genes whose expression levels were decreased by a factor ≤-2 in cultures exposed for 40 h to glucose-limited growth conditions in continuous culture at =0.3 h . [PDF](265 kb) genes whose expression levels were decreased by a factor ≤-2 in cultures exposed for 500 h to glucose-limited growth conditions in continuous culture at =0.3 h . [PDF](132 kb)

PDF

genes whose expression levels were increased by a factor ≥2 in cultures exposed for 40 h to glucose-limited growth conditions in continuous culture at =0.3 h . [PDF](185 kb) genes whose expression levels were increased by a factor ≥2 in cultures exposed for 500 h to glucose-limited growth conditions in continuous culture at =0.3 h . [PDF](57 kb) genes whose expression levels were decreased by a factor ≤-2 in cultures exposed for 40 h to glucose-limited growth conditions in continuous culture at =0.3 h . [PDF](265 kb) genes whose expression levels were decreased by a factor ≤-2 in cultures exposed for 500 h to glucose-limited growth conditions in continuous culture at =0.3 h . [PDF](132 kb)

PDF
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error