1887

Abstract

Expression of the major outer-membrane porins in is transcriptionally controlled during nutrient limitation. Expression of was more than 40-fold higher under glucose limitation than under nitrogen (ammonia) limitation in chemostat cultures at the same growth rate. In contrast, expression was higher under N limitation. The basis of regulation by nutrient limitation was investigated using mutations affecting expression of porin genes. The influence of , , and , as well as the two-component system, was studied under glucose and N limitation in chemostat cultures. A major contributor to low expression under N limitation was negative control by the RpoS sigma factor. RpoS levels were high under N limitation and loss of RpoS resulted in a 19-fold increase in transcription, but little change was observed with . Lack of RpoS under glucose limitation had a lesser stimulatory effect on expression. Porin production was minimally dependent on EnvZ under N limitation due to OmpR phosphorylation by acetyl phosphate. Evidence obtained with and mutants suggested that the acetyl phosphate level also regulates porins independently and indirectly via RpoS and other pathways. double mutants had a residual level of porin transcription, implicating alternative means of OmpR phosphorylation under nutrient limitation. Another critical factor in regulation was the level of cAMP, as a mutant hardly expressed under glucose limitation but boosted . In addition, the role of DNA-binding proteins encoded by was tested under glucose limitation: the mutation reduced the glucose-limitation peak, but the mutation suppressed the effect, suggesting a complex web of interrelationships between the DNA-binding proteins. Indeed, multiple inputs and no single regulator were responsible for the high peak of expression under glucose limitation.

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2001-11-01
2020-01-17
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References

  1. Atlung, T. & Ingmer, H. ( 1997; ). H-NS – a modulator of environmentally regulated gene expression. Mol Microbiol 24, 7-17.[CrossRef]
    [Google Scholar]
  2. Bouche, S., Klauck, E., Fischer, D., Lucassen, M., Jung, K. & Hengge-Aronis, R. ( 1998; ). Regulation of RssB-dependent proteolysis in Escherichia coli: a role for acetyl phosphate in a response regulator-controlled process. Mol Microbiol 27, 787-795.[CrossRef]
    [Google Scholar]
  3. Brass, J. M., Manson, M. D. & Larson, T. J. ( 1984; ). Transposon Tn10-dependent expression of the lamB gene in Escherichia coli. J Bacteriol 159, 93-99.
    [Google Scholar]
  4. Buckler, D. R., Anand, G. S. & Stock, A. M. ( 2000; ). Response-regulator phosphorylation and activation: a two-way street? Trends Microbiol 8, 153-156.[CrossRef]
    [Google Scholar]
  5. Casabadan, M. J. ( 1976; ). Transposition and fusion of the lac operon to selected promoters in E. coli using bacteriophage Lambda and Mu. J Mol Biol 104, 541-555.[CrossRef]
    [Google Scholar]
  6. Death, A. & Ferenci, T. ( 1994; ). Between feast and famine: endogenous inducer synthesis in the adaptation of Escherichia coli to growth with limiting carbohydrates. J Bacteriol 176, 5101-5107.
    [Google Scholar]
  7. Death, A., Notley, L. & Ferenci, T. ( 1993; ). Derepression of LamB protein facilitates outer membrane permeation of carbohydrates into Escherichia coli under conditions of nutrient stress. J Bacteriol 175, 1475-1483.
    [Google Scholar]
  8. Farewell, A., Kvint, K. & Nystrom, T. ( 1998; ). Negative regulation by RpoS: a case of sigma factor competition. Mol Microbiol 29, 1039-1051.[CrossRef]
    [Google Scholar]
  9. Ferenci, T. ( 1996; ). Adaptation to life at micromolar nutrient levels: the regulation of Escherichia coli glucose transport by endoinduction and cAMP. FEMS Microbiol Rev 18, 301-317.[CrossRef]
    [Google Scholar]
  10. Ferenci, T. ( 1999; ). Regulation by nutrient limitation. Curr Opin Microbiol 2, 208-213.[CrossRef]
    [Google Scholar]
  11. Ferenci, T. & Stretton, S. ( 1989; ). Cysteine-22 and cysteine-38 are not essential for the functions of maltoporin (LamB protein). FEMS Microbiol Lett 52, 335-339.
    [Google Scholar]
  12. Ferrario, M., Ernsting, B. R., Borst, D. W., Wiese, D. E.II, Blumenthal, R. M. & Matthews, R. G. ( 1995; ). The leucine-responsive regulatory protein of Escherichia coli negatively regulates transcription of ompC and micF and positively regulates translation of ompF. J Bacteriol 177, 103-113.
    [Google Scholar]
  13. Forst, S., Delgado, J., Ramakrishnan, G. & Inouye, M. ( 1988; ). Regulation of ompC and ompF expression in Escherichia coli in the absence of envZ. J Bacteriol 170, 5080-5085.
    [Google Scholar]
  14. Gentry, D. R., Hernadez, V. J., Nguyen, L. H., Jensen, D. B. & Cashel, M. ( 1993; ). Synthesis of stationary-phase sigma factor Sigma-S is positively regulated by ppGpp. J Bacteriol 175, 7982-7989.
    [Google Scholar]
  15. Goosen, N. & Van de Putte, P. ( 1995; ). The regulation of transcription initiation by integration host factor. Mol Microbiol 16, 1-7.[CrossRef]
    [Google Scholar]
  16. Graeme-Cook, K. A., May, G., Bremer, E. & Higgins, C. F. ( 1989; ). Osmotic regulation of porin expression: a role for DNA supercoiling. Mol Microbiol 3, 1287-1294.[CrossRef]
    [Google Scholar]
  17. Hall, M. N. & Silhavy, T. J. ( 1981; ). The ompB locus and the regulation of the major outer membrane porin proteins of Escherichia coli K12. J Mol Biol 146, 23-43.[CrossRef]
    [Google Scholar]
  18. Hengge-Aronis, R. ( 1999; ). Interplay of global regulators and cell physiology in the general stress response of Escherichia coli. Curr Opin Microbiol 2, 148-152.[CrossRef]
    [Google Scholar]
  19. Hengge-Aronis, R. ( 2000; ). The general stress response in Escherichia coli In Bacterial Stress Responses , pp. 161-178. Edited by R. Hengge-Aronis & K. Storz. Washington DC:American Society for Microbiology.
  20. Heyde, M., Laloi, P. & Portalier, R. ( 2000; ). Involvement of carbon source and acetyl phosphate in the external-pH-dependent expression of porin genes in Escherichia coli. J Bacteriol 182, 198-202.[CrossRef]
    [Google Scholar]
  21. Huang, L., Tsui, P. & Freundlich, M. ( 1992; ). Positive and negative control of ompB transcription in Escherichia coli by cyclic AMP and the cyclic AMP receptor protein. J Bacteriol 174, 664-670.
    [Google Scholar]
  22. Huisman, G. W. & Kolter, R. ( 1994; ). Sensing starvation: a homoserine lactone-dependent signaling pathway in Escherichia coli. Science 265, 537-539.[CrossRef]
    [Google Scholar]
  23. Kenney, L. J. ( 1997; ). Kinase activity of EnvZ, an osmoregulatory signal transducing protein of Escherichia coli. Arch Biochem Biophys 346, 303-311.[CrossRef]
    [Google Scholar]
  24. Kenney, L. J., Bauer, M. D. & Silhavy, T. J. ( 1995; ). Phosphorylation-dependent conformational changes in OmpR, an osmoregulatory DNA-binding protein of Escherichia coli. Proc Natl Acad Sci USA 92, 8866-8870.[CrossRef]
    [Google Scholar]
  25. Kornberg, A., Rao, N. N. & Ault-Riche, D. ( 1999; ). Inorganic polyphosphate: a molecule of many functions. Annu Rev Biochem 68, 89-125.[CrossRef]
    [Google Scholar]
  26. Lan, C. Y. & Igo, M. M. ( 1998; ). Differential expression of the OmpF and OmpC porin proteins in Escherichia coli K-12 depends upon the level of active OmpR. J Bacteriol 180, 171-174.
    [Google Scholar]
  27. Lange, R. & Hengge-Aronis, R. ( 1994; ). The cellular concentration of the sigma-S subunit of RNA polymerase in Escherichia coli is controlled at the levels of transcription, translation and protein stability. Genes Dev 8, 1600-1612.[CrossRef]
    [Google Scholar]
  28. Liu, X. & Ferenci, T. ( 1998; ). Regulation of porin-mediated outer membrane permeability by nutrient limitation in Escherichia coli. J Bacteriol 180, 3917-3922.
    [Google Scholar]
  29. Liu, X., Ng, C. & Ferenci, T. ( 2000; ). Global adaptations resulting from high population densities in Escherichia coli cultures. J Bacteriol 182, 4158-4164.[CrossRef]
    [Google Scholar]
  30. Lugtenberg, B., Peters, R., Bernheimer, H. & Berendsen, W. ( 1976; ). Influence of cultural conditions and mutations on the composition of the outer membrane proteins of Escherichia coli. Mol Gen Genet 147, 251-262.[CrossRef]
    [Google Scholar]
  31. McCleary, W. R., Stock, J. B. & Ninfa, A. J. ( 1993; ). Is acetyl phosphate a global signal in Escherichia coli? J Bacteriol 175, 2793-2798.
    [Google Scholar]
  32. el-Mansi, E. M. & Holms, W. H. ( 1989; ). Control of carbon flux to acetate excretion during growth of Escherichia coli in batch and continuous cultures. J Gen Microbiol 135, 2875-2883.
    [Google Scholar]
  33. Matsubara, M. & Mizuno, T. ( 1999; ). EnvZ-independent phosphotransfer signaling pathway of the OmpR-mediated osmoregulatory expression of OmpC and OmpF in Escherichia coli. Biosci Biotechnol Biochem 63, 408-414.[CrossRef]
    [Google Scholar]
  34. Miller, J. (1972). Experiments in Molecular Genetics. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
  35. Notley, L. & Ferenci, T. ( 1996; ). Induction of RpoS-dependent functions in glucose-limited continuous culture: what level of nutrient limitation induces the stationary phase of Escherichia coli? J Bacteriol 178, 1465-1468.
    [Google Scholar]
  36. Notley-McRobb, L., Death, A. & Ferenci, T. ( 1997; ). The relationship between external glucose concentration and cAMP levels inside Escherichia coli: implications for models of phosphotransferase-mediated regulation of adenylate cyclase. Microbiology 143, 1909-1918.[CrossRef]
    [Google Scholar]
  37. Nystrom, T. ( 1998; ). To be or not to be – the ultimate decision of the growth-arrested bacterial cell. FEMS Microbiol Rev 21, 283-290.[CrossRef]
    [Google Scholar]
  38. Overbeeke, N. & Lugtenberg, B. ( 1980; ). Expression of outer membrane protein e of Escherichia coli K12 by phosphate limitation. FEBS Lett 112, 229-232.[CrossRef]
    [Google Scholar]
  39. Painbeni, E., Caroff, M. & Rouviere-Yaniv, J. ( 1997; ). Alterations of the outer membrane composition in Escherichia coli lacking the histone-like protein HU. Proc Natl Acad Sci USA 94, 6712-6717.[CrossRef]
    [Google Scholar]
  40. Pratt, L. A., Hsing, W., Gibson, K. E. & Silhavy, T. J. ( 1996; ). From acids to osmZ: multiple factors influence the synthesis of the OmpF and OmpC porins in Escherichia coli. Mol Microbiol 20, 911-917.[CrossRef]
    [Google Scholar]
  41. Ramani, N., Huang, L. & Freundlich, M. ( 1992; ). In vitro interactions of integration host factor with the ompF promoter-regulatory region of Escherichia coli. Mol Gen Genet 231, 248-255.
    [Google Scholar]
  42. Russo, F. D. & Silhavy, T. J. ( 1991; ). EnvZ controls the concentration of phosphorylated OmpR to mediate osmoregulation of the porin genes. J Mol Biol 222, 567-580.[CrossRef]
    [Google Scholar]
  43. Scott, N. W. & Harwood, C. R. ( 1980; ). Studies on the influence of the cyclic AMP system on major outer membrane proteins of Escherichia coli K12. FEMS Microbiol Lett 9, 95-98.[CrossRef]
    [Google Scholar]
  44. Shiga, Y., Kametani, S., Kadokura, T. & Akanuma, H. ( 1999; ). 1,5-Anhydroglucitol promotes glycogenolysis in Escherichia coli. J Biochem 125, 166-172.[CrossRef]
    [Google Scholar]
  45. Shin, S. & Park, C. ( 1995; ). Modulation of flagellar expression in Escherichia coli by acetyl phosphate and the osmoregulator OmpR. J Bacteriol 177, 4696-4702.
    [Google Scholar]
  46. Slauch, J. M. & Silhavy, T. J. ( 1989; ). Genetic analysis of the switch that controls porin gene expression in Escherichia coli K-12. J Mol Biol 210, 281-292.[CrossRef]
    [Google Scholar]
  47. Slauch, J. M., Garrett, S., Jackson, D. E. & Silhavy, T. J. ( 1988; ). EnvZ functions through OmpR to control porin gene expression in Escherichia coli K-12. J Bacteriol 170, 439-441.
    [Google Scholar]
  48. Sterkenburg, A., Vlegels, E. & Wouters, J. T. M. ( 1984; ). Influence of nutrient limitation and growth rate on the outer membrane proteins of Klebsiella aerogenes NCTC 418. J Gen Microbiol 130, 2347-2355.
    [Google Scholar]
  49. Suzuki, T., Ueguchi, C. & Mizuno, T. ( 1996; ). H-NS regulates ompF expression through micF antisense RNA in Escherichia coli. J Bacteriol 178, 3650-3653.
    [Google Scholar]
  50. Teich, A., Meyer, S., Lin, H. Y., Andersson, L., Enfors, S. & Neubauer, P. ( 1999; ). Growth rate related concentration changes of the starvation response regulators sigma(S) and ppGpp in glucose-limited fed-batch and continuous cultures of Escherichia coli. Biotechnol Prog 15, 123-129.[CrossRef]
    [Google Scholar]
  51. Thomas, A. D. & Booth, I. R. ( 1992; ). The regulation of expression of the porin gene ompC by acid pH. J Gen Microbiol 138, 1829-1835.[CrossRef]
    [Google Scholar]
  52. Tokishita, S. & Mizuno, T. ( 1994; ). Transmembrane signal transduction by the Escherichia coli osmotic sensor, EnvZ: intermolecular complementation of transmembrane signalling. Mol Microbiol 13, 435-444.[CrossRef]
    [Google Scholar]
  53. Tsui, P., Helu, V. & Freundlich, M. ( 1988; ). Altered osmoregulation of ompF in integration host factor mutants of Escherichia coli. J Bacteriol 170, 4950-4953.
    [Google Scholar]
  54. 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]
  55. Yamada, H., Yoshida, T., Tanaka, K., Sasakawa, C. & Mizuno, T. ( 1991; ). Molecular analysis of the Escherichia coli hns gene encoding a DNA-binding protein, which preferentially recognizes curved DNA sequences. Mol Gen Genet 230, 332-336.[CrossRef]
    [Google Scholar]
  56. Yu, D. G., Ellis, H. M., Lee, E. C., Jenkins, N. A., Copeland, N. G. & Court, D. L. ( 2000; ). An efficient recombination system for chromosome engineering in Escherichia coli. Proc Natl Acad Sci USA 97, 5978-5983.[CrossRef]
    [Google Scholar]
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