Skip to main content
PMC home page
Journal of Bacteriology logoLink to Journal of Bacteriology
. 1997 Jan;179(1):297–300. doi: 10.1128/jb.179.1.297-300.1997

The RNA-binding protein HF-I plays a global regulatory role which is largely, but not exclusively, due to its role in expression of the sigmaS subunit of RNA polymerase in Escherichia coli.

A Muffler 1, D D Traulsen 1, D Fischer 1, R Lange 1, R Hengge-Aronis 1
PMCID: PMC178696  PMID: 8982015

Abstract

The hfq-encoded RNA-binding protein HF-I has long been known as a host factor for phage Qbeta RNA replication and has recently been shown to be essential for translation of rpoS, which encodes the sigmaS subunit of RNA polymerase. Here we demonstrate that an hfq null mutant does not synthesize glycogen, is starvation and multiple stress sensitive, and exhibits strongly reduced expression of representative sigmaS-regulated genes. These phenotypes are consistent with strongly reduced sigmaS levels in the hfq mutant. However, the analysis of global protein synthesis patterns on two-dimensional O'Farrell gels indicates that approximately 40% of the more than 30 proteins whose syntheses are altered in the hfq null mutant are not affected by an rpoS mutation. We conclude that HF-I is a global regulator involved in the regulation of expression of sigmaS and sigmaS-independent genes.

Full Text

The Full Text of this article is available as a PDF (276.5 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Barrera I., Schuppli D., Sogo J. M., Weber H. Different mechanisms of recognition of bacteriophage Q beta plus and minus strand RNAs by Q beta replicase. J Mol Biol. 1993 Jul 20;232(2):512–521. doi: 10.1006/jmbi.1993.1407. [DOI] [PubMed] [Google Scholar]
  2. Buettner M. J., Spitz E., Rickenberg H. V. Cyclic adenosine 3',5'-monophosphate in Escherichia coli. J Bacteriol. 1973 Jun;114(3):1068–1073. doi: 10.1128/jb.114.3.1068-1073.1973. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Cheng H. H., Echols H. A class of Escherichia coli proteins controlled by the hflA locus. J Mol Biol. 1987 Aug 5;196(3):737–740. doi: 10.1016/0022-2836(87)90046-5. [DOI] [PubMed] [Google Scholar]
  4. DuBow M. S., Ryan T., Young R. A., Blumenthal T. Host factor for coliphage Q beta RNA replication: presence in procaryotes and association with the 30S ribosomal subunit in Escherichia coli. Mol Gen Genet. 1977 May 20;153(1):39–43. doi: 10.1007/BF01035994. [DOI] [PubMed] [Google Scholar]
  5. Franze de Fernandez M. T., Eoyang L., August J. T. Factor fraction required for the synthesis of bacteriophage Qbeta-RNA. Nature. 1968 Aug 10;219(5154):588–590. doi: 10.1038/219588a0. [DOI] [PubMed] [Google Scholar]
  6. Franze de Fernandez M. T., Hayward W. S., August J. T. Bacterial proteins required for replication of phage Q ribonucleic acid. Pruification and properties of host factor I, a ribonucleic acid-binding protein. J Biol Chem. 1972 Feb 10;247(3):824–831. [PubMed] [Google Scholar]
  7. Hengge-Aronis R., Fischer D. Identification and molecular analysis of glgS, a novel growth-phase-regulated and rpoS-dependent gene involved in glycogen synthesis in Escherichia coli. Mol Microbiol. 1992 Jul;6(14):1877–1886. doi: 10.1111/j.1365-2958.1992.tb01360.x. [DOI] [PubMed] [Google Scholar]
  8. Jenkins D. E., Schultz J. E., Matin A. Starvation-induced cross protection against heat or H2O2 challenge in Escherichia coli. J Bacteriol. 1988 Sep;170(9):3910–3914. doi: 10.1128/jb.170.9.3910-3914.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Kajitani M., Ishihama A. Identification and sequence determination of the host factor gene for bacteriophage Q beta. Nucleic Acids Res. 1991 Mar 11;19(5):1063–1066. doi: 10.1093/nar/19.5.1063. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Kajitani M., Kato A., Wada A., Inokuchi Y., Ishihama A. Regulation of the Escherichia coli hfq gene encoding the host factor for phage Q beta. J Bacteriol. 1994 Jan;176(2):531–534. doi: 10.1128/jb.176.2.531-534.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Kaminski P. A., Desnoues N., Elmerich C. The expression of nifA in Azorhizobium caulinodans requires a gene product homologous to Escherichia coli HF-I, an RNA-binding protein involved in the replication of phage Q beta RNA. Proc Natl Acad Sci U S A. 1994 May 24;91(11):4663–4667. doi: 10.1073/pnas.91.11.4663. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Lange R., Hengge-Aronis R. Identification of a central regulator of stationary-phase gene expression in Escherichia coli. Mol Microbiol. 1991 Jan;5(1):49–59. doi: 10.1111/j.1365-2958.1991.tb01825.x. [DOI] [PubMed] [Google Scholar]
  13. Lange R., Hengge-Aronis R. 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. 1994 Jul 1;8(13):1600–1612. doi: 10.1101/gad.8.13.1600. [DOI] [PubMed] [Google Scholar]
  14. Latil-Damotte M., Lares C. Relative order of glg mutations affecting glycogen biosynthesis in Escherichia coli K12. Mol Gen Genet. 1977 Feb 15;150(3):325–328. doi: 10.1007/BF00268132. [DOI] [PubMed] [Google Scholar]
  15. Loewen P. C., Hengge-Aronis R. The role of the sigma factor sigma S (KatF) in bacterial global regulation. Annu Rev Microbiol. 1994;48:53–80. doi: 10.1146/annurev.mi.48.100194.000413. [DOI] [PubMed] [Google Scholar]
  16. Marschall C., Hengge-Aronis R. Regulatory characteristics and promoter analysis of csiE, a stationary phase-inducible gene under the control of sigma S and the cAMP-CRP complex in Escherichia coli. Mol Microbiol. 1995 Oct;18(1):175–184. doi: 10.1111/j.1365-2958.1995.mmi_18010175.x. [DOI] [PubMed] [Google Scholar]
  17. McCann M. P., Kidwell J. P., Matin A. The putative sigma factor KatF has a central role in development of starvation-mediated general resistance in Escherichia coli. J Bacteriol. 1991 Jul;173(13):4188–4194. doi: 10.1128/jb.173.13.4188-4194.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Muffler A., Fischer D., Hengge-Aronis R. 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. 1996 May 1;10(9):1143–1151. doi: 10.1101/gad.10.9.1143. [DOI] [PubMed] [Google Scholar]
  19. Muffler A., Traulsen D. D., Lange R., Hengge-Aronis R. Posttranscriptional osmotic regulation of the sigma(s) subunit of RNA polymerase in Escherichia coli. J Bacteriol. 1996 Mar;178(6):1607–1613. doi: 10.1128/jb.178.6.1607-1613.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Nakao H., Watanabe H., Nakayama S., Takeda T. yst gene expression in Yersinia enterocolitica is positively regulated by a chromosomal region that is highly homologous to Escherichia coli host factor 1 gene (hfq). Mol Microbiol. 1995 Dec;18(5):859–865. doi: 10.1111/j.1365-2958.1995.18050859.x. [DOI] [PubMed] [Google Scholar]
  21. Noble J. A., Innis M. A., Koonin E. V., Rudd K. E., Banuett F., Herskowitz I. The Escherichia coli hflA locus encodes a putative GTP-binding protein and two membrane proteins, one of which contains a protease-like domain. Proc Natl Acad Sci U S A. 1993 Nov 15;90(22):10866–10870. doi: 10.1073/pnas.90.22.10866. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Preiss J., Romeo T. Physiology, biochemistry and genetics of bacterial glycogen synthesis. Adv Microb Physiol. 1989;30:183–238. doi: 10.1016/s0065-2911(08)60113-7. [DOI] [PubMed] [Google Scholar]
  23. Senear A. W., Steitz J. A. Site-specific interaction of Qbeta host factor and ribosomal protein S1 with Qbeta and R17 bacteriophage RNAs. J Biol Chem. 1976 Apr 10;251(7):1902–1912. [PubMed] [Google Scholar]
  24. Tsui H. C., Leung H. C., Winkler M. E. Characterization of broadly pleiotropic phenotypes caused by an hfq insertion mutation in Escherichia coli K-12. Mol Microbiol. 1994 Jul;13(1):35–49. doi: 10.1111/j.1365-2958.1994.tb00400.x. [DOI] [PubMed] [Google Scholar]

Articles from Journal of Bacteriology are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES