Skip to main content
Journal of Bacteriology logoLink to Journal of Bacteriology
. 1996 Jan;178(1):293–297. doi: 10.1128/jb.178.1.293-297.1996

Serratia marcescens contains a heterodimeric HU protein like Escherichia coli and Salmonella typhimurium.

J Oberto 1, J Rouviere-Yaniv 1
PMCID: PMC177653  PMID: 8550432

Abstract

Homologs of the dimeric HU protein of Escherichia coli can be found in every prokaryotic organism that has been analyzed. In this work, we demonstrate that Serratia marcescens synthesizes two distinct HU subunits, like E. coli and Salmonella typhimurium, suggesting that the heterodimeric HU protein could be a common feature of enteric bacteria. A phylogenetic analysis of the HU-type proteins (HU and IHF) is presented, and a scheme for the origin of the hup genes and the onset of HU heterodimericity is suggested.

Full Text

The Full Text of this article is available as a PDF (218.5 KB).

Selected References

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

  1. Aitken A., Rouviere-Yaniv J. Amino and carboxy terminal sequences of the DNA-binding protein HU from the Cyanobacterium Synechocystis PCC 6701 (ATCC 27170). Biochem Biophys Res Commun. 1979 Nov 28;91(2):461–467. doi: 10.1016/0006-291x(79)91544-4. [DOI] [PubMed] [Google Scholar]
  2. Bolivar F., Rodriguez R. L., Greene P. J., Betlach M. C., Heyneker H. L., Boyer H. W., Crosa J. H., Falkow S. Construction and characterization of new cloning vehicles. II. A multipurpose cloning system. Gene. 1977;2(2):95–113. [PubMed] [Google Scholar]
  3. Bonnefoy E., Rouvière-Yaniv J. HU and IHF, two homologous histone-like proteins of Escherichia coli, form different protein-DNA complexes with short DNA fragments. EMBO J. 1991 Mar;10(3):687–696. doi: 10.1002/j.1460-2075.1991.tb07998.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bonnefoy E., Takahashi M., Yaniv J. R. DNA-binding parameters of the HU protein of Escherichia coli to cruciform DNA. J Mol Biol. 1994 Sep 16;242(2):116–129. doi: 10.1006/jmbi.1994.1563. [DOI] [PubMed] [Google Scholar]
  5. Boubrik F., Bonnefoy E., Rouvière-Yaniv J. HU and IHF: similarities and differences. In Escherichia coli, the lack of HU is not compensated for by IHF. Res Microbiol. 1991 Feb-Apr;142(2-3):239–247. doi: 10.1016/0923-2508(91)90036-a. [DOI] [PubMed] [Google Scholar]
  6. Craig N. L., Nash H. A. E. coli integration host factor binds to specific sites in DNA. Cell. 1984 Dec;39(3 Pt 2):707–716. doi: 10.1016/0092-8674(84)90478-1. [DOI] [PubMed] [Google Scholar]
  7. DeLange R. J., Williams L. C., Searcy D. G. A histone-like protein (HTa) from Thermoplasma acidophilum. II. Complete amino acid sequence. J Biol Chem. 1981 Jan 25;256(2):905–911. [PubMed] [Google Scholar]
  8. Delic-Attree I., Toussaint B., Vignais P. M. Cloning and sequence analyses of the genes coding for the integration host factor (IHF) and HU proteins of Pseudomonas aeruginosa. Gene. 1995 Feb 27;154(1):61–64. doi: 10.1016/0378-1119(94)00875-s. [DOI] [PubMed] [Google Scholar]
  9. Devereux J., Haeberli P., Smithies O. A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res. 1984 Jan 11;12(1 Pt 1):387–395. doi: 10.1093/nar/12.1part1.387. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Douillié A., Toussaint A., Faelen M. Identification of the integration host factor genes of Erwinia chrysanthemi 3937. Biochimie. 1994;76(10-11):1055–1062. doi: 10.1016/0300-9084(94)90030-2. [DOI] [PubMed] [Google Scholar]
  11. Drlica K., Rouviere-Yaniv J. Histonelike proteins of bacteria. Microbiol Rev. 1987 Sep;51(3):301–319. doi: 10.1128/mr.51.3.301-319.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Flamm E. L., Weisberg R. A. Primary structure of the hip gene of Escherichia coli and of its product, the beta subunit of integration host factor. J Mol Biol. 1985 May 25;183(2):117–128. doi: 10.1016/0022-2836(85)90206-2. [DOI] [PubMed] [Google Scholar]
  13. Fleischmann R. D., Adams M. D., White O., Clayton R. A., Kirkness E. F., Kerlavage A. R., Bult C. J., Tomb J. F., Dougherty B. A., Merrick J. M. Whole-genome random sequencing and assembly of Haemophilus influenzae Rd. Science. 1995 Jul 28;269(5223):496–512. doi: 10.1126/science.7542800. [DOI] [PubMed] [Google Scholar]
  14. Giladi H., Wang W. X., Oppenheim A. B. Isolation and characterization of the hupA gene coding for HU of Aeromonas proteolytica. Nucleic Acids Res. 1992 Aug 11;20(15):4092–4092. doi: 10.1093/nar/20.15.4092. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Givskov M., Olsen L., Molin S. Cloning and expression in Escherichia coli of the gene for extracellular phospholipase A1 from Serratia liquefaciens. J Bacteriol. 1988 Dec;170(12):5855–5862. doi: 10.1128/jb.170.12.5855-5862.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Greene J. R., Brennan S. M., Andrew D. J., Thompson C. C., Richards S. H., Heinrikson R. L., Geiduschek E. P. Sequence of the bacteriophage SP01 gene coding for transcription factor 1, a viral homologue of the bacterial type II DNA-binding proteins. Proc Natl Acad Sci U S A. 1984 Nov;81(22):7031–7035. doi: 10.1073/pnas.81.22.7031. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Haluzi H., Goitein D., Koby S., Mendelson I., Teff D., Mengeritsky G., Giladi H., Oppenheim A. B. Genes coding for integration host factor are conserved in gram-negative bacteria. J Bacteriol. 1991 Oct;173(19):6297–6299. doi: 10.1128/jb.173.19.6297-6299.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Higgins N. P., Hillyard D. Primary structure and mapping of the hupA gene of Salmonella typhimurium. J Bacteriol. 1988 Dec;170(12):5751–5758. doi: 10.1128/jb.170.12.5751-5758.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Kano Y., Osato K., Wada M., Imamoto F. Cloning and sequencing of the HU-2 gene of Escherichia coli. Mol Gen Genet. 1987 Sep;209(2):408–410. doi: 10.1007/BF00329674. [DOI] [PubMed] [Google Scholar]
  20. Kano Y., Yoshino S., Wada M., Yokoyama K., Nobuhara M., Imamoto F. Molecular cloning and nucleotide sequence of the HU-1 gene of Escherichia coli. Mol Gen Genet. 1985;201(2):360–362. doi: 10.1007/BF00425687. [DOI] [PubMed] [Google Scholar]
  21. Khanaka H., Laine B., Sautiere P., Guillaume J. Characterization and primary structures of DNA-binding HU-type proteins from Rhizobiaceae. Eur J Biochem. 1985 Mar 1;147(2):343–349. doi: 10.1111/j.1432-1033.1985.tb08755.x. [DOI] [PubMed] [Google Scholar]
  22. Kimura M., Wilson K. S. On the DNA binding protein II from Bacillus stearothermophilus. II. The amino acid sequence and its relation to those of homologous proteins from other prokaryotes. J Biol Chem. 1983 Mar 25;258(6):4007–4011. [PubMed] [Google Scholar]
  23. Konkel M. E., Marconi R. T., Mead D. J., Cieplak W., Jr Cloning and expression of the hup encoding a histone-like protein of Campylobacter jejuni. Gene. 1994 Aug 19;146(1):83–86. doi: 10.1016/0378-1119(94)90837-0. [DOI] [PubMed] [Google Scholar]
  24. Laine B., Bélaïche D., Khanaka H., Sautière P. Primary structure of the DNA-binding protein HRm from Rhizobium meliloti. Eur J Biochem. 1983 Mar 15;131(2):325–331. doi: 10.1111/j.1432-1033.1983.tb07265.x. [DOI] [PubMed] [Google Scholar]
  25. Li Z. J., Hillyard D., Higgins P. Nucleotide sequence of the Salmonella typhimurium himA gene. Nucleic Acids Res. 1989 Nov 11;17(21):8880–8880. doi: 10.1093/nar/17.21.8880. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Marsh M., Hillyard D. R. Nucleotide sequence of the HU-1 gene of Salmonella typhimurium. Nucleic Acids Res. 1988 Jul 25;16(14B):7196–7196. doi: 10.1093/nar/16.14.7196. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Miller H. I. Primary structure of the himA gene of Escherichia coli: homology with DNA-binding protein HU and association with the phenylalanyl-tRNA synthetase operon. Cold Spring Harb Symp Quant Biol. 1984;49:691–698. doi: 10.1101/sqb.1984.049.01.078. [DOI] [PubMed] [Google Scholar]
  28. Nagaraja R., Haselkorn R. Protein HU from the cyanobacterium Anabaena. Biochimie. 1994;76(10-11):1082–1089. doi: 10.1016/0300-9084(94)90034-5. [DOI] [PubMed] [Google Scholar]
  29. Neilan J. G., Lu Z., Kutish G. F., Sussman M. D., Roberts P. C., Yozawa T., Rock D. L. An African swine fever virus gene with similarity to bacterial DNA binding proteins, bacterial integration host factors, and the Bacillus phage SPO1 transcription factor, TF1. Nucleic Acids Res. 1993 Mar 25;21(6):1496–1496. doi: 10.1093/nar/21.6.1496. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Oberto J., Drlica K., Rouvière-Yaniv J. Histones, HMG, HU, IHF: Même combat. Biochimie. 1994;76(10-11):901–908. doi: 10.1016/0300-9084(94)90014-0. [DOI] [PubMed] [Google Scholar]
  31. Padas P. M., Wilson K. S., Vorgias C. E. The DNA-binding protein HU from mesophilic and thermophilic bacilli: gene cloning, overproduction and purification. Gene. 1992 Aug 1;117(1):39–44. doi: 10.1016/0378-1119(92)90487-a. [DOI] [PubMed] [Google Scholar]
  32. Painbéni E., Mouray E., Gottesman S., Rouvière-Yaniv J. An imbalance of HU synthesis induces mucoidy in Escherichia coli. J Mol Biol. 1993 Dec 20;234(4):1021–1037. doi: 10.1006/jmbi.1993.1656. [DOI] [PubMed] [Google Scholar]
  33. Pontiggia A., Negri A., Beltrame M., Bianchi M. E. Protein HU binds specifically to kinked DNA. Mol Microbiol. 1993 Feb;7(3):343–350. doi: 10.1111/j.1365-2958.1993.tb01126.x. [DOI] [PubMed] [Google Scholar]
  34. Rouvière-Yaniv J., Gros F. Characterization of a novel, low-molecular-weight DNA-binding protein from Escherichia coli. Proc Natl Acad Sci U S A. 1975 Sep;72(9):3428–3432. doi: 10.1073/pnas.72.9.3428. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Rouvière-Yaniv J., Kjeldgaard N. O. Native Escherichia coli HU protein is a heterotypic dimer. FEBS Lett. 1979 Oct 15;106(2):297–300. doi: 10.1016/0014-5793(79)80518-9. [DOI] [PubMed] [Google Scholar]
  36. Rouvière-Yaniv J., Yaniv M., Germond J. E. E. coli DNA binding protein HU forms nucleosomelike structure with circular double-stranded DNA. Cell. 1979 Jun;17(2):265–274. doi: 10.1016/0092-8674(79)90152-1. [DOI] [PubMed] [Google Scholar]
  37. Sanger F., Coulson A. R., Barrell B. G., Smith A. J., Roe B. A. Cloning in single-stranded bacteriophage as an aid to rapid DNA sequencing. J Mol Biol. 1980 Oct 25;143(2):161–178. doi: 10.1016/0022-2836(80)90196-5. [DOI] [PubMed] [Google Scholar]
  38. Studier F. W., Moffatt B. A. Use of bacteriophage T7 RNA polymerase to direct selective high-level expression of cloned genes. J Mol Biol. 1986 May 5;189(1):113–130. doi: 10.1016/0022-2836(86)90385-2. [DOI] [PubMed] [Google Scholar]
  39. Tanaka I., Appelt K., Dijk J., White S. W., Wilson K. S. 3-A resolution structure of a protein with histone-like properties in prokaryotes. Nature. 1984 Aug 2;310(5976):376–381. doi: 10.1038/310376a0. [DOI] [PubMed] [Google Scholar]
  40. Toussaint B., Bosc C., Richaud P., Colbeau A., Vignais P. M. A mutation in a Rhodobacter capsulatus gene encoding an integration host factor-like protein impairs in vivo hydrogenase expression. Proc Natl Acad Sci U S A. 1991 Dec 1;88(23):10749–10753. doi: 10.1073/pnas.88.23.10749. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Toussaint B., Delic-Attree I., De Sury D'Aspremont R., David L., Vinçon M., Vignais P. M. Purification of the integration host factor homolog of Rhodobacter capsulatus: cloning and sequencing of the hip gene, which encodes the beta subunit. J Bacteriol. 1993 Oct;175(20):6499–6504. doi: 10.1128/jb.175.20.6499-6504.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Wang S. L., Liu X. Q. The plastid genome of Cryptomonas phi encodes an hsp70-like protein, a histone-like protein, and an acyl carrier protein. Proc Natl Acad Sci U S A. 1991 Dec 1;88(23):10783–10787. doi: 10.1073/pnas.88.23.10783. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Weiss D. S., Batut J., Klose K. E., Keener J., Kustu S. The phosphorylated form of the enhancer-binding protein NTRC has an ATPase activity that is essential for activation of transcription. Cell. 1991 Oct 4;67(1):155–167. doi: 10.1016/0092-8674(91)90579-n. [DOI] [PubMed] [Google Scholar]
  44. Zierer R., Choli D. The primary structure of DNA binding protein II from the extreme thermophilic bacterium Thermus thermophilus. FEBS Lett. 1990 Oct 29;273(1-2):59–62. doi: 10.1016/0014-5793(90)81050-x. [DOI] [PubMed] [Google Scholar]

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

RESOURCES