Deletion of the archaeal histone in Methanosarcina mazei Gö1 results in reduced growth and genomic transcription

Molecular Microbiology

Volumn 67, Issue 3, 2008, Pages 662-671

  Weidenbach, Katrin ^a   Glöer, Jens ^a   Ehlers, Claudia ^a   Sandman, Kathleen ^b   Reeve, John N ^b   Schmitz, Ruth A ^a  

^a UNIVERSITY OF KIEL   (Germany)

^b OHIO STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AROMATIC AMINO ACID; CORRINOID METHYLTRANSFERASE; HISTONE; METHANOL; METHYLTRANSFERASE; PROTEIN HMM; PUROMYCIN; SMALL HEAT SHOCK PROTEIN; TRIMETHYLAMINE; UNCLASSIFIED DRUG;

ARCHAEBACTERIUM; ARTICLE; BACTERIAL GENE; BACTERIAL GROWTH; BACTERIAL STRAIN; CONTROLLED STUDY; DNA BINDING; ESCHERICHIA COLI; GENE INSERTION; GENETIC TRANSCRIPTION; GENOTYPE; METHANOSARCINA; METHANOSARCINA MAZEI; NONHUMAN; OPERON; PAC GENE; PLASMID; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN FUNCTION; PROTEIN SYNTHESIS; RADIOSENSITIVITY; TRANSCRIPTION REGULATION; ULTRAVIOLET RADIATION; WILD TYPE;

ARCHAEAL PROTEINS; DNA, ARCHAEAL; DNA-BINDING PROTEINS; GENE DELETION; GENE EXPRESSION PROFILING; GENETIC COMPLEMENTATION TEST; HISTONES; METHANOL; METHANOSARCINA; METHYLAMINES; MUTAGENESIS, INSERTIONAL; PROTEIN BINDING; RECOMBINANT PROTEINS; TRANSCRIPTION, GENETIC; ULTRAVIOLET RAYS;

ARCHAEA; ESCHERICHIA COLI; METHANOSARCINA MAZEI; METHANOSARCINA MAZEI GO1;

EID: 37749047864     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2007.06076.x     Document Type: Article

References (55)

1. Arfin, S.M., Long, A.D., Ito, E.T., Tolleri, L., Riehle, M.M., Paegle, E.S. Hatfield, G.W. (2000) Global gene expression profiling in Escherichia coli K12. The effects of integration host factor. J Biol Chem 275 : 29672 29684.
2. Azam, T.A. Ishihama, A. (1999) Twelve species of the nucleoid-associated protein from Escherichia coli. Sequence recognition specificity and DNA binding affinity. J Biol Chem 274 : 33105 33113.
3. Bailey, K.A., Pereira, S.L., Widom, J. Reeve, J.N. (2000) Archaeal histone selection of nucleosome positioning sequences and the procaryotic origin of histone-dependent genome evolution. J Mol Biol 303 : 25 34.
4. Bradford, M.M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72 : 248 254.
5. Cam, E.L., Culard, F., Larquet, E., Delain, E. Cognet, J.A. (1999) DNA bending induced by the archaebacterial histone-like protein MC1. J Mol Biol 285 : 1011 1021.
6. Cavicchioli, R. (2007) Archaea. Molecular and Cellular Biology. Washington, DC : American Society for Microbiology Press.
7. De Vuyst, G., Aci, S., Genest, D. Culard, F. (2005) Atypical recognition of particular DNA sequences by the archaeal chromosomal MC1 protein. Biochemistry 44 : 10369 10377.
8. DeLange, R.J., Williams, L.C. Searcy, D.G. (1981) A histone-like protein (HTa) from Thermoplasma acidophilum. II. Complete amino acid sequence. J Biol Chem 256 : 905 911.
9. Deppenmeier, U., Johann, A., Hartsch, T., Merkl, R., Schmitz, R.A., Martinez-Arias, R., et al. (2002) The genome of Methanosarcina mazei: evidence for lateral gene transfer between bacteria and archaea. J Mol Microbiol Biotechnol 4 : 453 461.
10. Dinger, M.E., Baillie, G.J. Musgrave, D.R. (2000) Growth phase-dependent expression and degradation of histones in the thermophilic archaeon Thermococcus zilligii. Mol Microbiol 36 : 876 885.
11. Dorman, C.J. Deighan, P. (2003) Regulation of gene expression by histone-like proteins in bacteria. Curr Opin Genet Dev 13 : 179 184.
12. Ehlers, C., Veit, K., Gottschalk, G. Schmitz, R.A. (2002) Functional organization of a single nif cluster in the mesophilic archaeon Methanosarcina mazei strain Gö1. Archaea 1 : 143 150.
13. Ehlers, C., Weidenbach, K., Veit, K., Deppenmeier, U., Metcalf, W.W. Schmitz, R.A. (2005a) Development of genetic methods and construction of a chromosomal glnK(1) mutant in Methanosarcina mazei strain Gö1. Mol Genet Genomics 273 : 290 298.
14. Ehlers, C., Weidenbach, K., Veit, K., Forchhammer, K. Schmitz, R.A. (2005b) Unique mechanistic features of post-translational regulation of glutamine synthetase activity in Methanosarcina mazei strain Gö1 in response to nitrogen availability. Mol Microbiol 55 : 1841 1854.
15. Garrett, R.A. Klenk, H.-P. (2007) Archaea. Evolution, Physiology, and Molecular Biology. Oxford : Blackwell Publishing.
16. Gernhardt, P., Possot, O., Foglino, M., Sibold, L. Klein, A. (1990) Construction of an integration vector for use in the archaebacterium Methanococcus voltae and expression of a eubacterial resistance gene. Mol Gen Genet 221 : 273 279.
17. Grainger, D.C., Hurd, D., Goldberg, M.D. Busby, S.J. (2006) Association of nucleoid proteins with coding and non-coding segments of the Escherichia coli genome. Nucleic Acids Res 34 : 4642 4652.
18. Hays, S.M., Swanson, J. Selker, E.U. (2002) Identification and characterization of the genes encoding the core histones and histone variants of Neurospora crassa. Genetics 160 : 961 973.
19. Heinicke, I., Muller, J., Pittelkow, M. Klein, A. (2004) Mutational analysis of genes encoding chromatin proteins in the archaeon Methanococcus voltae indicates their involvement in the regulation of gene expression. Mol Genet Genomics 272 : 76 87.
20. Hommais, F., Krin, E., Laurent-Winter, C., Soutourina, O., Malpertuy, A., Le Caer, J.P., et al. (2001) Large-scale monitoring of pleiotropic regulation of gene expression by the prokaryotic nucleoid-associated protein, H-NS. Mol Microbiol 40 : 20 36.
21. Hovey, R., Lentes, S., Ehrenreich, A., Salmon, K., Saba, K., Gottschalk, G., et al. (2005) DNA microarray analysis of Methanosarcina mazei Gö1 reveals adaptation to different methanogenic substrates. Mol Genet Genomics 273 : 225 239.
22. Huisman, O., Faelen, M., Girard, D., Jaffe, A., Toussaint, A. Rouviere-Yaniv, J. (1989) Multiple defects in Escherichia coli mutants lacking HU protein. J Bacteriol 171 : 3704 3712.
23. Inoue, H., Nojima, H. Okayama, H. (1990) High efficiency transformation of Escherichia coli with plasmids. Gene 96 : 23 28.
24. Kar, S., Edgar, R. Adhya, S. (2005) Nucleoid remodeling by an altered HU protein: reorganization of the transcription program. Proc Natl Acad Sci USA 102 : 16397 16402.
25. Kelly, A., Goldberg, M.D., Carroll, R.K., Danino, V., Hinton, J.C. Dorman, C.J. (2004) A global role for Fis in the transcriptional control of metabolism and type III secretion in Salmonella enterica serovar Typhimurium. Microbiology 150 : 2037 2053.
26. Li, S. Waters, R. (1998) Escherichia coli strains lacking protein HU are UV sensitive due to a role for HU in homologous recombination. J Bacteriol 180 : 3750 3756.
27. Luger, K., Mader, A.W., Richmond, R.K., Sargent, D.F. Richmond, T.J. (1997) Crystal structure of the nucleosome core particle at 2.8 A resolution. Nature 389 : 251 260.
28. McLeod, S.M. Johnson, R.C. (2001) Control of transcription by nucleoid proteins. Curr Opin Microbiol 4 : 152 159.
29. Mangan, M.W., Lucchini, S., Danino, V., Croinin, T.O., Hinton, J.C. Dorman, C.J. (2006) The integration host factor (IHF) integrates stationary-phase and virulence gene expression in Salmonella enterica serovar Typhimurium. Mol Microbiol 59 : 1831 1847.
30. Manzur, K.L. Zhou, M.M. (2005) An archaeal SET domain protein exhibits distinct lysine methyltransferase activity towards DNA-associated protein MC1-alpha. FEBS Lett 579 : 3859 3865.
31. Marc, F., Sandman, K., Lurz, R. Reeve, J.N. (2002) Archaeal histone tetramerization determines DNA affinity and the direction of DNA supercoiling. J Biol Chem 277 : 30879 30886.
32. Marino-Ramirez, L., Hsu, B., Baxevanis, A.D. Landsman, D. (2006) The histone database: a comprehensive resource for histones and histone fold-containing proteins. Proteins 62 : 838 842.
33. Metcalf, W.W., Zhang, J.K., Apolinario, E., Sowers, K.R. Wolfe, R.S. (1997) A genetic system for Archaea of the genus Methanosarcina: liposome-mediated transformation and construction of shuttle vectors. Proc Natl Acad Sci USA 94 : 2626 2631.
34. Nakano, Y., Yoshida, Y., Yamashita, Y. Koga, T. (1995) Construction of a series of pACYC-derived plasmid vectors. Gene 162 : 157 158.
35. Oshima, T., Ishikawa, S., Kurokawa, K., Aiba, H. Ogasawara, N. (2006) Escherichia coli histone-like protein H-NS preferentially binds to horizontally acquired DNA in association with RNA polymerase. DNA Res 13 : 141 153.
36. Paquet, F., Culard, F., Barbault, F., Maurizot, J.C. Lancelot, G. (2004) NMR solution structure of the archaebacterial chromosomal protein MC1 reveals a new protein fold. Biochemistry 43 : 14971 14978.
37. Reeve, J.N. (2003) Archaeal chromatin and transcription. Mol Microbiol 48 : 587 598.
38. Reeve, J.N. Sandman, K. (2007) Chromatin regulation. In Archaea, Evolution, Physiology and Molecular Biology. Garrett, R.A. Klenk, H.-P. (eds). Oxford : Blackwell Publishing, pp. 147 157.
39. Rimsky, S. (2004) Structure of the histone-like protein H-NS and its role in regulation and genome superstructure. Curr Opin Microbiol 7 : 109 114.
40. Rogers, J.E. Whiteman, W.B. (eds) (1991) Microbial production and consumption of greenhouse gases: methane, nitrogen oxides and halomethanes. Washington, DC : American Society for Microbiology Press.
41. Sambrook, J., Fritsch E.F. Maniatis T. (1989) Molecular Cloning: A Laboratory Manual. New York : Cold Spring Harbor Laboratory Press.
42. Sandman, K., Krzycki, J.A., Dobrinski, B., Lurz, R. Reeve, J.N. (1990) HMf, a DNA-binding protein isolated from the hyperthermophilic archaeon Methanothermus fervidus, is most closely related to histones. Proc Natl Acad Sci USA 87 : 5788 5791.
43. Sandman, K., Grayling, R.A., Dobrinski, B., Lurz, R. Reeve, J.N. (1994) Growth-phase-dependent synthesis of histones in the archaeon Methanothermus fervidus. Proc Natl Acad Sci USA 91 : 12624 12628.
44. Sandman, K., Bailey, K.A., Pereira, S.L., Soares, D., Li, W.T. Reeve, J.N. (2001) Archaeal histones and nucleosomes. Methods Enzymol 334 : 116 129.
45. Schagger, H. von Jagow, G. (1987) Tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa. Anal Biochem 166 : 368 379.
46. Slesarev, A.I., Belova, G.I., Kozyavkin, S.A. Lake, J.A. (1998) Evidence for an early prokaryotic origin of histones H2A and H4 prior to the emergence of eukaryotes. Nucleic Acids Res 26 : 427 430.
47. Struhl, K. (1999) Fundamentally different logic of gene regulation in eukaryotes and prokaryotes. Cell 98 : 1 4.
48. Talaat, A.M., Lyons, R., Howard, S.T. Johnston, S.A. (2004) The temporal expression profile of Mycobacterium tuberculosis infection in mice. Proc Natl Acad Sci USA 101 : 4602 4607.
49. Teyssier, C., Laine, B., Gervais, A., Maurizot, J.C. Culard, F. (1994) Archaebacterial histone-like protein MC1 can exhibit a sequence-specific binding to DNA. Biochem J 303 (Part 2 567 573.
50. Travers, A. Muskhelishvili, G. (2005) Bacterial chromatin. Curr Opin Genet Dev 15 : 507 514.
51. Veit, K., Ehlers, C. Schmitz, R.A. (2005) Effects of nitrogen and carbon sources on transcription of soluble methyltransferases in Methanosarcina mazei strain Gö1. J Bacteriol 187 : 6147 6154.
52. Veit, K., Ehlers, C., Ehrenreich, A., Salmon, K., Hovey, R., Gunsalus, R.P., et al. (2006) Global transcriptional analysis of Methanosarcina mazei strain Gö1 under different nitrogen availabilities. Mol Genet Genomics 276 : 41 55.
53. Wada, M., Kano, Y., Ogawa, T., Okazaki, T. Imamoto, F. (1988) Construction and characterization of the deletion mutant of hupA and hupB genes in Escherichia coli. J Mol Biol 204 : 581 591.
54. Wyrick, J.J., Holstege, F.C., Jennings, E.G., Causton, H.C., Shore, D., Grunstein, M., et al. (1999) Chromosomal landscape of nucleosome-dependent gene expression and silencing in yeast. Nature 402 : 418 421.
55. Yuan, G.C., Liu, Y.J., Dion, M.F., Slack, M.D., Wu, L.F., Altschuler, S.J. Rando, O.J. (2005) Genome-scale identification of nucleosome positions in S. cerevisiae. Science 309 : 626 630.