Archaea

Archaea / 2002 / Article

Research Article | Open Access

Volume 1 |Article ID 362813 | https://doi.org/10.1155/2002/362813

Claudia Ehlers, Katharina Veit, Gerhard Gottschalk, Ruth A. Schmitz, "Functional organization of a single nif cluster in the mesophilic archaeon Methanosarcina mazei strain Gö1", Archaea, vol. 1, Article ID 362813, 8 pages, 2002. https://doi.org/10.1155/2002/362813

Functional organization of a single nif cluster in the mesophilic archaeon Methanosarcina mazei strain Gö1

Received06 Jun 2002
Accepted10 Jul 2002

Abstract

The mesophilic methanogenic archaeon Methanosarcina mazei strain Gö1 is able to utilize molecular nitrogen (N2) as its sole nitrogen source. We have identified and characterized a single nitrogen fixation (nif) gene cluster in M. mazei Gö1 with an approximate length of 9 kbp. Sequence analysis revealed seven genes with sequence similarities to nifH, nifI1, nifI2, nifD, nifK, nifE and nifN, similar to other diazotrophic methanogens and certain bacteria such as Clostridium acetobutylicum, with the two glnB-like genes (nifI1 and nifI2) located between nifH and nifD. Phylogenetic analysis of deduced amino acid sequences for the nitrogenase structural genes of M. mazei Gö1 showed that they are most closely related to Methanosarcina barkeri nif2 genes, and also closely resemble those for the corresponding nif products of the gram-positive bacterium C. acetobutylicum. Northern blot analysis and reverse transcription PCR analysis demonstrated that the M. mazei nif genes constitute an operon transcribed only under nitrogen starvation as a single 8 kb transcript. Sequence analysis revealed a palindromic sequence at the transcriptional start site in front of the M. mazei nifH gene, which may have a function in transcriptional regulation of the nif operon.

References

  1. T. Arcondeguy, R. Jack, and M. Merrick, “The PII signal transduction proteins: pivotal players in microbial nitrogen control,” Microbiol. Mol. Biol. Rev., vol. 65, pp. 80–105, 2001. View at: Google Scholar
  2. S.D. Bell and S.P. Jackson, “Mechanism and regulation of transcription in archaea,” Curr. Opin. Microbiol., vol. 4, pp. 208–213, 2001. View at: Google Scholar
  3. C.J. Bult, O. White, G.J. Olsen et al., “Complete genome sequence of the methanogenic archaeon, Methanococcus jannaschii,” Science, vol. 273, pp. 1058–1073, 1996. View at: Google Scholar
  4. J.S. Chen, J. Toth, and M. Kasap, “Genbank submission AF266462,” 2001. View at: Google Scholar
  5. Y.T. Chien and S.H. Zinder, “Cloning, DNA sequencing, and characterization of a nifD-homologous gene from the archaeon Methanosarcina barkeri 227 which resembles nifD1 from the eubacterium Clostridium pasteurianum,” J. Bacteriol., vol. 176, pp. 6590–6598, 1994. View at: Google Scholar
  6. Y.T. Chien and S.H. Zinder, “Cloning, functional organization, transcript studies, and phylogenetic analysis of the complete nitrogenase structural genes (nifHDK2) and associated genes in the archaeon Methanosarcina barkeri 227,” J. Bacteriol., vol. 178, pp. 143–148, 1996. View at: Google Scholar
  7. Y.T. Chien, J.D. Helmann, and S.H. Zinder, “Interactions between the promoter regions of nitrogenase structural genes (nifHDK2) and DNA-binding proteins from N2- and ammonium-grown cells of the archaeon Methanosarcina barkeri 227,” J. Bacteriol., vol. 180, pp. 2723–2728, 1998. View at: Google Scholar
  8. Y.T. Chien, V. Auerbuch, A.D. Brabban, and S.H. Zinder, “Analysis of genes encoding an alternative nitrogenase in the archaeon Methanosarcina barkeri 227,” J. Bacteriol., vol. 182, pp. 3247–3253, 2000. View at: Google Scholar
  9. R. Cohen-Kupiec, C. Blank, and J.A. Leigh, “Transcriptional regulation in Archaea: in vivo demonstration of a repressor binding site in a methanogen,” Proc. Natl. Acad. Sci. USA, vol. 94, pp. 1316–1320, 1997. View at: Google Scholar
  10. D.R. Dean and M.R. Jacobson, “Biochemical genetics of nitrogenases,” in Biological Nitrogen Fixation, G. Stacey, R.H. Burris, and H.J. Evans, Eds., pp. 763–834, Chapman & Hall, New York, 1992. View at: Google Scholar
  11. D.R. Dean, J.T. Bolin, and L. Zheng, “Nitrogenase metalloclusters: structures, organization, and synthesis,” J. Bacteriol., vol. 175, pp. 6737–6744, 1993. View at: Google Scholar
  12. U. Deppenmeier, M. Blaut, A. Mahlmann, and G. Gottschalk, “Reduced coenzyme F420 H2-dependent heterodisulfide oxidoreductase: a proton translocating redox system in methanogenic bacteria,” Proc. Natl. Acad. Sci. USA, vol. 87, pp. 9449–9453, 1990. View at: Google Scholar
  13. U. Deppenmeier, A. Johann, T. Hartsch et al., “The genome of Methanosarcina mazei: evidence for lateral gene transfer between Bacteria and Archaea,” J. Mol. Microbiol. Biotechnol., vol. 4, pp. 453–461, 2002. View at: Google Scholar
  14. J. Devereux, P. Haeberli, and O. Smithies, “A comprehensive set of sequence analysis programs for the VAX,” Nucleic Acids Res., vol. 12, pp. 387–395, 1984. View at: Google Scholar
  15. C. Ehlers, R. Grabbe, K. Veit, and R.A. Schmitz, “Characterization of GlnK1 from Methanosarcina mazei strain Gö1: complementation of an Escherichia coli glnK mutant strain by M. mazei GlnK1.,” J. Bacteriol., vol. 184, pp. 1028–1040, 2002. View at: Google Scholar
  16. J.G. Ferry, “Enzymology of one-carbon metabolism in methanogenic pathways,” FEMS Microbiol. Rev., vol. 23, pp. 13–38, 1999. View at: Google Scholar
  17. H.M. Fischer, “Genetic regulation of nitrogen fixation in rhizobia,” Microbiol. Rev., vol. 58, pp. 352–386, 1994. View at: Google Scholar
  18. J.E. Galagan, C. Nusbaum, A. Roy et al., “The genome of M. acetivorans reveals extensive metabolic and physiological diversity.,” Genome Res., vol. 12, pp. 532–542, 2002. View at: Google Scholar
  19. M.M. Georgiadis, H. Komiya, P. Chakrabarti, D. Woo, J.J. Kornuc, and D.C. Rees, “Crystallographic structure of the nitrogenase iron protein from Azotobacter vinelandii,” Science, vol. 257, pp. 1653–1659, 1992. View at: Google Scholar
  20. R. Haselkorn and W.J. Buikema, “Methanococcus genome,” Science, vol. 274, pp. 901–902, 1996. View at: Google Scholar
  21. W. Hausner, J. Wettach, C. Hethke, and M. Thomm, “Two transcription factors related with the eucaryal transcription factors TATA-binding protein and transcription factor IIB direct promoter recognition by an archaeal RNA polymerase,” J. Biol. Chem., vol. 271, pp. 30144–30148, 1996. View at: Google Scholar
  22. P.S. Kessler and J.A. Leigh, “Genetics of nitrogen regulation in Methanococcus maripaludis,” Genetics, vol. 152, pp. 1343–1351, 1999. View at: Google Scholar
  23. P.S. Kessler, J. Mclarnan, and J.A. Leigh, “Nitrogenase phylogeny and the molybdenum dependence of nitrogen fixation in Methanococcus maripaludis,” J. Bacteriol., vol. 179, pp. 541–543, 1997. View at: Google Scholar
  24. P.S. Kessler, C. Blank, and J.A. Leigh, “The nif gene operon of the methanogenic archaeon Methanococcus maripaludis,” J. Bacteriol., vol. 180, pp. 1504–1511, 1998. View at: Google Scholar
  25. P.S. Kessler, K. Daniel, and J.A. Leigh, “Ammonium switch-off of nitrogen fixation in the methanogenic archeaon Methanococcus maripaludis: Mechanistic features and requirement for the novel GlnB homologues, NifI1 and NifI2,” J. Bacteriol., vol. 183, pp. 882–889, 2001. View at: Google Scholar
  26. D. Langer and W. Zillig, “Putative tfIIs gene of Sulfolobus acidocaldarius encoding an archaeal transcription elongation factor is situated directly downstream of the gene for a small subunit of DNA-dependent RNA polymerase,” Nucleic Acids Res., vol. 21, p. 2251, 1993. View at: Google Scholar
  27. D. Langer, J. Hain, P. Thuriaux, and W. Zillig, “Transcription in Archaea: similarity to that in Eucarya,” Proc. Natl. Acad. Sci. USA, vol. 92, pp. 5768–5772, 1995. View at: Google Scholar
  28. A.L. Lobo and S.H. Zinder, “Nitrogen fixation by methanogenic bacteria,” in Biological Nitrogen Fixation, G. Stacey, R.H. Burris, and H.J. Evans, Eds., pp. 191–211, Chapman & Hall, New York, 1992. View at: Google Scholar
  29. T.L. Marsh, C.I. Reich, R.B. Whitelock, and G.J. Olsen, “Transcription factor IID in the Archaea: sequences in the Thermococcus celer genome would encode a product closely related to the TATA-binding protein of eukaryotes,” Proc. Natl. Acad. Sci. USA, vol. 91, pp. 4180–4184, 1994. View at: Google Scholar
  30. M.J. Merrick and R.A. Edwards, “Nitrogen control in bacteria,” Microbiol. Rev., vol. 59, pp. 604–622, 1995. View at: Google Scholar
  31. J. Nölling, G. Breton, M.V. Omelchenko et al., “Genome sequence and comparative analysis of the solvent-producing bacterium Clostridium acetobutylicum,” J. Bacteriol., vol. 183, pp. 4823–4838, 2001. View at: Google Scholar
  32. S.A. Qureshi, B. Khoo, P. Baumann, and S.P. Jackson, “Molecular cloning of the transcription factor TFIIB homolog from Sulfolobus shibatae,” Proc. Natl. Acad. Sci. USA, vol. 92, pp. 6077–6081, 1995. View at: Google Scholar
  33. D.C. Rees and J.B. Howard, “Structural bioenergetics and energy transduction mechanisms,” J. Mol. Biol., vol. 293, pp. 343–350, 1999. View at: Google Scholar
  34. J. Sambrook, E.F. Fritsch, and T. Maniatis, “Molecular cloning: a laboratory manual,” in Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York., Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York, 2nd Edn. edition, 1989. View at: Google Scholar
  35. L. Sibold, M. Henriquet, O. Possot, and J.P. Aubert, “Nucleotide sequence of nifH regions from Methanobacterium ivanovii and Methanosarcina barkeri 227 and characterization of glnB-like genes,” Res. Microbiol., vol. 142, pp. 5–12, 1991. View at: Google Scholar
  36. D.R. Smith, L.A. Doucette-Stamm, C. Deloughery et al., “Complete genome sequence of Methanobacterium thermoautotrophicum ΔH: functional analysis and comparative genomics,” J. Bacteriol., vol. 179, pp. 7135–7155, 1997. View at: Google Scholar
  37. N. Souillard and L. Sibold, “Primary structure, functional organization and expression of nitrogenase structural genes of the thermophilic archaebacterium Methanococcus thermolithotrophicus,” Mol. Microbiol., vol. 3, pp. 541–551, 1989. View at: Google Scholar
  38. R. Staden, K.F. Beal, and J.K. Bonfield, “The Staden package,” Methods Mol. Biol., vol. 132, pp. 115–130, 2000. View at: Google Scholar
  39. R.K. Thauer, “Biochemistry of methanogenesis: a tribute to Marjory Stephenson 1998 Marjory Stephenson Prize Lecture,” Microbiology, vol. 144, pp. 2377–2406, 1998. View at: Google Scholar
  40. M. Thomm, “Die Transkriptionsmaschinerie der Archaea,” Biospektrum, vol. 3, pp. 179–185, 2000. View at: Google Scholar
  41. J.P.W. Young, “Phylogenetic classification of nitrogen fixing organisms,” in Biological Nitrogen Fixation, G. Stacey, R.H. Burris, and H.J. Evans, Eds., pp. 736–762, Chapman & Hall, New York, 1992. View at: Google Scholar

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