Summary
DNA fragments bearing sequence similarity to eubacterialnifH probes were cloned from two nitrogen-fixing archaebacteria, a thermophilic methanogen,Methanococcus (Mc.) thermolithotrophicus, and a mesophilic methanogen,Methanobacterium (Mb.) ivanovii. Regions carrying similarities with the probes were sequenced. They contained several open reading frames (ORF), separated by A+T-rich regions. The largest ORFs in both regions, an 876-bp sequence inMc. thermolithotrophicus and a 789-bp sequence inMb.ivanovii, were assumed to be ORFsnifH. They code for polypeptides of mol. wt. 32,025 and 28,347, respectively. Both ORFsnifH were preceded by potential ribosome binding sites and followed by potential hairpin structures and by oligo-T sequences, which may act as transcription termination signals. The codon usage was similar in both ORFsnifH and was analogous to that used in theClostridium pasteurianum nifH gene, with a preference for codons ending with A or U. The ORFnifH deduced polypeptides contained 30% sequence matches with all eubacterialnifH products already sequenced. Four cysteine residues were found at the same position in all sequences, and regions surrounding the cysteine residues are highly conserved. Comparison of all pairs of methanogenic and eubacterialnifH sequences is in agreeement with a distant phylogenetic position of archaebacteria and with a very ancient origin ofnif genes. However, sequence similarity between Methanobacteriales and Methanococcales is low (around 50%) as compared to that found among eubacteria, suggesting a profound divergence between the two orders of methanogens. From comparison of amino acid sequences,C. pasteurianum groups with the other eubacteria, whereas comparison of nucleotide sequences seems to bringC. pasteurianum closer to methanogens. The latter result may be due to the high A+T content of bothC. pasteurianum and methanogens ORFsnifH or may come from an ancient lateral transfer betweenClostridium and methanogens.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
References
Avtges P, Scolnik PA, Haselkorn R (1983) Genetic and physical map of the structural genes (nifHDK) coding for the nitrogenase complex ofRhodopseudomonas capsulata. J Bacteriol 156:251–256
Balch WE, Fox GE, Magrum LJ, Woese CR, Wolfe RS (1979) Methanogens: reevaluation of a unique biological group. Microbiol Rev 43:260–293
Belay N, Sparling R, Daniels L (1984) Dinitrogen fixation by a thermophilic methanogenic bacterium. Nature 312:286–288
Belyaev SS, Wolkin R, Kenealy WR, De Niro MJ, Epstein S, Zeikus JG (1983) Methanogenic bacteria from the Bondyuzhskoe oil field: general characterization and analysis of stable-carbon isotopic fractionation. Appl Environ Microbiol 45:691–697
Bomar M, Knoll K, Widdel F (1985) Fixation of molecular nitrogen byMethanosarcina barkeri. FEMS Microbiol Ecol Lett 31:47–55
Breathnach R, Chambon P (1981) Organization and expression of eukaryotic split genes coding for proteins. Annu Rev Biochem 50:349–383
Brigle KE, Newton WE, Dean DR (1985) Complete nucleotide sequence of theAzotobacter vinelandii nitrogenase structural gene cluster. Gene 37:37–44
Cannon FC, Riedel GE, Ausubel FM (1979) Overlapping sequences ofK. pneumoniae nif DNA cloned and characterized. Mol Gen Genet 174:59–66
Chen KCK, Chen JS, Johnson JL (1986) Structural features of multiplenifH-like sequences and very biased codon usage in nitrogenase genes ofClostridium pasteurianum. J Bacteriol 166:162–172
Denèfle P, Kush A, Norel F, Paquelin A, Elmerich C (1987) Biochemical and genetic analysis of thenifHDKE region of Rhizobium ORS571. Mol Gen Genet 207:280–287
Dennis PP (1986) Molecular biology of archaebacteria. J Bacteriol 168:471–478
Dixon R (1984) The genetic complexity of nitrogen fixation. J Gen Microbiol 130:2745–2755
Donald RGK, Nees DW, Raymond CK, Loroch AI, Ludwig RA (1986) Characterization of three genomic loci encodingRhizobium sp. strain ORS571 N2 fixation genes. J Bacteriol 165:72–81
Eady RR, Smith BE (1979) Physico-chemical properties of nitrogenase and its components. In: Hardy RWF, Bottomley F, Burns RC (eds) A treatise on dinitrogen fixation, sections I and II. Wiley and Sons, London, pp 399–490
Elmerich C, Houmard J, Sibold L, Manheimer I, Charpin N (1978) Genetic and biophysical analysis of mutants induced by bacteriophage Mu DNA integration intoKlebsiella pneumoniae nitrogen fixation genes. Mol Gen Genet 165:181–189
Frischauf AM, Lehrach H, Poustka A, Murray N (1983) Lambda replacement vectors carrying polylinker sequences. J Mol Biol 170:827–842
Fuhrmann M, Hennecke H (1984)Rhizobium japonicum nitrogenase Fe protein gene (nifH). J Bacteriol 158:1005–1011
Hamilton W, Reeve JN (1985a) Structure of genes and an insertion element in the methane producing archaebacteriumMethanobrevibacter smithii. Mol Gen Genet 200:47–59
Hamilton W, Reeve JN (1985b) Sequence divergence of an archaebacterial gene cloned from a mesophilic and a thermophilic methanogen. J Mol Evol 22:351–360
Hennecke H, Kaluza K, Thöny B, Fuhrmann M, Ludwig W, Stackebrandt E (1985) Concurrent evolution of nitrogenase genes and 16S rRNA inRhizobium species and other nitrogen fixing bacteria. Arch Microbiol 142:342–348
Higgins CF, Hiles ID, Salmond GPC, Gill DR, Downie JA, Evans IJ, Holland IB, Gray L, Buckel SD, Bell AW, Hermodson MA (1986) A family of related ATP-binding subunits coupled to many distinct biological processes in bacteria. Nature 323:448–453
Huber H, Thomm M, König H, Thies G, Stetter KO (1982)Methanococcus thermolithotrophicus, a novel thermophilic lithotrophic methanogen. Arch Microbiol 132:47–50
Jain MK, Thompson TE, Conway de Macario E, Zeikus JG (1987) Speciation ofMethanobacterium strain Ivanov asMethanobacterium invanovii, sp. nov. System Appl. Microbiol 9:77–82
Jones R, Woodley P, Robson R (1984) Cloning and organisation of some genes for nitrogen fixation forAzotobacter chroococcum and their expression inKlebsiella pneumoniae. Mol Gen Genet 197:318–327
Kallas T, Rebiere MC, Rippka R, Tandeau de Marsac N (1983) The structuralnif genes of the cyanobacteriaGloeothece sp. andCalothrix sp. share homology withAnabaena sp. but theGloeothece genes have a different arrangement. J Bacteriol 155:427–431
König H, Nusser E, Stetter KO (1985) Glycogen inMethanolobus andMethanococcus. FEMS Microbiol Lett 28:265–269
Krol ADM, Hondelez JGJ, Roozendaal B, van Kammen A (1981) On the operon structure of the nitrogenase genes ofRhizobium leguminosarum andAzotobacter vinelandii. Nucleic Acids Res 10:4147–4156
Lipman WJ, Wilbur DJ (1983) Rapid similarity searches of nucleic acid and protein data banks. Proc Natl Acad Sci USA 80:726–730
Magot M, Possot O, Souillard N, Henriquet M, Sibold L (1986) Structure and expression ofnif (nitrogen fixation) genes in methanogens. In: Dubourguier HC, Albagnac G, Montreuil J, Romond C, Sautiere P, Guillaume J (eds) Biology of anaerobic bacteria. Elsevier, Amsterdam, pp 193–199
Maniatis T, Fritsch E, Sambrook J (1982) Molecular cloning, a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor NY
Marlière P, Kofoid EC, Ganoza MC (1987) Can the T loop of initiator tRNA act as a second anticodon? Ann Inst Pasteur (Microbiology) (in press)
Mevarech M, Rice D, Haselkorn R (1980) Nucleotide sequence of a cyanobacterialnifH gene coding for nitrogenase reductase. Proc Natl Acad Sci USA 77:6476–6480
Merrick M, Filser M, Kennedy C Dixon R (1978) Polarity of mutations induced by insertion of transposon Tn5, Tn7 and Tn10 into thenif gene cluster ofKlebsiella pneumoniae. Mol Gen Genet 165:103–111
Murray PA, Zinder S (1984) Nitrogen fixation by a methanogenic archaebacterium. Nature 312:284–286
Norel F, Elmerich C (1987) Nucleotide sequence and functional analysis of the twonifH copies ofRhizobium ORS571. J Gen Microbiol 133:1563–1576
Perroud B, Bandhari SK, Elmerich C (1985) ThenifHDK operon ofAzospirillum brasilense Sp7. In: Klingmüller W (ed) Azospirillum III: genetics, physiology, ecology. Springer, Berlin, pp 10–19
Possot O, Henry M, Sibold L (1986) Distribution of DNA sequences homologous tonifH among archaebacteria. FEMS Microbiol Lett 34:173–177
Quinto C, de la Vega H, Flores M, Leemans J, Cevallos MA, Pardo MA, Azpiroz R, de Lourdes Girard M, Calva E, Palacios R (1985) Nitrogenase reductase: a functional multigene family inRhizobium phaseoli. Proc Natl Acad Sci USA 82:1170–1174
Reeve JN, Hamilton PT, Beckler GS, Morris CJ, Clarke CH (1986) Structure of methanogens genes. Syst Appl Microbiol 7:5–12
Rice D, Mazur BJ, Haselkorn R (1982) Isolation and physical mapping of nitrogen fixation genes from the cyanobacteriumAnabaena 7120. J Biol Chem 257:13157–13163
Robson RL (1984) Identification of possible adenine nucleotide-binding sites in nitrogenase Fe- and MoFe-proteins by amino acid sequence comparison. FEBS Lett 173:394–398
Robson R, Woodley P, Jones R (1986) Second gene (nifH *) coding for a nitrogenase iron protein inAzotobacter chroococcum is adjacent to a gene coding for a ferredoxin-like protein. EMBO J 5:1159–1163
Ruvkun GB, Ausubel FM (1980) Interspecies homology of nitrogenase genes. Proc Natl Acad Sci USA 77:191–195
Ruvkun GB, Sundaresan V, Ausubel FM (1982) Directed transposon Tn5 mutagenesis and complementation analysis ofRhizobium meliloti symbiotic nitrogen fixations genes. Cell 29:551–555
Sanger F, Nicklen S, Coulson AR (1977) DNA sequencing with chain terminating inhibitors. Proc Natl Acad Sci USA 74:5463–5467
Schetgens TMP, Bakkeren G, van Dun C, Hontelez JGJ, van Kammen A, van den Bos RC (1984) Identification and analysis of the expression ofRhizobium leguminosarum PRE symbiotic genes. In: Veeger C, Newton WE (eds) Advances in nitrogen fixation research. Martinus Nijhoff, Dr W Junk, The Hague, Netherlands, p 699
Scott KF, Rolfe GB, Shine J (1981) Biological nitrogen fixation: primary structure of theKlebsiella pneumoniae nifH andnifD genes. J Mol Appl Genet 1:71–81
Scott KF, Rolfe GB, Shine J (1983a) Nitrogenase structural genes are unlinked in the nonlegume symbiot ParasponiaRhizobium. DNA 2:141–148
Scott KF, Rolfe GB, Shine J (1983b) Biological nitrogen fixation: primary structure of theRhizobium trifolii iron protein gene. DNA 2:149–155
Shine J, Dalgarno L (1974) The 3′-terminal sequence ofEscherichia coli 16S ribosomal RNA: complementarity to nonsense triplets and ribosome binding sites. Proc Natl Acad Sci USA 71:1342–1346
Sibold L, Pariot D, Bhatnagar L, Henriquet M, Aubert JP (1985) Hybridization of DNA from methanogenic bacteria with nitrogenase structural genes (nifHDK). Mol Gen Genet 200:40–46
Souillard N, Sibold L (1986) Primary structure and expression of a gene homologous tonifH (nitrogenase Fe protein) from the archaebacteriumMethanococcus voltae. Mol Gen Genet 203:21–28
Sundaresan VK, Ausubel FM (1981) Nucleotide sequence of the gene coding for nitrogenase iron protein fromKlebsiella pneumoniae. J Biol Chem 256:2808–2812
Török I, Kondorosi A (1981) Nucleotide sequence of theR. meliloti nitrogenase reductase (nifH) gene. Nucleic Acids Res 9:5711–5723
Vieira J, Messing J (1982) The pUC plasmids, an M13mp7-derived system for insertion mutagenesis and sequencing with synthetic universal primers. Gene 129:259–268
Wain-Hobson S, Sonigo P, Danos O, Cole S, Alizon M (1985) Nucleotide sequence of the AIDS virus, LAV. Cell 40:9–17
Wich G, Hummel H, Jarsch M, Bar U, Böck A (1986) Transcription signals for stable RNA genes inMethanococcus. Nucleic Acids Res 14:2459–2478
Whitman WB (1985) Methanogenic bacteria. In: Woese CR, Wolfe RS (eds) Archaebacteria. Academic Press, New York, pp 4–84
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Souillard, N., Magot, M., Possot, O. et al. Nucleotide sequence of regions homologous tonifH (nitrogenase Fe protein) from the nitrogen-fixing archaebacteriaMethanococcus thermolithotrophicus andMethanobacterium ivanovii: Evolutionary implications. J Mol Evol 27, 65–76 (1988). https://doi.org/10.1007/BF02099731
Received:
Revised:
Issue Date:
DOI: https://doi.org/10.1007/BF02099731