Summary
We have determined the DNA sequence of aRhizobium meliloti gene that encodes glutamine synthetase II (GSII). The deduced amino acid sequence was compared to that ofBradyrhizobium japonicum GSII and those of various plant and mammalian glutamine synthetases (GS) in order to evaluate a proposal that the gene for this enzyme was recently transferred from plants to their symbiotic bacteria. There is 83.6% identity between theR. meliloti andB. japonicum proteins. The bacterial GSII proteins average 42.5% identity with the plant GS proteins and 41.8% identity with their mammalian counterparts. The plant proteins average 53.7% identity with the mammalian proteins. Thus, the GS proteins are highly conserved and the divergence of these proteins is proportional to the phylogenetic divergence of the organisms from which the sequences were determined. No transfer of genes across large taxonomic gaps is needed to explain the presence of GSII in these bacteria.
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Almassy RJ, Janson CA, Hamlin R, Xuong N-H, Eisenberg D (1986) Novel subunit-subunit interactions in the structure of glutamine synthetase. Nature (London) 323:304–309
Benson DR, Noridge NA, Tsai YL, Taylor DA (1988). Enzymes of ammonia assimilation in hyphae and vesicles ofFrankia sp. strain CpII. In: Bothe H, de Bruijn FJ, Newton WE (eds) Nitrogen fixation: hundred years after. Proceedings of the 7th Intenational Congress on Nitrogen Fixation. Gustav Fischer, New York, p 693
Carlson TA, Chelm BK (1986) Apparent eukaryotic origin of glutamine synthetase II from the bacteriumBradyrhizobium japonicum. Nature (London) 322:568–570
Carlson TA, Martin GB, Chelm BK (1987) Differntial transcription of the two glutamine synthetase genes ofBradyrhizobium japonicum J Bacteriol 169:5861–5866
Colombo G, Villafranca JJ (1986) Amino acid sequence ofEscherichia coli glutamine synthetase deduced from the DNA nucleotide sequence. J Biol Chem 261:10587–10591
Crepet WL, Taylor DW (1985) The diversification of the Leguminosae: first fossil evidence of the Mimosoideae and Papilionoideae.Science 228:1087–1089
Darrow RA (1980) Role of glutamine synthetase in nitrogen fixation. In: Mora J, Palacios R (eds) Glutamine metabolism, enzymology, and regulation. Academic Press, New York, pp 139–166
Darrow RA, Knotts RR (1977) Two forms of glutamine synthetase in free-living root-nodule bacteria. Biochem Biophys Res Commun 78:554–559
Devereux J, Haeberli P, Smithies O (1984) A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res 12(1):387–395
Doolittle RF (1986) Of urfs and orfs: a primer on how to analyze derived amino acid sequences. University Science Books, Mill Valley CA
Edmands J, Noridge NA, Benson DR (1987) The actinorhizal root-nodule symbiontFrankia sp. strain CpI1 has two glutamine synthetases. Proc Natl Acad Sci USA 84:6126–6130
Egelhoff TT, Fisher RF, Jacobs TW, Mulligan JT, Long SR (1985) Nucleotide sequence ofRhizobium meliloti 1021 nodulation genes:nodD is read divergently fromnodABC. DNA 4:241–248
Fuchs RL, Keister DL (1980) Identification of two glutamine synthetases inAgrobacterium. J Bacteriol 141:996–998
Fuhrmann M, Hennecke H (1984)Rhizobium japonicum nitrogenase Fe protein gene (nifH). J Bacteriol 158:1005–1011
Gebhardt C, Oliver JE, Forde BG, Saarelainen R, Miflin BJ (1986) Primary structure and differential expression of glutamine synthetase genes in nodules, roots and leaves ofPhaseolus vulgaris. EMBO J 5:1429–1435
Gibbs CS, Campbell KE, Wilson RH (1987) Sequence of a human glutamine synthetase gene. Nucleic Acids Res 15:6293
Gussin GN, Ronson CW, Ausubel FM (1986) Regulation of nitrogen fixation genes. Annu Rev Genet 20:567–591
Hasegawa M, Iida Y, Yano T-A, Takaiwa F, Iwabuchi M (1985) Phylogenetic relationships among eukaryotic kingdoms inferred from ribosomal RNA sequences. J Mol Evol 22:32–38
Hayward BE, Hussain A, Wilson RH, Lyons A, Woodcock V, McIntosh B, Harris TJR (1986) The cloning and nucleotide sequence of cDNA for an amplified glutamine synthetase gene from the Chinese hamster. Nucleic Acids Res 14:999–1007
Hennecke HK, Kaluza B, Stackebrandt E (1985) Concurrent evolution of nitrogenase genes and 16S rRNA inRhizobium species and other nitrogen fixing bacteria. Arch Microbiol 142:342–348
Kimura M, Ohta T (1973) Eukaryotes-prokaryotes divergence estimated by 5S RNA sequences. Nature (New Biol) 243:199–200
Lim G, Burton JC (1983) Nodulation status of the Leguminosae. In: Broughton WJ (ed) Nitrogen fixation, vol 2.Rhizobium. Clarendon, London, pp 1–34
McKenna MG (1975) Toward a phylogenetic classification of the Mammalia. In: Lucket WP, Szalay FS (eds) Phylogeny of the primates, Plenum Press, New York, p 21–37
Ochman H, Wilson AC (1987) Evolution in bacteria: evidence for a universal substitution rate in cellular genomes. J Mol Evol 26:74–86
Pustell J, Kafatos FC (1982) A convenient and adaptable package of DNA sequence analysis programs. Nucleic Acids Res 10:51–59
Rossbach S, Schell, J, de Bruijn FJ (1988) Cloning and analysis ofAgrobacterium tumefaciens C58 loci involved in glutamine biosynthesis: neither theglnA (GSI) nor theglnII (GSII) gene plays a special role in virulence. Mol Gen Genet 212:38–47
Ruvkun GB, Ausubel FM, (1980) Interspecies homology of nitrogenase genes. Proc Natl Acad Sci USA 77:191–195
Scott KF (1986) Conserved nodulation genes from the nonlegume symbiontBradyrhizobium sp. (Parasponia). Nucleic Acids Res 14:2905–2919
Somerville JE, Kahn ML (1983) Cloning of the glutamine synthetase I gene fromRhizobium meliloti. J Bacteriol 156:168–176
Somerville JE, Shatters RG, Kahn ML (1989) Isolation, characterization and complementation ofRhizobium meliloti 104A14 mutants that lack glutamine synthetase II activity. J Bacteriol (in press)
Stadtman ER, Ginsburg A (1974) The glutamine synthetase ofEscherichia coli: structure and control. In: Boyer PD (ed) The enzymes 10:755–807
Tingey SV, Coruzzi GM (1987) Glutamine synthetase ofNicotiana plumbaginifolia. Plant Physiol 84:366–373
Tingey SV, Walker EL, Coruzzi GM (1987) Glutamine synthetase genes of pea encode distinct polypeptides which are differentially expressed in leaves, roots and nodules. EMBO J 6:1–9
Tischer E, DasSarma S, Goodman HM (1986) Nucleotide sequence of an alfalfa glutamine synthetase gene. Mol Gen Genet 203:221–229
Torok I, Kondorosi A (1981) Nucleotide sequence of theRhizobium meliloti nitrogenase reductase (nifH) gene. Nucleic Acids Res 9:5711–5723
Yang D, Oyaizu Y, Oyaizu H, Olsen GJ, Woese CR (1985) Mitochondrial origins. Proc Natl Acad Sci USA 82:4443–4447
Yanisch-Perron C, Vieira J, Messing J (1985) Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors. Gene 33:103–119
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Shatters, R.G., Kahn, M.L. Glutamine synthetase II inRhizobium: Reexamination of the proposed horizontal transfer of DNA from eukaryotes to prokaryotes. J Mol Evol 29, 422–428 (1989). https://doi.org/10.1007/BF02602912
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DOI: https://doi.org/10.1007/BF02602912