Home LiteratureArticle Details
PMID: 8599534 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Bradyrhizobium japonicum possesses two discrete sets of electron transfer flavoprotein genes: fixA, fixB and etfS, etfL.

Archives of microbiology ·Vol. 165 ·No. 3 ·1996-03-00 ·Pages 169-78

Weidenhaupt M, Rossi P, Beck C, Fischer HM, Hennecke H

Abstract

A group of four co-regulated genes (fixA, fixB, fixC, fixX) essential for symbiotic nitrogen fixation has been described in several rhizobial species, including Bradyrhizobium japonicum. The complete nucleotide sequence of the B. japonicum fixA, fixB and fixC, genes is reported here. The derived amino acid sequences confirmed the previously noted sequence similarity between FixA and the beta-subunit and between FixB and the alpha-subunit of mammalian and Paracoccus denitrificans electron transfer flavoproteins (ETF). Since the classical role of ETF is in beta-oxidation of fatty acids, a process unrelated to nitrogen fixation, we rationalized that B. japonicum ought to contain bona fide etf genes in addition to the etf-like genes fixA and fixB. Therefore, we identified, cloned, sequenced, and transcriptionally analyzed the B. japonicum etfSL genes encoding the beta- and alpha-subunits of ETF. The etfSL genes, but not the fix genes, are transcribed in aerobically grown cells. An amino acid sequence comparison between all available ETFs and ETF-like proteins revealed the existence of two distinguishable subfamilies. Group I comprises housekeeping ETFs that link acyl-CoA dehydrogenase reactions with the respiratory chain, such as in the fatty acid degradation pathway. B. japonicum EtfS and EtfL clearly belong to this group. Group II contains ETF-like proteins that are synthesized only under certain specific growth conditions and receive electrons from the oxidation of specific substrates. The products of the anaerobically induced fixA and fixB genes of B. japonicum are members of that group. B. japonicum is the first example of an organism in which genes for proteins of both groups I and II of the ETF family have been identified.

MeSH Terms
Amino Acid Sequence Bacterial Proteins/chemistry,genetics Base Sequence Chromosome Mapping Cloning, Molecular Electron Transport Electron-Transferring Flavoproteins Escherichia coli Proteins Flavoproteins/chemistry,genetics Genes, Bacterial Molecular Sequence Data Nitrogen Fixation/genetics Operon Phylogeny Rhizobiaceae/chemistry,genetics,metabolism Sequence Alignment Transcription, Genetic
Chemicals
Bacterial Proteins Electron-Transferring Flavoproteins Escherichia coli Proteins FixA protein, E coli Flavoproteins fixB protein, E coli
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Weidenhaupt M
Mikrobiologisches Institut, Eidgenössische Technische Hochschule, ETH-Zentrum, Schmelzbergstrasse 7, CH-8092 Zürich, Switzerland.
Rossi P
Beck C
Fischer H M
Hennecke H
References (45)
45 references, click to expand
  1. Two different mechanisms are involved in the heat-shock regulation of chaperonin gene expression in Bradyrhizobium japonicum.
    Mol Microbiol. 1996 Feb;19(4):827-39 PMID: 8820652
  2. Characterization of the fixABC region of Azorhizobium caulinodans ORS571 and identification of a new nitrogen fixation gene.
    Mol Gen Genet. 1988 Nov;214(3):496-502 PMID: 3216855
  3. Molecular characterization of the cai operon necessary for carnitine metabolism in Escherichia coli.
    Mol Microbiol. 1994 Sep;13(5):775-86 PMID: 7815937
  4. Molecular cloning and nucleotide sequence of cDNAs encoding the alpha-subunit of human electron transfer flavoprotein.
    J Biol Chem. 1988 Oct 25;263(30):15773-80 PMID: 3170610
  5. Localization of the major dehydrogenases in two methylotrophs by radiochemical labeling.
    J Bacteriol. 1983 Oct;156(1):348-53 PMID: 6311799
  6. Bradyrhizobium japonicum TlpA, a novel membrane-anchored thioredoxin-like protein involved in the biogenesis of cytochrome aa3 and development of symbiosis.
    EMBO J. 1993 Sep;12(9):3373-83 PMID: 8253065
  7. Molecular cloning and expression of a cDNA encoding human electron transfer flavoprotein-ubiquinone oxidoreductase.
    Eur J Biochem. 1994 Jan 15;219(1-2):277-86 PMID: 8306995
  8. The fix Escherichia coli region contains four genes related to carnitine metabolism.
    J Basic Microbiol. 1995;35(4):217-27 PMID: 7473063
  9. RNA polymerase from Rhizobium japonicum.
    Arch Microbiol. 1983 Aug;135(2):103-9 PMID: 6639271
  10. Separation and purification of sarcosine dehydrogenase and dimethylglycine dehydrogenase.
    J Biol Chem. 1962 Jan;237:94-8 PMID: 13895406
  11. Fine-tuning of nif and fix gene expression by upstream activator sequences in Bradyrhizobium japonicum.
    Mol Microbiol. 1989 Feb;3(2):149-59 PMID: 2503675
  12. Phylogeny of the phototrophic rhizobium strain BTAi1 by polymerase chain reaction-based sequencing of a 16S rRNA gene segment.
    J Bacteriol. 1991 Apr;173(7):2271-7 PMID: 2007551
  13. "A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity". Addendum.
    Anal Biochem. 1984 Feb;137(1):266-7 PMID: 6329026
  14. cDNA cloning and mitochondrial import of the beta-subunit of the human electron-transfer flavoprotein.
    Eur J Biochem. 1993 May 1;213(3):1003-8 PMID: 8504797
  15. Genes for a microaerobically induced oxidase complex in Bradyrhizobium japonicum are essential for a nitrogen-fixing endosymbiosis.
    Proc Natl Acad Sci U S A. 1993 Apr 15;90(8):3309-13 PMID: 8386371
  16. A gene upstream of the Rhizobium trifolii nifA gene encodes a ferredoxin-like protein.
    Nucleic Acids Res. 1987 Apr 10;15(7):3180 PMID: 3562251
  17. Identification of DNA regions homologous to nitrogen fixation genes nifE, nifUS and fixABC in Azospirillum brasilense Sp7.
    J Gen Microbiol. 1989 May;135(5):1047-59 PMID: 2695597
  18. New M13 vectors for cloning.
    Methods Enzymol. 1983;101:20-78 PMID: 6310323
  19. Rhizobium meliloti insertion element ISRm2 and its use for identification of the fixX gene.
    J Bacteriol. 1987 Apr;169(4):1403-9 PMID: 3031010
  20. Cloning and sequence of the Rhizobium leguminosarum biovar phaseoli fixA gene.
    Biochim Biophys Acta. 1993 Sep 13;1144(2):232-3 PMID: 8369342
  21. Organization and partial sequence of a DNA region of the Rhizobium leguminosarum symbiotic plasmid pRL6JI containing the genes fixABC, nifA, nifB and a novel open reading frame.
    Nucleic Acids Res. 1987 Jan 12;15(1):31-49 PMID: 3029674
  22. Evidence for gene duplication forming similar binding folds for NAD(P)H and FAD in pyridine nucleotide-dependent flavoenzymes.
    FEBS Lett. 1991 Feb 11;279(1):5-8 PMID: 1995341
  23. The Bradyrhizobium japonicum fixBCX operon: identification of fixX and of a 5' mRNA region affecting the level of the fixBCX transcript.
    Mol Microbiol. 1989 Feb;3(2):141-8 PMID: 2503674
  24. Genetic regulation of nitrogen fixation in rhizobia.
    Microbiol Rev. 1994 Sep;58(3):352-86 PMID: 7968919
  25. Cloning, sequence analysis, and expression of the genes encoding the two subunits of the methylotrophic bacterium W3A1 electron transfer flavoprotein.
    J Biol Chem. 1994 Dec 23;269(51):32120-30 PMID: 7798207
  26. Phylogenetic analysis of the family Rhizobiaceae and related bacteria by sequencing of 16S rRNA gene using PCR and DNA sequencer.
    FEMS Microbiol Lett. 1993 Feb 15;107(1):115-20 PMID: 7682191
  27. Phylogenetic characterization of the ubiquitous electron transfer flavoprotein families ETF-alpha and ETF-beta.
    Res Microbiol. 1995 Jun;146(5):397-404 PMID: 8525056
  28. Cloning, sequencing, and expression of the genes encoding subunits of Paracoccus denitrificans electron transfer flavoprotein.
    J Biol Chem. 1993 Sep 25;268(27):20211-7 PMID: 8376381
  29. The purification and characterization of glutaryl-coenzyme A dehydrogenase from porcine and human liver.
    J Biol Chem. 1986 Mar 25;261(9):4090-6 PMID: 3081514
  30. Correlated physical and genetic map of the Bradyrhizobium japonicum 110 genome.
    J Bacteriol. 1993 Feb;175(3):613-22 PMID: 8423135
  31. A Rhizobium meliloti symbiotic regulatory gene.
    Cell. 1984 Apr;36(4):1035-43 PMID: 6423287
  32. Partial purification and characterization of glutaryl-coenzyme A dehydrogenase, electron transfer flavoprotein, and electron transfer flavoprotein-Q oxidoreductase from Paracoccus denitrificans.
    J Bacteriol. 1985 Aug;163(2):709-15 PMID: 2991202
  33. Purification and characterization of isovaleryl coenzyme A dehydrogenase from rat liver mitochondria.
    J Biol Chem. 1983 Jan 25;258(2):1077-85 PMID: 6401713
  34. Purification and characterization of 2-methyl-branched chain acyl coenzyme A dehydrogenase, an enzyme involved in the isoleucine and valine metabolism, from rat liver mitochondria.
    J Biol Chem. 1983 Aug 10;258(15):9477-87 PMID: 6874697
  35. Structural and redox relationships between Paracoccus denitrificans, porcine and human electron-transferring flavoproteins.
    Eur J Biochem. 1992 May 1;205(3):1089-97 PMID: 1576992
  36. Further analysis of nitrogen fixation (nif) genes in Azotobacter chroococcum: identification and expression in Klebsiella pneumoniae of nifS, nifV, nifM, and nifB genes and localization of nifE/N-, nifU-, nifA- and fixABC-like genes.
    J Gen Microbiol. 1988 Apr;134(4):931-42 PMID: 3053983
  37. Construction of improved M13 vectors using oligodeoxynucleotide-directed mutagenesis.
    Gene. 1983 Dec;26(1):101-6 PMID: 6323249
  38. Molecular cloning of a cDNA for alpha-subunit of rat liver electron transfer flavoprotein.
    Biochem Biophys Res Commun. 1988 Aug 30;155(1):300-4 PMID: 3415685
  39. Genetic and structural analysis of the Rhizobium meliloti fixA, fixB, fixC, and fixX genes.
    J Bacteriol. 1987 Mar;169(3):1127-36 PMID: 3029021
  40. Nucleotide sequence of the fixABC region of Azorhizobium caulinodans ORS571: similarity of the fixB product with eukaryotic flavoproteins, characterization of fixX, and identification of nifW.
    Mol Gen Genet. 1991 Mar;225(3):514-20 PMID: 1850088
  41. Systematic sequencing of the Escherichia coli genome: analysis of the 0-2.4 min region.
    Nucleic Acids Res. 1992 Jul 11;20(13):3305-8 PMID: 1630901
  42. Molecular and biochemical analyses of fatty acid transport, metabolism, and gene regulation in Escherichia coli.
    Biochim Biophys Acta. 1994 Jan 3;1210(2):123-45 PMID: 8280762
  43. On the mechanism of dehydrogenation of fatty acyl derivatives of coenzyme A. III. Palmityl coA dehydrogenase.
    J Biol Chem. 1956 Apr;219(2):727-33 PMID: 13319294
  44. Homology between hydroxybutyryl and hydroxyacyl coenzyme A dehydrogenase enzymes from Clostridium acetobutylicum fermentation and vertebrate fatty acid beta-oxidation pathways.
    J Bacteriol. 1989 Dec;171(12):6800-7 PMID: 2687255
  45. Regulation of the fixA gene and fixBC operon in Bradyrhizobium japonicum.
    J Bacteriol. 1988 Mar;170(3):1205-14 PMID: 3343218
Article Info
Journal
Archives of microbiology
Abbr.
Arch Microbiol
ISSN
0302-8933
Published
1996-03-00
Pages
169-78
Language
English
Region
Germany
NLM ID
0410427
Subset
IM
Databases
GENBANK
U32226, U32227, U32228
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com