Home LiteratureArticle Details
PMID: 11157954 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Potential symbiosis-specific genes uncovered by sequencing a 410-kilobase DNA region of the Bradyrhizobium japonicum chromosome.

Journal of bacteriology ·Vol. 183 ·No. 4 ·2001-02-00 ·Pages 1405-12

Göttfert M, Röthlisberger S, Kündig C, Beck C, Marty R, Hennecke H

Abstract

The physical and genetic map of the Bradyrhizobium japonicum chromosome revealed that nitrogen fixation and nodulation genes are clustered. Because of the complex interactions between the bacterium and the plant, we expected this chromosomal sector to contain additional genes that are involved in the maintenance of an efficient symbiosis. Therefore, we determined the nucleotide sequence of a 410-kb region. The overall G+C nucleotide content was 59.1%. Using a minimum gene length of 150 nucleotides, 388 open reading frames (ORFs) were selected as coding regions. Thirty-five percent of the predicted proteins showed similarity to proteins of rhizobia. Sixteen percent were similar only to proteins of other bacteria. No database match was found for 29%. Repetitive DNA sequence-derived ORFs accounted for the rest. The sequenced region contained all nitrogen fixation genes and, apart from nodM, all nodulation genes that were known to exist in B. japonicum. We found several genes that seem to encode transport systems for ferric citrate, molybdate, or carbon sources. Some of them are preceded by -24/-12 promoter elements. A number of putative outer membrane proteins and cell wall-modifying enzymes as well as a type III secretion system might be involved in the interaction with the host.

MeSH Terms
Acyltransferases/genetics Amidohydrolases/genetics Bacterial Outer Membrane Proteins/genetics Bacterial Proteins/genetics,metabolism Bradyrhizobium/genetics Cations/metabolism Cell Wall/metabolism Chromosomes, Bacterial DNA, Bacterial Ferredoxins/genetics Genes, Bacterial Glucuronidase/genetics Metals/metabolism Models, Genetic Molecular Sequence Data N-Acetylglucosaminyltransferases/genetics Nitrogen Fixation/genetics Open Reading Frames Peptide Synthases/genetics Propanolamines/metabolism Recombination, Genetic/genetics Sequence Analysis, DNA/standards Symbiosis/genetics
Chemicals
Bacterial Outer Membrane Proteins Bacterial Proteins Cations DNA, Bacterial Ferredoxins Metals Propanolamines nodB protein, Bacteria Acyltransferases NodA protein, Rhizobiales N-Acetylglucosaminyltransferases NodC protein, Rhizobiales Glucuronidase Amidohydrolases Peptide Synthases rhizobitoxine
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Göttfert M
Institut für Genetik, Technische Universität Dresden, D-01062 Dresden, Germany. mgoettfe@rcs.urz.tu-dresden.de
Röthlisberger S
Kündig C
Beck C
Marty R
Hennecke H
References (82)
82 references, click to expand
  1. One member of a gro-ESL-like chaperonin multigene family in Bradyrhizobium japonicum is co-regulated with symbiotic nitrogen fixation genes.
    EMBO J. 1993 Jul;12(7):2901-12 PMID: 8101485
  2. Cloning, nucleotide sequence, and expression of the Brucella melitensis omp31 gene coding for an immunogenic major outer membrane protein.
    Infect Immun. 1996 Sep;64(9):3744-51 PMID: 8751924
  3. Identification of alanine dehydrogenase and its role in mixed secretion of ammonium and alanine by pea bacteroids.
    Mol Microbiol. 2000 Apr;36(2):508-15 PMID: 10792736
  4. Insertion and deletion mutations within the nif region of Rhizobium japonicum.
    Plant Mol Biol. 1984 May;3(3):159-68 PMID: 24310349
  5. Role of the nifQ gene product in the incorporation of molybdenum into nitrogenase in Klebsiella pneumoniae.
    J Bacteriol. 1984 Apr;158(1):187-94 PMID: 6370956
  6. Compilation of E. coli mRNA promoter sequences.
    Nucleic Acids Res. 1993 Apr 11;21(7):1507-16 PMID: 8479900
  7. Functional diversity, conservation, and convergence in the evolution of the alpha-, beta-, and gamma-carbonic anhydrase gene families.
    Mol Phylogenet Evol. 1996 Feb;5(1):50-77 PMID: 8673298
  8. Inhibition of ethylene production by rhizobitoxine.
    Plant Physiol. 1971 Jul;48(1):1-4 PMID: 16657720
  9. Uptake and Metabolism of Carbohydrates by Bradyrhizobium japonicum Bacteroids.
    Plant Physiol. 1987 Mar;83(3):535-40 PMID: 16665284
  10. Molecular basis of symbiosis between Rhizobium and legumes.
    Nature. 1997 May 22;387(6631):394-401 PMID: 9163424
  11. Microbial gene identification using interpolated Markov models.
    Nucleic Acids Res. 1998 Jan 15;26(2):544-8 PMID: 9421513
  12. In vitro sulfotransferase activity of NoeE, a nodulation protein of Rhizobium sp. NGR234.
    Mol Plant Microbe Interact. 1998 Jul;11(7):592-600 PMID: 9650293
  13. Uptake of iron by symbiosomes and bacteroids from soybean nodules.
    FEBS Lett. 1995 Mar 20;361(2-3):225-8 PMID: 7698328
  14. Gene-for-gene interactions between Pseudomonas syringae pv. phaseolicola and Phaseolus.
    Mol Plant Microbe Interact. 1991 Nov-Dec;4(6):553-62 PMID: 1666524
  15. Purification and characterization of a ferredoxin from Rhizobium japonicum bacteroids.
    J Biol Chem. 1980 May 10;255(9):4213-23 PMID: 6246115
  16. Induction of type III secretion in Shigella flexneri is associated with differential control of transcription of genes encoding secreted proteins.
    EMBO J. 1998 May 15;17(10):2894-903 PMID: 9582283
  17. Cloning of organic solvent tolerance gene ostA that determines n-hexane tolerance level in Escherichia coli.
    Appl Environ Microbiol. 1994 Dec;60(12):4624-6 PMID: 7811102
  18. Alanine, not ammonia, is excreted from N2-fixing soybean nodule bacteroids.
    Proc Natl Acad Sci U S A. 1998 Sep 29;95(20):12038-42 PMID: 9751786
  19. RNA polymerase from Rhizobium japonicum.
    Arch Microbiol. 1983 Aug;135(2):103-9 PMID: 6639271
  20. Role of pectic and cellulolytic enzymes in the invasion of the soybean by Rhizobium japonicum.
    Can J Microbiol. 1975 Aug;21(8):1254-8 PMID: 1172457
  21. A nonribosomal system of peptide biosynthesis.
    Eur J Biochem. 1996 Mar 1;236(2):335-51 PMID: 8612601
  22. A succinate transport mutant of Bradyrhizobium japonicum forms ineffective nodules on soybeans.
    Can J Microbiol. 1992 Mar;38(3):230-4 PMID: 1393826
  23. Salmonella typhimurium leucine-rich repeat proteins are targeted to the SPI1 and SPI2 type III secretion systems.
    Mol Microbiol. 1999 Nov;34(4):850-64 PMID: 10564523
  24. Carbohydrate, organic Acid, and amino Acid composition of bacteroids and cytosol from soybean nodules.
    Plant Physiol. 1987 Nov;85(3):768-73 PMID: 16665774
  25. Surface signaling: novel transcription initiation mechanism starting from the cell surface.
    Arch Microbiol. 1997 Jun;167(6):325-31 PMID: 9148773
  26. Codon usage and G + C content in Bradyrhizobium japonicum genes are not uniform.
    Arch Microbiol. 1991;156(4):270-6 PMID: 1793334
  27. Organization of the hydrogenase gene cluster from Bradyrhizobium japonicum: sequences and analysis of five more hydrogenase-related genes.
    Gene. 1994 Jul 22;145(1):91-6 PMID: 8045431
  28. Type III protein secretion systems in bacterial pathogens of animals and plants.
    Microbiol Mol Biol Rev. 1998 Jun;62(2):379-433 PMID: 9618447
  29. Symbiotic effectiveness of indigenous soybean bradyrhizobia as related to serological, morphological, rhizobitoxine, and hydrogenase phenotypes.
    Appl Environ Microbiol. 1990 Jan;56(1):224-9 PMID: 16348095
  30. Siderophore Utilization by Bradyrhizobium japonicum.
    Appl Environ Microbiol. 1993 May;59(5):1688-90 PMID: 16348945
  31. New M13 vectors for cloning.
    Methods Enzymol. 1983;101:20-78 PMID: 6310323
  32. Insertion sequences.
    Microbiol Mol Biol Rev. 1998 Sep;62(3):725-74 PMID: 9729608
  33. Purification and characterization of a novel dimeric ferredoxin (FdIII) from Rhodobacter capsulatus.
    J Biol Chem. 1993 May 15;268(14):10636-44 PMID: 8387524
  34. Translocation of iron citrate and phosphorus in xylem exudate of soybean.
    Plant Physiol. 1970 Mar;45(3):280-3 PMID: 16657313
  35. Characterization of an ammonium transport protein from the peribacteroid membrane of soybean nodules.
    Science. 1998 Aug 21;281(5380):1202-6 PMID: 9712587
  36. Rhizobitoxine production by Bradyrhizobium elkanii enhances nodulation and competitiveness on Macroptilium atropurpureum.
    Appl Environ Microbiol. 2000 Jun;66(6):2658-63 PMID: 10831453
  37. Specific interaction of the [2Fe-2S] ferredoxin from Clostridium pasteurianum with the nitrogenase MoFe protein.
    Biochemistry. 1997 Sep 30;36(39):11797-803 PMID: 9305970
  38. Evidence for the direct interaction of the nifW gene product with the MoFe protein.
    J Biol Chem. 1996 Apr 19;271(16):9764-70 PMID: 8621656
  39. Rhizobial-Induced Chlorosis in Soybeans: Isolation, Production in Nodules, and Varietal Specificity of the Toxin.
    Plant Physiol. 1965 Sep;40(5):927-30 PMID: 16656176
  40. Improved microbial gene identification with GLIMMER.
    Nucleic Acids Res. 1999 Dec 1;27(23):4636-41 PMID: 10556321
  41. Machine learning approaches for the prediction of signal peptides and other protein sorting signals.
    Protein Eng. 1999 Jan;12(1):3-9 PMID: 10065704
  42. The Rhizobium meliloti fdxN gene encoding a ferredoxin-like protein is necessary for nitrogen fixation and is cotranscribed with nifA and nifB.
    Mol Gen Genet. 1989 Apr;216(2-3):293-302 PMID: 2747618
  43. Sulphation of Rhizobium sp. NGR234 Nod factors is dependent on noeE, a new host-specificity gene.
    Mol Microbiol. 1997 Jun;24(6):1119-29 PMID: 9218762
  44. One of two hemN genes in Bradyrhizobium japonicum is functional during anaerobic growth and in symbiosis.
    J Bacteriol. 2001 Feb;183(4):1300-11 PMID: 11157943
  45. Three new NifA-regulated genes in the Bradyrhizobium japonicum symbiotic gene region discovered by competitive DNA-RNA hybridization.
    J Bacteriol. 2000 Mar;182(6):1472-80 PMID: 10692350
  46. Genetic regulation of nitrogen fixation in rhizobia.
    Microbiol Rev. 1994 Sep;58(3):352-86 PMID: 7968919
  47. Bradyrhizobium japonicum has two differentially regulated, functional homologs of the sigma 54 gene (rpoN).
    J Bacteriol. 1991 Feb;173(3):1125-38 PMID: 1991712
  48. Use of a promoter-probe vector system in the cloning of a new NifA-dependent promoter (ndp) from Bradyrhizobium japonicum.
    Gene. 1993 Jul 15;129(1):33-40 PMID: 8335258
  49. Transcriptional organization and expression of noIXWBTUV, a locus that regulates cultivar-specific nodulation of soybean by Rhizobium fredii USDA257.
    Mol Microbiol. 1995 Sep;17(5):923-33 PMID: 8596441
  50. Evidence countering the role of polygalacturonase in invasion of root hairs of leguminous plants by Rhizobium spp.
    Can J Microbiol. 1968 Jun;14(6):617-25 PMID: 5665279
  51. Identification of a pathogenicity island, which contains genes for virulence and avirulence, on a large native plasmid in the bean pathogen Pseudomonas syringae pathovar phaseolicola.
    Proc Natl Acad Sci U S A. 1999 Sep 14;96(19):10875-80 PMID: 10485919
  52. Symbiotic implications of type III protein secretion machinery in Rhizobium.
    Mol Microbiol. 1998 Jun;28(6):1381-9 PMID: 9680225
  53. Mapping of a Bradyrhizobium japonicum DNA Region Carrying Genes for Symbiosis and an Asymmetric Accumulation of Reiterated Sequences.
    Appl Environ Microbiol. 1987 Sep;53(9):2247-52 PMID: 16347445
  54. nolMNO genes of Bradyrhizobium japonicum are co-transcribed with nodYABCSUIJ, and nolO is involved in the synthesis of the lipo-oligosaccharide nodulation signals.
    J Biol Chem. 1993 Dec 25;268(36):27053-9 PMID: 8262943
  55. Bradyrhizobium japonicum rhizobitoxine genes and putative enzyme functions: expression requires a translational frameshift.
    Proc Natl Acad Sci U S A. 1993 Apr 1;90(7):2641-5 PMID: 8464870
  56. Molecular cloning and characterization of a sym plasmid locus that regulates cultivar-specific nodulation of soybean by Rhizobium fredii USDA257.
    Mol Microbiol. 1993 Jul;9(1):17-29 PMID: 8412662
  57. Lambdoid phages that simplify the recovery of in vitro recombinants.
    Mol Gen Genet. 1977 Jan 7;150(1):53-61 PMID: 319344
  58. Correlated physical and genetic map of the Bradyrhizobium japonicum 110 genome.
    J Bacteriol. 1993 Feb;175(3):613-22 PMID: 8423135
  59. The Bradyrhizobium japonicum noeD gene: a negatively acting, genotype-specific nodulation gene for soybean.
    Mol Plant Microbe Interact. 1998 Jun;11(6):476-88 PMID: 9612946
  60. Lorist6, a cosmid vector with BamHI, NotI, ScaI and HindIII cloning sites and altered neomycin phosphotransferase gene expression.
    Gene. 1987;53(2-3):283-6 PMID: 3038694
  61. Six nodulation genes of nod box locus 4 in Rhizobium meliloti are involved in nodulation signal production: nodM codes for D-glucosamine synthetase.
    Mol Gen Genet. 1991 Aug;228(1-2):113-24 PMID: 1909418
  62. A 2-O-methylfucose moiety is present in the lipo-oligosaccharide nodulation signal of Bradyrhizobium japonicum.
    Proc Natl Acad Sci U S A. 1992 Sep 15;89(18):8789-93 PMID: 1528893
  63. The regulated outer membrane protein Omp21 from Comamonas acidovorans is identified as a member of a new family of eight-stranded beta-sheet proteins by its sequence and properties.
    J Bacteriol. 1998 Aug;180(15):3741-9 PMID: 9683466
  64. Identification of a new Bradyrhizobium japonicum gene (frxA) encoding a ferredoxinlike protein.
    J Bacteriol. 1988 Apr;170(4):1999-2001 PMID: 3350797
  65. Evolution of rhizobia by acquisition of a 500-kb symbiosis island that integrates into a phe-tRNA gene.
    Proc Natl Acad Sci U S A. 1998 Apr 28;95(9):5145-9 PMID: 9560243
  66. nolO and noeI (HsnIII) of Rhizobium sp. NGR234 are involved in 3-O-carbamoylation and 2-O-methylation of Nod factors.
    J Biol Chem. 1998 May 15;273(20):12047-55 PMID: 9575146
  67. Hydrogen evolution and uptake by nodules of soybeans inoculated with different strains of Rhizobium japonicum.
    Can J Microbiol. 1978 Mar;24(3):307-11 PMID: 565672
  68. Genetic analysis on the NifW by utilizing the yeast two-hybrid system revealed that the NifW of Azotobacter vinelandii interacts with the NifZ to form higher-order complexes.
    Biochem Biophys Res Commun. 1998 Mar 17;244(2):498-504 PMID: 9514861
  69. Carbonic anhydrase is an ancient enzyme widespread in prokaryotes.
    Proc Natl Acad Sci U S A. 1999 Dec 21;96(26):15184-9 PMID: 10611359
  70. Symbiotic properties of C4-dicarboxylic acid transport mutants of Rhizobium leguminosarum.
    J Bacteriol. 1983 Jun;154(3):1403-13 PMID: 6853448
  71. Complete sequence of a 184-kilobase catabolic plasmid from Sphingomonas aromaticivorans F199.
    J Bacteriol. 1999 Mar;181(5):1585-602 PMID: 10049392
  72. Site-specific mutagenesis of Rhodobacter capsulatus ferredoxin I, FdxN, that functions in nitrogen fixation. Role of extra residues.
    J Biol Chem. 1996 Dec 6;271(49):31399-406 PMID: 8940149
  73. Construction of improved M13 vectors using oligodeoxynucleotide-directed mutagenesis.
    Gene. 1983 Dec;26(1):101-6 PMID: 6323249
  74. Regulation and function of rhizobial nodulation genes.
    FEMS Microbiol Rev. 1993 Jan;10(1-2):39-63 PMID: 8431309
  75. Two C4-dicarboxylate transport systems in Rhizobium sp. NGR234: rhizobial dicarboxylate transport is essential for nitrogen fixation in tropical legume symbioses.
    Mol Plant Microbe Interact. 1992 Mar-Apr;5(2):179-86 PMID: 1617199
  76. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs.
    Nucleic Acids Res. 1997 Sep 1;25(17):3389-402 PMID: 9254694
  77. Pectolytic enzymes in Rhizobium.
    Appl Environ Microbiol. 1978 Jan;35(1):210-3 PMID: 623465
  78. C(4)-dicarboxylate transport mutants of Rhizobium trifolii form ineffective nodules on Trifolium repens.
    Proc Natl Acad Sci U S A. 1981 Jul;78(7):4284-8 PMID: 16593058
  79. Genetic relatedness of Bradyrhizobium japonicum field isolates as revealed by repeated sequences and various other characteristics.
    Appl Environ Microbiol. 1992 Sep;58(9):2832-9 PMID: 1444394
  80. The role of polygalacturonase in root-hair invasion by nodule bacteria.
    J Gen Microbiol. 1961 Nov;26:521-8 PMID: 14466017
  81. Identification and characterization of a novel Bradyrhizobium japonicum gene involved in host-specific nitrogen fixation.
    J Bacteriol. 1994 Nov;176(21):6717-29 PMID: 7961425
  82. Crystal structure of polygalacturonase from Erwinia carotovora ssp. carotovora.
    J Biol Chem. 1998 Sep 18;273(38):24660-4 PMID: 9733763
Article Info
Journal
Journal of bacteriology
Abbr.
J Bacteriol
ISSN
0021-9193
Published
2001-02-00
Pages
1405-12
Language
English
Region
United States
NLM ID
2985120R
PMCID
PMC95015
Subset
IM
Databases
GENBANK
AF322012, AF322013
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