1887

Abstract

In a survey of the biodiversity and biogeography of rhizobia associated with soybean ( L.) in different sites of the Northern (Huang-Huai-Hai) Plain of China, ten strains were defined as representing a novel genomic species in the genus of . They were distinguished from defined species in restriction fragment length polymorphism (RFLP) analysis of the 16S rRNA gene and the 16S–23S rRNA gene intergenic spacer (IGS). In BOX-PCR, these strains presented two patterns that shared 94 % similarity, demonstrating that they were a homogenous group with limited diversity. In phylogenetic analyses of the 16S rRNA gene, IGS and housekeeping gene sequences, four representative strains formed a distant lineage within the genus , which was consistent with the results of DNA–DNA hybridization. The strains of this novel group formed effective nodules with , and in cross-nodulation tests and harboured symbiotic genes ( and ) identical to those of reference strains of , and ‘’ originating from soybean, implying that the novel group may have obtained these symbiotic genes by lateral gene transfer. In analyses of cellular fatty acids and phenotypic features, some differences were found between the novel group and related species, demonstrating that the novel group is distinct phenotypically from other species. Based upon the data obtained, these strains are proposed to represent a novel species, sp. nov., with CCBAU 23303 ( = LMG 26136  = CGMCC 1.10948  = HAMBI 3180) as the type strain. The DNA G+C content of strain CCBAU 23303 is 61.5 mol% ( ).

Funding
This study was supported by the:
  • Foundation of the State Key Basic Research and Development Plan of China (Award 2010CB126500)
  • Funds of Commercialization of Agricultural and Scientific Findings, MOST (Award 2008GB23600460)
  • National Natural Science Foundation of China (Award 30870004 and 30970004)
  • SKLAB (Award 20110423, SIP20100067, 2010SKLAB01-1 and 2009SKLAB05-1)
  • IPN (Award PICS08-3)
  • ICyT DF of Mexico
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2012-08-01
2021-10-25
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References

  1. Ando S., Yokoyama T. 1999; Phylogenetic analyses of Bradyrhizobium strains nodulating soybean (Glycine max) in Thailand with reference to the USDA strains of Bradyrhizobium . Can J Microbiol 45:639–645[PubMed] [CrossRef]
    [Google Scholar]
  2. Appunu C., N’Zoue A., Laguerre G. 2008; Genetic diversity of native bradyrhizobia isolated from soybeans (Glycine max L.) in different agricultural-ecological-climatic regions of India. Appl Environ Microbiol 74:5991–5996 [View Article][PubMed]
    [Google Scholar]
  3. Barrow G. I., Feltham R. K. A. (editors) 1993 Cowan and Steel’s Manual for the Identification of Medical Bacteria, 3rd edn. Cambridge: Cambridge University Press; [View Article]
    [Google Scholar]
  4. Chahboune R., Carro L., Peix A., Barrijal S., Velázquez E., Bedmar E. J. 2011; Bradyrhizobium cytisi sp. nov., isolated from effective nodules of Cytisus villosus . Int J Syst Evol Microbiol 61:2922–2927 [View Article][PubMed]
    [Google Scholar]
  5. Chang Y. L., Wang J. Y., Wang E. T., Liu H. C., Sui X. H., Chen W. X. 2011; Bradyrhizobium lablabi sp. nov., isolated from effective nodules of Lablab purpureus and Arachis hypogaea . Int J Syst Evol Microbiol 61:2496–2502 [View Article][PubMed]
    [Google Scholar]
  6. Chen W. X., Yan G. H., Li J. L. 1988; Numerical taxonomic study of fast-growing soybean rhizobia and a proposal that Rhizobium fredii be assigned to Sinorhizobium gen. nov.. Int J Syst Bacteriol 38:392–397 [View Article]
    [Google Scholar]
  7. De Ley J., Cattoir H., Reynaerts A. 1970; The quantitative measurement of DNA hybridization from renaturation rates. Eur J Biochem 12:133–142 [View Article][PubMed]
    [Google Scholar]
  8. Gao J. L., Sun J. G., Li Y., Wang E. T., Chen W. X. 1994; Numerical taxonomy and DNA relatedness of tropical rhizobia isolated from Hainan Province, China. Int J Syst Bacteriol 44:151–158 [View Article]
    [Google Scholar]
  9. Guindon S., Gascuel O. 2003; A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704 [View Article][PubMed]
    [Google Scholar]
  10. Han L. L., Wang E. T., Han T. X., Liu J., Sui X. H., Chen W. F., Chen W. X. 2009; Unique community structure and biogeography of soybean rhizobia in the saline-alkaline soils of Xinjiang, China. Plant Soil 324:291–305 [View Article]
    [Google Scholar]
  11. Hurek T., Wagner B., Reinhold-Hurek B. 1997; Identification of N2-fixing plant- and fungus-associated Azoarcus species by PCR-based genomic fingerprints. Appl Environ Microbiol 63:4331–4339[PubMed]
    [Google Scholar]
  12. Islam M. S., Kawasaki H., Muramatsu Y., Nakagawa Y., Seki T. 2008; Bradyrhizobium iriomotense sp. nov., isolated from a tumor-like root of the legume Entada koshunensis from Iriomote Island in Japan. Biosci Biotechnol Biochem 72:1416–1429 [View Article][PubMed]
    [Google Scholar]
  13. Kimura M. 1980; A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120 [View Article][PubMed]
    [Google Scholar]
  14. Kuykendall L., Saxena B., Devine T., Udell S. 1992; Genetic diversity in Bradyrhizobium japonicum Jordan 1982 and a proposal for Bradyrhizobium elkanii sp. nov.. Can J Microbiol 38:501–505 [View Article]
    [Google Scholar]
  15. Laguerre G., Nour S. M., Macheret V., Sanjuan J., Drouin P., Amarger N. 2001; Classification of rhizobia based on nodC and nifH gene analysis reveals a close phylogenetic relationship among Phaseolus vulgaris symbionts. Microbiology 147:981–993[PubMed]
    [Google Scholar]
  16. Li Q. Q., Wang E. T., Chang Y. L., Zhang Y. Z., Zhang Y. M., Sui X. H., Chen W. F., Chen W. X. 2011a; Ensifer sojae sp. nov., isolated from root nodules of Glycine max grown in saline-alkaline soils. Int J Syst Evol Microbiol 61:1981–1988 [View Article][PubMed]
    [Google Scholar]
  17. Li Q. Q., Wang E. T., Zhang Y. Z., Zhang Y. M., Tian C. F., Sui X. H., Chen W. F., Chen W. X. 2011b; Diversity and biogeography of rhizobia isolated from root nodules of Glycine max grown in Hebei Province, China. Microb Ecol 61:917–931 [View Article][PubMed]
    [Google Scholar]
  18. Man C. X., Wang H., Chen W. F., Sui X. H., Wang E. T., Chen W. X. 2008; Diverse rhizobia associated with soybean grown in the subtropical and tropical regions of China. Plant Soil 310:77–87 [View Article]
    [Google Scholar]
  19. Mandel M., Marmur J. 1968; Use of ultraviolet absorbance-temperature profile for determining the guanine plus cytosine content of DNA. Methods Enzymol 12B:195–206 [View Article]
    [Google Scholar]
  20. Marmur J. 1961; A procedure for the isolation of deoxyribonucleic acid from micro-organisms. J Mol Biol 3:208–218 [View Article]
    [Google Scholar]
  21. Miller K. J., Shon B. C., Gore R. S., Hunt W. P. 1990; The phospholipid composition of Bradyrhizobium spp.. Curr Microbiol 21:205–210 [View Article]
    [Google Scholar]
  22. Minnikin D. E., O’Donnell A. G., Goodfellow M., Alderson G., Athalye M., Schaal A., Parlett J. H. 1984; An integrated procedure for the extraction of bacterial isoprenoid quinones and polar lipids. J Microbiol Methods 2:233–241 [View Article]
    [Google Scholar]
  23. Moulin L., Béna G., Boivin-Masson C., Stepkowski T. 2004; Phylogenetic analyses of symbiotic nodulation genes support vertical and lateral gene co-transfer within the Bradyrhizobium genus. Mol Phylogenet Evol 30:720–732 [View Article][PubMed]
    [Google Scholar]
  24. Nick G., de Lajudie P., Eardly B. D., Suomalainen S., Paulin L., Zhang X., Gillis M., Lindström K. 1999; Sinorhizobium arboris sp. nov. and Sinorhizobium kostiense sp. nov., isolated from leguminous trees in Sudan and Kenya. Int J Syst Bacteriol 49:1359–1368 [View Article][PubMed]
    [Google Scholar]
  25. Normand P., Cournoyer B., Simonet P., Nazaret S. 1992; Analysis of a ribosomal RNA operon in the actinomycete Frankia . Gene 111:119–124 [View Article][PubMed]
    [Google Scholar]
  26. Posada D., Crandall K. A. 1998; ModelTest: testing the model of DNA substitution. Bioinformatics 14:817–818 [View Article][PubMed]
    [Google Scholar]
  27. Ramírez-Bahena M. H., Peix A., Rivas R., Camacho M., Rodríguez-Navarro D. N., Mateos P. F., Martínez-Molina E., Willems A., Velázquez E. 2009; Bradyrhizobium pachyrhizi sp. nov. and Bradyrhizobium jicamae sp. nov., isolated from effective nodules of Pachyrhizus erosus . Int J Syst Evol Microbiol 59:1929–1934 [View Article][PubMed]
    [Google Scholar]
  28. Rasolomampianina R., Bailly X., Fetiarison R., Rabevohitra R., Béna G., Ramaroson L., Raherimandimby M., Moulin L., De Lajudie P. other authors 2005; Nitrogen-fixing nodules from rose wood legume trees (Dalbergia spp.) endemic to Madagascar host seven different genera belonging to alpha- and beta-Proteobacteria. Mol Ecol 14:4135–4146 [View Article][PubMed]
    [Google Scholar]
  29. Rivas R., Willems A., Palomo J. L., García-Benavides P., Mateos P. F., Martínez-Molina E., Gillis M., Velázquez E. 2004; Bradyrhizobium betae sp. nov., isolated from roots of Beta vulgaris affected by tumour-like deformations. Int J Syst Evol Microbiol 54:1271–1275 [View Article][PubMed]
    [Google Scholar]
  30. Saitou N., Nei M. 1987; The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425[PubMed]
    [Google Scholar]
  31. Sarita S., Sharma P. K., Priefer U. B., Prell J. 2005; Direct amplification of rhizobial nodC sequences from soil total DNA and comparison to nodC diversity of root nodule isolates. FEMS Microbiol Ecol 54:1–11 [View Article][PubMed]
    [Google Scholar]
  32. Sasser M. 1990 Identification of bacteria by gas chromatography of cellular fatty acids, MIDI Technical Note 101. Newark, DE: MIDI Inc.
  33. Smibert R. M., Krieg N. R. 1994; Phenotypic characterization. In Methods for General and Molecular Bacteriology pp. 607–654 Edited by Gerhardt P., Murray R. G. E., Wood W. A., Krieg N. R. Washington, DC: American Society for Microbiology;
    [Google Scholar]
  34. Swofford D. 2000 paup*: phylogenetic analysis using parsimony (and other methods), version 4, b10. Sunderland, MA: Sinauer Associates.
  35. Tamura K., Dudley J., Nei M., Kumar S. 2007; mega4: molecular evolutionary genetics analysis (mega) software version 4.0. Mol Biol Evol 24:1596–1599 [View Article][PubMed]
    [Google Scholar]
  36. Tan Z. Y., Xu X. D., Wang E. T., Gao J. L., Martinez-Romero E., Chen W. X. 1997; Phylogenetic and genetic relationships of Mesorhizobium tianshanense and related rhizobia. Int J Syst Bacteriol 47:874–879 [View Article][PubMed]
    [Google Scholar]
  37. Terefework Z., Kaijalainen S., Lindström K. 2001; AFLP fingerprinting as a tool to study the genetic diversity of Rhizobium galegae isolated from Galega orientalis and Galega officinalis . J Biotechnol 91:169–180 [View Article][PubMed]
    [Google Scholar]
  38. Tighe S. W., de Lajudie P., Dipietro K., Lindström K., Nick G., Jarvis B. D. 2000; Analysis of cellular fatty acids and phenotypic relationships of Agrobacterium, Bradyrhizobium, Mesorhizobium, Rhizobium and Sinorhizobium species using the Sherlock Microbial Identification System. Int J Syst Evol Microbiol 50:787–801 [View Article][PubMed]
    [Google Scholar]
  39. van Berkum P., Leibold J. M., Eardly B. D. 2006; Proposal for combining Bradyrhizobium spp. (Aeschynomene indica) with Blastobacter denitrificans and to transfer Blastobacter denitrificans (Hirsch and Muller, 1985) to the genus Bradyrhizobium as Bradyrhizobium denitrificans (comb. nov.). Syst Appl Microbiol 29:207–215 [View Article][PubMed]
    [Google Scholar]
  40. Vauterin L., Vauterin P. 1992; Computer-aided objective comparison of electrophoresis patterns for grouping and identification of microorganisms. Eur Microbiol 1:37–41
    [Google Scholar]
  41. Versalovic J., Schneider M., De Bruijn F., Lupski J. 1994; Genomic fingerprinting of bacteria using repetitive sequence based PCR (rep-PCR). Methods Mol Cell Biol 5:25–40
    [Google Scholar]
  42. Vincent J. M. 1970 A Manual for the Practical Study of the Root Nodule Bacteria Oxford: Blackwell Scientific;
    [Google Scholar]
  43. Vinuesa P., León-Barrios M., Silva C., Willems A., Jarabo-Lorenzo A., Pérez-Galdona R., Werner D., Martínez-Romero E. 2005a; Bradyrhizobium canariense sp. nov., an acid-tolerant endosymbiont that nodulates endemic genistoid legumes (Papilionoideae: Genisteae) from the Canary Islands, along with Bradyrhizobium japonicum bv. genistearum, Bradyrhizobium genospecies alpha and Bradyrhizobium genospecies beta. Int J Syst Evol Microbiol 55:569–575 [View Article][PubMed]
    [Google Scholar]
  44. Vinuesa P., Silva C., Lorite M. J., Izaguirre-Mayoral M. L., Bedmar E. J., Martínez-Romero E. 2005b; Molecular systematics of rhizobia based on maximum likelihood and Bayesian phylogenies inferred from rrs, atpD, recA and nifH sequences, and their use in the classification of Sesbania microsymbionts from Venezuelan wetlands. Syst Appl Microbiol 28:702–716 [View Article][PubMed]
    [Google Scholar]
  45. Wang J. Y., Zhang Y. M., Wang R., Liu H. C., Wang E. T., Sui X. H., Chen W. X. 2012; Bradyrhizobium daqingense sp. nov., a novel root nodule bacteria isolated from nodules of soybean grown in Daqing City of China. Int J Syst Evol Microbiol (in press) http://dx.doi.org/10.1099/ijs.0.034280-0 [View Article]
    [Google Scholar]
  46. Wayne L. G., Brenner D. J., Colwell R. R., Grimont P. A. D., Kandler O., Krichevsky M. I., Moore L. H., Moore W. E. C., Murray R. G. E. other authors 1987; International Committee on Systematic Bacteriology. Report of the ad hoc committee on reconciliation of approaches to bacterial systematics. Int J Syst Bacteriol 37:463–464 [View Article]
    [Google Scholar]
  47. Weisburg W. G., Barns S. M., Pelletier D. A., Lane D. J. 1991; 16S ribosomal DNA amplification for phylogenetic study. J Bacteriol 173:697–703[PubMed]
    [Google Scholar]
  48. Willems A., Collins M. D. 1992; Evidence for a close genealogical relationship between Afipia (the causal organism of cat scratch disease), Bradyrhizobium japonicum and Blastobacter denitrificans . FEMS Microbiol Lett 96:241–246 [View Article][PubMed]
    [Google Scholar]
  49. Willems A., Munive A., de Lajudie P., Gillis M. 2003; In most Bradyrhizobium groups sequence comparison of 16S-23S rDNA internal transcribed spacer regions corroborates DNA-DNA hybridizations. Syst Appl Microbiol 26:203–210 [View Article][PubMed]
    [Google Scholar]
  50. Young J. P. W. 1996; Phylogeny and taxonomy of rhizobia. Plant Soil 186:45–52 [View Article]
    [Google Scholar]
  51. Zhang Y. M., Li Y. Jr, Chen W. F., Wang E. T., Tian C. F., Li Q. Q., Zhang Y. Z., Sui X. H., Chen W. X. 2011; Biodiversity and biogeography of rhizobia associated with soybean plants grown in the North China Plain. Appl Environ Microbiol 77:6331–6342 [View Article][PubMed]
    [Google Scholar]
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