1887

Abstract

Thirteen slow-growing rhizobial strains isolated from root nodules of soybean ( L.) grown in Daqing city in China were classified in the genus based on 16S rRNA gene sequence analysis. Multilocus sequence analysis of IGS, , and genes revealed that the isolates represented a novel clade in this genus. DNA–DNA relatedness lower than 42.5 % between the representative strain CCBAU 15774 and the type strains of the closely related species USDA 3622, CCBAU 10071 and LMG 21987, further confirmed that this group represented a novel species. CCBAU 15774 shared seven cellular fatty acids with the three above-mentioned species, but the fatty acids 15 : 0 iso and summed feature 5 (18 : 2ω6,9 and/or 18 : 0 anteiso) were unique for this strain. The respiratory quinone in CCBAU 15774 was ubiquinone-10 and the cellular polar lipids were phosphatidylethanolamine, phosphatidylglycerol, phosphatidylcholine, cardiolipin and unknown aminolipid, polar lipid and phospholipid. In addition, some phenotypic features could be used to differentiate the novel group from the related species. On basis of these results, we propose the name sp. nov., with CCBAU 15774 ( = LMG 26137 = HAMBI 3184 = CGMCC 1.10947) as the type strain. The DNA G+C content of the type strain is 61.2 mol% ( ).

Loading

Article metrics loading...

/content/journal/ijsem/10.1099/ijs.0.034280-0
2013-02-01
2019-10-20
Loading full text...

Full text loading...

/deliver/fulltext/ijsem/63/2/616.html?itemId=/content/journal/ijsem/10.1099/ijs.0.034280-0&mimeType=html&fmt=ahah

References

  1. Bergersen F. J. . ( 1961; ). The growth of Rhizobium in synthetic media.. Aust J Biol 14:, 349–360.
    [Google Scholar]
  2. Brunel B. , Rome S. , Ziani R. , Cleyet-Marel J. C. . ( 1996; ). Comparison of nucleotide diversity and symbiotic properties of Rhizobium meliloti populations from annual Medicago species. . FEMS Microbiol Ecol 19:, 71–82. [CrossRef]
    [Google Scholar]
  3. 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. [CrossRef] [PubMed]
    [Google Scholar]
  4. 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. [CrossRef] [PubMed]
    [Google Scholar]
  5. Cho J. C. , Tiedje J. M. . ( 2000; ). Biogeography and degree of endemicity of Pseudomonas fluorescent strains in soil. . Appl Environ Microbiol 66:, 5448–5456. [CrossRef] [PubMed]
    [Google Scholar]
  6. Choma A. , Komaniecka I. . ( 2003; ). The polar lipid composition of Mesorhizobium ciceri . . Biochim Biophys Acta 1631:, 188–196. [CrossRef] [PubMed]
    [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. [CrossRef] [PubMed]
    [Google Scholar]
  8. Felsenstein J. . ( 1985; ). Confidence limits on phylogenies: an approach using the bootstrap. . Evolution 39:, 783–791. [CrossRef]
    [Google Scholar]
  9. Gao J. , Sun J. , Li Y. , Wang E. , Chen W. . ( 1994; ). Numerical taxonomy and DNA relatedness of tropical rhizobia isolated from Hainan Province, China. . Int J Syst Bacteriol 44:, 151–158. [CrossRef]
    [Google Scholar]
  10. Graham P. , Sadowsky M. , Keyser H. , Barnet Y. , Bradley R. , Cooper J. , De Ley D. , Jarvis B. , Roslycky E. . & other authors ( 1991; ). Proposed minimal standards for the description of new genera and species of root-and stem-nodulating bacteria. . Int J Syst Bacteriol 41:, 582–587.[CrossRef]
    [Google Scholar]
  11. Han L. , Wang E. , Han T. , Liu J. , Sui X. , Chen W. , Chen W. . ( 2009; ). Unique community structure and biogeography of soybean rhizobia in the saline-alkaline soils of Xinjiang, China. . Plant Soil 324:, 291–305. [CrossRef]
    [Google Scholar]
  12. Haukka K. , Lindström K. , Young J. P. . ( 1998; ). Three phylogenetic groups of nodA and nifH genes in Sinorhizobium and Mesorhizobium isolates from leguminous trees growing in Africa and Latin America. . Appl Environ Microbiol 64:, 419–426.[PubMed]
    [Google Scholar]
  13. Healy M. , Huong J. , Bittner T. , Lising M. , Frye S. , Raza S. , Schrock R. , Manry J. , Renwick A. . & other authors ( 2005; ). Microbial DNA typing by automated repetitive-sequence-based PCR. . J Clin Microbiol 43:, 199–207. [CrossRef] [PubMed]
    [Google Scholar]
  14. 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]
  15. 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. [CrossRef] [PubMed]
    [Google Scholar]
  16. Jordan D. C. . ( 1982; ). Transfer of Rhizobium japonicum to Bradyrhizobium gen. nov., a genus of slow-growing, root nodule bacteria from leguminous plants. . Int J Syst Bacteriol 32:, 136–139. [CrossRef]
    [Google Scholar]
  17. Jukes T. H. , Cantor C. R. . ( 1969; ). Evolution of protein molecules. . In Mammalian Protein Metabolism, vol. 3, pp. 21–132. Edited by Munro H. N. . . New York:: Academic Press;.
    [Google Scholar]
  18. Kimura M. . ( 1983; ). The Neutral Theory of Molecular Evolution. Cambridge:: Cambridge University Press;. [CrossRef]
    [Google Scholar]
  19. Kumar S. , Tamura K. , Nei M. . ( 1994; ). mega: molecular evolutionary genetics analysis software for microcomputers. . Comput Appl Biosci 10:, 189–191.[PubMed]
    [Google Scholar]
  20. Kumar S. , Nei M. , Dudley J. , Tamura K. . ( 2008; ). mega: a biologist-centric software for evolutionary analysis of DNA and protein sequences. . Brief Bioinform 9:, 299–306. [CrossRef] [PubMed]
    [Google Scholar]
  21. Kuykendall L. D. , Saxena B. , Devine T. E. , Udell S. E. . ( 1992; ). Genetic diversity in Bradyrhizobium japonicum Jordan 1982 and a proposal for Bradyrhizobium elkanii sp. nov.. Can J Microbiol 38:, 501–505. [CrossRef]
    [Google Scholar]
  22. Kwon S. W. , Park J. Y. , Kim J. S. , Kang J. W. , Cho Y. H. , Lim C. K. , Parker M. A. , Lee G. B. . ( 2005; ). Phylogenetic analysis of the genera Bradyrhizobium, Mesorhizobium, Rhizobium and Sinorhizobium on the basis of 16S rRNA gene and internally transcribed spacer region sequences. . Int J Syst Evol Microbiol 55:, 263–270. [CrossRef] [PubMed]
    [Google Scholar]
  23. Laguerre G. , Mavingui P. , Allard M. R. , Charnay M. P. , Louvrier P. , Mazurier S. I. , Rigottier-Gois L. , Amarger N. . ( 1996; ). Typing of rhizobia by PCR DNA fingerprinting and PCR-restriction fragment length polymorphism analysis of chromosomal and symbiotic gene regions: application to Rhizobium leguminosarum and its different biovars. . Appl Environ Microbiol 62:, 2029–2036.[PubMed]
    [Google Scholar]
  24. 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]
  25. Lee J. S. , Shin Y. K. , Yoon J. H. , Takeuchi M. , Pyun Y. R. , Park Y. H. . ( 2001; ). Sphingomonas aquatilis sp. nov., Sphingomonas koreensis sp. nov., and Sphingomonas taejonensis sp. nov., yellow-pigmented bacteria isolated from natural mineral water. . Int J Syst Evol Microbiol 51:, 1491–1498.[PubMed]
    [Google Scholar]
  26. Li Q. Q. , Wang E. T. , Zhang Y. Z. , Zhang Y. M. , Tian C. F. , Sui X. H. , Chen W. F. , Chen W. X. . ( 2011a; ). Diversity and biogeography of rhizobia isolated from root nodules of Glycine max grown in Hebei Province, China. . Microb Ecol 61:, 917–931. [CrossRef] [PubMed]
    [Google Scholar]
  27. Li Q. Q. , Wang E. T. , Chang Y. L. , Zhang Y. Z. , Zhang Y. M. , Sui X. H. , Chen W. F. , Chen W. X. . ( 2011b; ). Ensifer sojae sp. nov., isolated from root nodules of Glycine max grown in saline-alkaline soils. . Int J Syst Evol Microbiol 61:, 1981–1988. [CrossRef] [PubMed]
    [Google Scholar]
  28. Liu X. B. , Jin J. , Wang G. H. , Herbert S. J. . ( 2008; ). Soybean yield physiology and development of high-yielding practices in Northeast China. . Field Crops Res 105:, 157–171. [CrossRef]
    [Google Scholar]
  29. Ludwig W. , Rossello-Mora R. , Aznar R. , Klugbauer S. , Spring S. , Reetz K. , Beimfohr C. , Brockmann E. , Kirchhof G. . & other authors ( 1995; ). Comparative sequence analysis of 23S rRNA from Proteobacteria . . Syst Appl Microbiol 18:, 164–188. [CrossRef]
    [Google Scholar]
  30. Man C. , Wang H. , Chen W. , Sui X. , Wang E. , Chen W. . ( 2008; ). Diverse rhizobia associated with soybean grown in the subtropical and tropical regions of China. . Plant Soil 310:, 77–87. [CrossRef]
    [Google Scholar]
  31. Marmur J. . ( 1961; ). A procedure for the isolation of deoxyribonucleic acid from microorganisms. . J Mol Biol 3:, 208–218. [CrossRef]
    [Google Scholar]
  32. Marmur J. , Doty P. . ( 1962; ). Determination of the base composition of deoxyribonucleic acid from its thermal denaturation temperature. . J Mol Biol 5:, 109–118. [CrossRef] [PubMed]
    [Google Scholar]
  33. Miller K. J. , Shon B. C. , Gore R. S. , Hunt W. P. . ( 1990; ). The phospholipid composition of Bradyrhizobium spp. . Curr Microbiol 21:, 205–210. [CrossRef]
    [Google Scholar]
  34. Minder A. C. , de Rudder K. E. E. , Narberhaus F. , Fischer H. M. , Hennecke H. , Geiger O. . ( 2001; ). Phosphatidylcholine levels in Bradyrhizobium japonicum membranes are critical for an efficient symbiosis with the soybean host plant. . Mol Microbiol 39:, 1186–1198. [CrossRef] [PubMed]
    [Google Scholar]
  35. 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. [CrossRef]
    [Google Scholar]
  36. Nick G. , Lindstrom K. . ( 1994; ). Use of repetitive sequences and the polymerase chain reaction to fingerprint the genomic DNA of Rhizobium galegae strains and to identify the DNA obtained by sonicating the liquid cultures and root nodules. . Syst Appl Microbiol 17:, 265–273. [CrossRef]
    [Google Scholar]
  37. Ohta H. , Hattori T. . ( 1983; ). Agromonas oligotrophica gen. nov., sp. nov., a nitrogen-fixing oligotrophic bacterium. . Antonie van Leeuwenhoek 49:, 429–446.[PubMed]
    [Google Scholar]
  38. Orgambide G. G. , Huang Z. H. , Gage D. A. , Dazzo F. B. . ( 1993; ). Phospholipid and fatty acid compositions of Rhizobium leguminosarum biovar trifolii ANU843 in relation to flavone-activated pSym nod gene expression. . Lipids 28:, 975–979. [CrossRef] [PubMed]
    [Google Scholar]
  39. Rademaker J. L. , Hoste B. , Louws F. J. , Kersters K. , Swings J. , Vauterin L. , Vauterin P. , de Bruijn F. J. . ( 2000; ). Comparison of AFLP and rep-PCR genomic fingerprinting with DNA– DNA homology studies: Xanthomonas as a model system. . Int J Syst Evol Microbiol 50:, 665–677. [CrossRef] [PubMed]
    [Google Scholar]
  40. 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. [CrossRef] [PubMed]
    [Google Scholar]
  41. 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. [CrossRef] [PubMed]
    [Google Scholar]
  42. Rivas R. , Martens M. , de Lajudie P. , Willems A. . ( 2009; ). Multilocus sequence analysis of the genus Bradyrhizobium . . Syst Appl Microbiol 32:, 101–110. [CrossRef] [PubMed]
    [Google Scholar]
  43. Sahgal M. , Johri B. N. . ( 2006; ). Taxonomy of rhizobia: current status. . Curr Sci 90:, 486–487.
    [Google Scholar]
  44. 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]
  45. 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. [CrossRef] [PubMed]
    [Google Scholar]
  46. Sasser, M. (1990). Identification of bacteria by gas chromatography of cellular fatty acids, MIDI Technical Note 101. Newark, DE: MIDI Inc.
  47. Schutter M. E. , Dick R. P. . ( 2000; ). Comparison of fatty acid methylester (FAME) methods for characterizing microbial communities. . Soil Sci Soc Am J 64:, 1659–1668. [CrossRef]
    [Google Scholar]
  48. 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. [CrossRef] [PubMed]
    [Google Scholar]
  49. Tighe S. W. , de Lajudie P. , Dipietro K. , Lindström K. , Nick G. , Jarvis B. D. W. . ( 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. [CrossRef] [PubMed]
    [Google Scholar]
  50. Tindall B. J. , Rosselló-Móra R. , Busse H.-J. , Ludwig W. , Kämpfer P. . ( 2010; ). Notes on the characterization of prokaryote strains for taxonomic purposes. . Int J Syst Evol Microbiol 60:, 249–266. [CrossRef] [PubMed]
    [Google Scholar]
  51. 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. [CrossRef] [PubMed]
    [Google Scholar]
  52. Versalovic J. , Schneider M. , de Bruijn F. J. , Lupski J. R. . ( 1994; ). Genomic fingerprinting of bacteria using repetitive sequence-based polymerase chain reaction. . Methods Mol Cell Biol 5:, 25–40.
    [Google Scholar]
  53. Vincent J. M. . ( 1970; ). Manual for the Practical Study of the Root-Nodule Bacteria, IBP Handbook, vol. 15. Oxford:: Blackwell;.
    [Google Scholar]
  54. 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 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. [CrossRef] [PubMed]
    [Google Scholar]
  55. Vinuesa P. , Silva C. , Werner D. , Martínez-Romero E. . ( 2005b; ). Population genetics and phylogenetic inference in bacterial molecular systematics: the roles of migration and recombination in Bradyrhizobium species cohesion and delineation. . Mol Phylogenet Evol 34:, 29–54. [CrossRef] [PubMed]
    [Google Scholar]
  56. Wang F. Q. , Wang E. T. , Liu J. , Chen Q. , Sui X. H. , Chen W. F. , Chen W. X. . ( 2007; ). Mesorhizobium albiziae sp. nov., a novel bacterium nodulating Albizia kalkora in a subtropical region of China. . Int J Syst Evol Microbiol 57:, 1192–1199. [CrossRef] [PubMed]
    [Google Scholar]
  57. Wang H. , Man C. , Wang E. , Chen W. . ( 2009; ). Diversity of rhizobia and interactions among the host legumes and rhizobial genotypes in an agricultural-forestry ecosystem. . Plant Soil 314:, 169–182. [CrossRef]
    [Google Scholar]
  58. 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. [CrossRef]
    [Google Scholar]
  59. 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. [CrossRef] [PubMed]
    [Google Scholar]
  60. Willems A. , Coopman R. , Gillis M. . ( 2001a; ). Phylogenetic and DNA–DNA hybridization analyses of Bradyrhizobium species. . Int J Syst Evol Microbiol 51:, 111–117.[PubMed]
    [Google Scholar]
  61. Willems A. , Coopman R. , Gillis M. . ( 2001b; ). Comparison of sequence analysis of 16S–23S rDNA spacer regions, AFLP analysis and DNA–DNA hybridizations in Bradyrhizobium . . Int J Syst Evol Microbiol 51:, 623–632.[PubMed]
    [Google Scholar]
  62. 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. [CrossRef] [PubMed]
    [Google Scholar]
  63. Xu L. M. , Ge C. , Cui Z. , Li J. , Fan H. . ( 1995; ). Bradyrhizobium liaoningense sp. nov., isolated from the root nodules of soybeans. . Int J Syst Bacteriol 45:, 706–711. [CrossRef] [PubMed]
    [Google Scholar]
  64. Yao Z. Y. , Kan F. L. , Wang E. T. , Wei G. H. , Chen W. X. . ( 2002; ). Characterization of rhizobia that nodulate legume species of the genus Lespedeza and description of Bradyrhizobium yuanmingense sp. nov.. Int J Syst Evol Microbiol 52:, 2219–2230. [CrossRef] [PubMed]
    [Google Scholar]
  65. 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. [CrossRef] [PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/ijsem/10.1099/ijs.0.034280-0
Loading
/content/journal/ijsem/10.1099/ijs.0.034280-0
Loading

Data & Media loading...

Supplements

Supplementary material 

PDF

Most Cited This Month

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error