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INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY logo

Volume 59, Issue 12

Phylogeny and taxonomy of a diverse collection of strains based on multilocus sequence analysis of the 16S rRNA gene, ITS region and , , and genes Free

Abstract

The genus encompasses a variety of bacteria that can live in symbiotic and endophytic associations with legumes and non-legumes, and are characterized by physiological and symbiotic versatility and broad geographical distribution. However, despite indications of great genetic variability within the genus, only eight species have been described, mainly because of the highly conserved nature of the 16S rRNA gene. In this study, 169 strains isolated from 43 different legumes were analysed by rep-PCR with the BOX primer, by sequence analysis of the 16S rRNA gene and the 16S–23S rRNA intergenic transcribed spacer (ITS) and by multilocus sequence analysis (MLSA) of four housekeeping genes, , , and . Considering a cut-off at a level of 70 % similarity, 80 rep-PCR profiles were distinguished, which, together with type strains, were clustered at a very low level of similarity (24 %). In both single and concatenated analyses of the 16S rRNA gene and ITS sequences, two large groups were formed, with bootstrap support of 99 % in the concatenated analysis. The first group included the type and/or reference strains of , , , and . and USDA 110, and the second group included strains related to USDA 76, PAC48 and PAC68. Similar results were obtained with MLSA of , , and . Greatest variability was observed when the gene was amplified, and five strains related to revealed a level of variability never reported before. Another important observation was that a group composed of strains USDA 110, SEMIA 5080 and SEMIA 6059, all isolated from soybean, clustered in all six trees with high bootstrap support and were quite distinct from the clusters that included USDA 6. The results confirm that MLSA is a rapid and reliable way of providing information on phylogenetic relationships and of identifying rhizobial strains potentially representative of novel species.

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Keyword(s): ITS, intergenic transcribed spacer and MLSA, multilocus sequence analysis
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References

  1. Abaidoo, R. C., Keyser, H. H., Singleton, P. W. & Borthakur, D.(2000).Bradyrhizobium spp. (TGx) isolates nodulating the new soybean cultivars in Africa are diverse and distinct from bradyrhizobia that nodulate North American soybeans. Int J Syst Evol Microbiol 50, 225–234.[CrossRef] [Google Scholar]
  2. Achtman, M. & Wagner, M.(2008). Microbial diversity and the genetic nature of microbial species. Nat Rev Microbiol 6, 431–440. [Google Scholar]
  3. Alberton, O., Kaschuk, G. & Hungria, M.(2006). Sampling effects on the assessment of genetic diversity of rhizobia associated with soybean and common bean. Soil Biol Biochem 38, 1298–1307.[CrossRef] [Google Scholar]
  4. Barrera, L. L., Trujillo, M. E., Goodfellow, M., Garcia, F. J., Hernandez-Lucas, I., Davila, G., van Berkum, P. & Martinez-Romero, E.(1997). Biodiversity of bradyrhizobia nodulating Lupinus spp. Int J Syst Bacteriol 47, 1086–1091.[CrossRef] [Google Scholar]
  5. Batista, J. S. S., Hungria, M., Barcellos, F. G., Ferreira, M. C. & Mendes, I. C.(2007). Variability in Bradyrhizobium japonicum and B. elkanii seven years after introduction of both the exotic microsymbiont and the soybean host in a Cerrados soil. Microb Ecol 53, 270–284.[CrossRef] [Google Scholar]
  6. Brett, P. J., Deshazer, D. & Woods, D. E.(1998).Burkholderia thailandensis sp. nov., a Burkholderia pseudomallei-like species. Int J Syst Bacteriol 48, 317–320.[CrossRef] [Google Scholar]
  7. Bull, J. J., Huelsenbeck, J. P., Cunningham, C. W., Swofford, D. L. & Waddell, P. J.(1993). Partitioning and combining data in phylogenetic analyses. Syst Biol 42, 384–397.[CrossRef] [Google Scholar]
  8. Coenye, T., Gevers, D., Van de Peer, Y., Vandamme, P. & Swings, J.(2005). Towards a prokaryotic genomic taxonomy. FEMS Microbiol Rev 29, 147–167. [Google Scholar]
  9. Cooper, J. E. & Feil, E. J.(2004). Multilocus sequence typing – what is resolved? Trends Microbiol 12, 373–377.[CrossRef] [Google Scholar]
  10. Doignon-Bourcier, F., Willems, A., Coopman, R., Laguerre, G., Gillis, M. & de Lajudie, P.(2000). Genotypic characterization of Bradyrhizobium strains nodulating small Senegalese legumes by 16S–23S rRNA interfgenic gene spacers and amplified length polymorphism fingerprint analyses. Appl Environ Microbiol 66, 3987–3997.[CrossRef] [Google Scholar]
  11. Dupuy, N. C. & Dreyfus, B. L.(1992).Bradyrhizobium populations occur in deep soil under the leguminous tree Acacia albida. Appl Environ Microbiol 58, 2415–2419. [Google Scholar]
  12. Ewing, B. & Green, P.(1998). Base-calling of automated sequencer traces using phred. II. Error probabilities. Genome Res 8, 186–194. [Google Scholar]
  13. Ewing, B., Hillier, L., Wendl, M. C. & Green, P.(1998). Base-calling of automated sequencer traces using phred. I. Accuracy assessment. Genome Res 8, 175–185.[CrossRef] [Google Scholar]
  14. Felsenstein, J.(1985). Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39, 783–791.[CrossRef] [Google Scholar]
  15. Garrity, G. M. & Holt, J. G.(2001). The road map to the Manual. In Bergey's Manual of Systematic Bacteriology, 2nd edn, vol. 1, pp. 119–166. Edited by D. R. Boone, R. W. Castenholz & G. M. Garrity. New York: Springer.
  16. Gaunt, M. W., Turner, S. L., Rigottier-Gois, L., Lloyd-Macgilp, S. A. & Young, J. P.(2001). Phylogenies of atpD and recA support the small subunit rRNA-based classification of rhizobia. Int J Syst Evol Microbiol 51, 2037–2048.[CrossRef] [Google Scholar]
  17. Germano, M. G., Menna, P., Mostasso, F. L. & Hungria, M.(2006). RFLP analysis of the rRNA operon of a Brazilian collection of bradyrhizobial strains from 33 legume species. Int J Syst Evol Microbiol 56, 217–229.[CrossRef] [Google Scholar]
  18. Giongo, A., Ambrosini, A., Vargas, L. K., Freire, J. R. J., Bodanese-Zanettini, M. H. & Passaglia, L. M. P.(2008). Evaluation of genetic diversity of bradyrhizobia strains nodulating soybean [Glycine max (L.) Merrill] isolated from South Brazilian fields. Appl Soil Ecol 38, 261–269.[CrossRef] [Google Scholar]
  19. Godoy, D., Randle, G., Simpson, A. J., Aanensen, D. M., Pitt, T. L., Kinoshita, R. & Spratt, B. G.(2003). Multilocus sequence typing and evolutionary relationships among the causative agents of melioidosis and glanders, Burkholderia pseudomallei and Burkholderia mallei. J Clin Microbiol 41, 2068–2079.[CrossRef] [Google Scholar]
  20. Gordon, D., Abajian, C. & Green, P.(1998). Consed: a graphical tool for sequence finishing. Genome Res 8, 195–202.[CrossRef] [Google Scholar]
  21. Grange, L. & Hungria, M.(2004). Genetic diversity of indigenous common bean (Phaseolus vulgaris) rhizobia in two Brazilian ecosystems. Soil Biol Biochem 36, 1389–1398.[CrossRef] [Google Scholar]
  22. Hedges, S. B.(1992). The number of replications needed for accurate estimation of the bootstrap p-value in phylogenetic studies. Mol Biol Evol 9, 366–369. [Google Scholar]
  23. Hungria, M., Chueire, L. M. O., Megías, M., Lamrabet, Y., Probanza, A., Guttierrez-Mañero, F. J. & Campo, R. J.(2006). Genetic diversity of indigenous tropical fast-growing rhizobia isolated from soybean nodules. Plant Soil 288, 343–356.[CrossRef] [Google Scholar]
  24. Jaccard, P.(1912). The distribution of the flora in the alpine zone. New Phytol 11, 37–50.[CrossRef] [Google Scholar]
  25. Jordan, D. C.(1982). Transfer of Rhizobium japonicum Buchan 1980 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]
  26. Kaschuk, G., Hungria, M., Andrade, D. S. & Campo, R. J.(2006a). Genetic diversity of rhizobia associated with common bean (Phaseolus vulgaris L.) grown under no-tillage and conventional systems in Southern Brazil. Appl Soil Ecol 32, 210–220.[CrossRef] [Google Scholar]
  27. Kaschuk, G., Hungria, M., Santos, J. C. P. & Berton-Junior, J. F.(2006b). Differences in common bean rhizobial populations associated with soil tillage management in southern Brazil. Soil Tillage Res 87, 205–217.[CrossRef] [Google Scholar]
  28. 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.[CrossRef] [Google Scholar]
  29. Koeuth, T., Versalovic, J. & Lupski, J. R.(1995). Differential subsequence conservation of interspersed repetitive Streptococcus pneumoniae BOX elements in diverse bacteria. Genome Res 5, 408–418.[CrossRef] [Google Scholar]
  30. Konstantinidis, K. T. & Tiedje, J. M.(2004). Trends between gene content and genome size in prokaryotic species with larger genomes. Proc Natl Acad Sci U S A 101, 3160–3165.[CrossRef] [Google Scholar]
  31. 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]
  32. 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. [Google Scholar]
  33. Liu, J., Wang, E. T. & Chen, W. X.(2005). Diverse rhizobia associated with woody legumes Wisteria sinensis, Cercis racemosa and Amorpha fruticosa grown in the temperate zone of China. Syst Appl Microbiol 28, 465–477.[CrossRef] [Google Scholar]
  34. Loureiro, M. F., Kaschuk, G., Alberton, O. & Hungria, M.(2007). Soybean [Glycine max (L.) Merrill] rhizobial diversity in Brazilian oxisols under various soil, cropping and inoculation managements. Biol Fertil Soils 43, 665–674.[CrossRef] [Google Scholar]
  35. Ludwig, W. & Schleifer, K. H.(1994). Bacterial phylogeny based on 16S and 23S rRNA sequence analysis. FEMS Microbiol Rev 15, 155–173.[CrossRef] [Google Scholar]
  36. Maiden, M. C. J., Bygraves, J. A., Feil, E., Morelli, G., Russell, J. E., Urwin, R., Zhang, Q., Zhou, J., Zurth, K. & other authors(1998). Multilocus sequence typing: a portable approach to the identification of clones within populations of pathogenic microorganisms. Proc Natl Acad Sci U S A 95, 3140–3145.[CrossRef] [Google Scholar]
  37. Martens, M., Delaere, M., Coopman, R., De Vos, P., Gillis, M. & Willems, A.(2007). Multilocus sequence analysis of Ensifer and related taxa. Int J Syst Evol Microbiol 57, 489–503.[CrossRef] [Google Scholar]
  38. Menna, P., Hungria, M., Barcellos, F. G., Bangel, E. V., Hess, P. N. & Martinez-Romero, E.(2006). Molecular phylogeny based on the 16S rRNA gene of elite rhizobial strains used in Brazilian commercial inoculants. Syst Appl Microbiol 29, 315–332.[CrossRef] [Google Scholar]
  39. Menna, P., Pereira, A. A., Bangel, E. V. & Hungria, M.(2009). rep-PCR of tropical rhizobia for strain fingerprinting, biodiversity appraisal and as a taxonomic and phylogenetic tool. Symbiosis 48, 120–130.[CrossRef] [Google Scholar]
  40. Miyamoto, M. M. & Fitch, W. M.(1995). Testing species phylogenies and phylogenetic methods with congruence. Syst Biol 44, 64–76.[CrossRef] [Google Scholar]
  41. Mostasso, L., Mostasso, F. L., Dias, B. G., Vargas, M. A. T. & Hungria, M.(2002). Selection of bean (Phaseolus vulgaris L.) rhizobial strains for the Brazilian Cerrados. Field Crops Res 73, 121–132.[CrossRef] [Google Scholar]
  42. Moulin, L., Béna, G., Boivin-Masson, C. & Stepkowski, T.(2004). Phylogenetic analysis of symbiotic nodulation genes support vertical and lateral gene co-transfer within the Bradyrhizobium genus. Mol Phylogenet Evol 30, 720–732.[CrossRef] [Google Scholar]
  43. Olsen, G. J. & Woese, C. R.(1993). Ribosomal RNA: a key to phylogeny. FASEB J 7, 113–123. [Google Scholar]
  44. Parker, M. A.(2004). rRNA and dnaK relationships of Bradyrhizobium sp. nodule bacteria from four Papilionoid legume trees in Costa Rica. Syst Appl Microbiol 27, 334–342.[CrossRef] [Google Scholar]
  45. Parker, M. A. & Lunk, A.(2000). Relationships of bradyrhizobia from Platypodium and Machaerium (Papilionoideae: tribe Dalbergieae) on Barro Colorado Island, Panama. Int J Syst Evol Microbiol 50, 1179–1186.[CrossRef] [Google Scholar]
  46. Pérez-Ramírez, N. O., Rogel, M. A., Wang, E., Castellanos, J. Z. & Martínez-Romero, E.(1998). Seeds of Phaseolus vulgaris bean carry Rhizobium etli. FEMS Microbiol Ecol 26, 289–296.[CrossRef] [Google Scholar]
  47. Pinto, F. G. S., Hungria, M. & Mercante, F. M.(2007). Polyphasic characterization of Brazilian Rhizobium tropici strains effective in fixing N2 with common bean (Phaseolus vulgaris L.). Soil Biol Biochem 39, 1851–1864.[CrossRef] [Google Scholar]
  48. Qian, J., Kwon, S. W. & Parker, M. A.(2003). rRNA and nifD phylogeny of Bradyrhizobium from sites across the Pacific Basin. FEMS Microbiol Lett 219, 159–165.[CrossRef] [Google Scholar]
  49. Ramírez-Bahena, M.-H., Peix, A., Rivas, P., 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] [Google Scholar]
  50. Ribeiro, R. A., Barcellos, F. G., Thompson, F. L. & Hungria, M.(2009). Multilocus sequence analysis of Brazilian Rhizobium microsymbionts of common bean (Phaseolus vulgaris L.) reveals unexpected taxonomic diversity. Res Microbiol 160, 297–306.[CrossRef] [Google Scholar]
  51. 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] [Google Scholar]
  52. Rodríguez-Navarro, D. N., Camacho, M., Leidi, E. O., Rivas, R. & Velázquez, E.(2004). Phenotypic and genotypic characterization of rhizobia from diverse geographical origin that nodulate Pachyrhizus species. Syst Appl Microbiol 27, 737–745.[CrossRef] [Google Scholar]
  53. Saito, A., Mitsui, H., Hattori, R., Minamisawa, K. & Hattori, T.(1998). Slow-growing and oligotrophic soil bacteria phylogenetically close to Bradyrhizobium japonicum. FEMS Microbiol Ecol 25, 277–286.[CrossRef] [Google Scholar]
  54. Saitou, N. & Nei, M.(1987). The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4, 406–425. [Google Scholar]
  55. Saldaña, G., Martinez-Alcántara, V., Vinardell, J. M., Bellogín, R., Ruíz-Sainz, J. E. & Balatti, P. A.(2003). Genetic diversity of fast-growing rhizobia that nodulate soybean (Glycine max L. Merr.). Arch Microbiol 180, 45–52.[CrossRef] [Google Scholar]
  56. Santillana, N., Ramírez-Bahena, M. H., García-Fraile, P., Velázquez, E. & Zúñiga, D.(2008). Phylogenetic diversity based on rrs, atpD, recA genes and 16S–23S intergenic sequence analyses of rhizobial strains isolated from Vicia faba and Pisum sativum in Peru. Arch Microbiol 189, 239–247.[CrossRef] [Google Scholar]
  57. Sawada, H., Kuykendall, L. D. & Young, J. M.(2003). Changing concepts in the systematics of bacterial nitrogen-fixing legume symbionts. J Gen Appl Microbiol 49, 155–179.[CrossRef] [Google Scholar]
  58. Sneath, P. H. A. & Sokal, R. R.(1973).Numerical Taxonomy. San Francisco: W. H. Freeman.
  59. Sprent, J. I.(2001).Nodulation in Legumes. Kew, UK: Royal Botanic Gardens.
  60. Stepkowski, T., Czaplínska, M., Miedzinska, K. & Moulin, L.(2003). The variable part of the dnaK gene as an alternative marker for phylogenetic studies of rhizobia and related alpha Proteobacteria. Syst Appl Microbiol 26, 483–494.[CrossRef] [Google Scholar]
  61. Stepkowski, T., Moulin, L., Krzyzanska, A., McInnes, A., Law, I. J. & Howieson, J.(2005). European origin of Bradyrhizobium populations infecting lupins and serradella in soils of western Australia and South Africa. Appl Environ Microbiol 71, 7041–7052.[CrossRef] [Google Scholar]
  62. Strijdom, B. W.(1998). South African studies on biological nitrogen-fixing systems and the exploitation of the nodule bacterium-legume symbiosis. S Afr J Sci 94, 11–23. [Google Scholar]
  63. Tan, Z., Hurek, T., Vinuesa, P., Muller, P., Ladha, J. K. & Reinhold-Hurek, B.(2001). Specific detection of Bradyrhizobium and Rhizobium strains colonizing rice (Oryza sativa) roots by 16S–23S ribosomal DNA intergenic spacer-targeted PCR. Appl Environ Microbiol 67, 3655–3664.[CrossRef] [Google Scholar]
  64. Trinick, M. J.(1973). Symbiosis between Rhizobium and the non-legume, Trema aspera. Nature 244, 459–460.[CrossRef] [Google Scholar]
  65. Turner, S. L. & Young, J. P. W.(2000). The glutamine synthetase of rhizobia: phylogenetics and evolutionary implications. Mol Biol Evol 17, 309–319.[CrossRef] [Google Scholar]
  66. van Berkum, P. & Eardly, B. D.(2002). The aquatic budding bacterium Blastobacter denitrificans is a nitrogen-fixing symbiont of Aeschynomene indica. Appl Environ Microbiol 68, 1132–1136.[CrossRef] [Google Scholar]
  67. van Berkum, P. & Fuhrmann, J. J.(2000). Evolutionary relationships among the soybean bradyrhizobia reconstructed from 16S rRNA gene and internally transcribed spacer region sequence divergence. Int J Syst Evol Microbiol 50, 2165–2172.[CrossRef] [Google Scholar]
  68. 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 (Hirsh and Muller, 1985) to the genus Bradyrhizobium as Bradyrhizobium denitrificans (comb. nov.). Syst Appl Microbiol 29, 207–215.[CrossRef] [Google Scholar]
  69. Vandamme, P., Pot, B., Gillis, M., de Vos, P., Kersters, K. & Swings, J.(1996). Polyphasic taxonomy, a consensus approach to bacterial systematics. Microbiol Rev 60, 407–438. [Google Scholar]
  70. 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]
  71. 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.[CrossRef] [Google Scholar]
  72. Vinuesa, P., Silva, C., Werner, D. & Martinez-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] [Google Scholar]
  73. Wang, E. T. & Martínez-Romero, E.(2000). Phylogeny of root- and stem-nodule bacteria associated with legumes. In Prokaryotic Nitrogen Fixation: a Model System for Analysis of a Biological Process, pp. 177–186. Edited by E. W. Triplett. Wymondham, UK: Horizon Scientific.
  74. Wang, F. Q., Wang, E. T., Zhang, Y. F. & Chen, W. X.(2006). Characterization of rhizobia isolated from Albizia spp. in comparison with microsymbionts of Acacia spp. and Leucaena leucocephala grown in China. Syst Appl Microbiol 29, 502–517.[CrossRef] [Google Scholar]
  75. 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 that nodulates Albizia kalkora in a subtropical region of China. Int J Syst Evol Microbiol 57, 1192–1199.[CrossRef] [Google Scholar]
  76. Weir, B. S., Turner, S. J., Silvester, W. B., Park, D. C. & Young, J. M.(2004). Unexpectedly diverse Mesorhizobium strains and Rhizobium leguminosarum nodulate native legume genera of New Zealand, while introduced legume weeds are nodulated by Bradyrhizobium species. Appl Environ Microbiol 70, 5980–5987.[CrossRef] [Google Scholar]
  77. 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. [Google Scholar]
  78. Willems, A. & Collins, M. D.(1993). Phylogenetic analysis of rhizobia and agrobacteria based on 16S rRNA gene sequences. Int J Syst Bacteriol 43, 305–313.[CrossRef] [Google Scholar]
  79. Willems, A., Coopman, R. & Gillis, M.(2001a). Phylogenetic and DNA–DNA hybridization analyses of Bradyrhizobium species. Int J Syst Evol Microbiol 51, 111–117. [Google Scholar]
  80. Willems, A., Doignon-Bourcier, F., Goris, J., Coopman, R., de Lajudie, P., De Vos, P. & Gillis, M.(2001b). DNA–DNA hybridization study of Bradyrhizobium strains. Int J Syst Evol Microbiol 51, 1315–1322. [Google Scholar]
  81. 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] [Google Scholar]
  82. Wolde-Meskel, E., Terefework, Z., Lindström, K. & Frostegard, A.(2004). Rhizobia nodulating African Acacia spp. and Sesbania sesban trees in southern Ethiopian soils are metabolically and genomically diverse. Soil Biol Biochem 36, 2013–2025.[CrossRef] [Google Scholar]
  83. Wong, F. Y. K., Stackebrandt, E., Ladha, J. K., Fleischman, D. E., Date, R. A. & Fuerst, J. A.(1994). Phylogenetic analysis of Bradyrhizobium japonicum and photosynthetic stem-nodulating bacteria from Aeschynomene species grown in separated geographical regions. Appl Environ Microbiol 60, 940–946. [Google Scholar]
  84. 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] [Google Scholar]
  85. Yanagi, M. & Yamasato, K.(1993). Phylogenetic analysis of the family Rhizobiaceae and related bacteria by sequencing of 16S rRNA gene using PCR and DNA sequencer. FEMS Microbiol Lett 107, 115–120.[CrossRef] [Google Scholar]
  86. 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] [Google Scholar]
  87. Young, J. P. W. & Haukka, K. E.(1996). Diversity and phylogeny of rhizobia. New Phytol 133, 87–94.[CrossRef] [Google Scholar]
  88. Young, J. M., Kuykendall, L. D., Martínez-Romero, E., Kerr, A. & Sawada, H.(2001). A revision of Rhizobium Frank 1889, with an emended description of the genus, and the inclusion of all species of Agrobacterium Conn 1942 and Allorhizobium undicola de Lajudie et al. 1998 as new combinations: Rhizobium radiobacter, R. rhizogenes, R. rubi, R. undicola and R. vitis. Int J Syst Evol Microbiol 51, 89–103. [Google Scholar]
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Phylogeny and taxonomy of a diverse collection of Bradyrhizobium strains based on multilocus sequence analysis of the 16S rRNA gene, ITS region and glnII, recA, atpD and dnaK genes
Int J Syst Evol Microbiol 59, 2934 (2009); https://doi.org/10.1099/ijs.0.009779-0
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