Phylogeny of bradyrhizobia from Chinese cowpea miscellany inferred from 16s rRNA, atpD, glnii, and 16S-23S intergenic spacer sequences

Canadian Journal of Microbiology

Volumn 57, Issue 4, 2011, Pages 316-327

  Zhang, Sufang ^a   Xie, Fuli ^a   Yang, Jiangke ^b   Li, Youguo ^a  

^a HUAZHONG AGRICULTURAL UNIVERSITY   (China)

^b HUAZHONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

Author keywords

16S rRNA; atpD; Bradyrhizobia; Cowpea miscellany; Glnii; Intergenic spacer; Phylogeny

Indexed keywords

16S RRNA; ATPD; BRADYRHIZOBIA; COWPEA MISCELLANY; GLNII; INTERGENIC SPACERS; PHYLOGENY;

CULTIVATION; GENES; GEOGRAPHICAL REGIONS; RNA;

PLANTS (BOTANY);

RNA 16S; RNA 23S;

GENETIC ANALYSIS; GEOGRAPHICAL REGION; LEGUME; NODULATION; PHYLOGENY; RELATEDNESS; RHIZOBACTERIUM; RHIZOSPHERE; SPECIES DIVERSITY;

ARTICLE; ATPD GENE; BACTERIAL GENE; BACTERIAL STRAIN; BRADYRHIZOBIACEAE; BRADYRHIZOBIUM; BRADYRHIZOBIUM CANARIENSE; BRADYRHIZOBIUM ELKANII; BRADYRHIZOBIUM JAPONICUM; BRADYRHIZOBIUM LIAONINGENSE; BRADYRHIZOBIUM YUANMINGENSE; CHINA; COWPEA; GENE SEQUENCE; GEOGRAPHIC ORIGIN; GLNLL GENE; HOUSEKEEPING GENE; MUNG BEAN; NODULATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PEANUT; PHYLOGENY; PLANT ROOT; PRIORITY JOURNAL; RIBOSOME; SEQUENCE ANALYSIS; UNINDEXED SEQUENCE;

ARACHIS HYPOGAEA; BRADYRHIZOBIUM; CHINA; DNA, RIBOSOMAL SPACER; FABACEAE; GENES, BACTERIAL; MOLECULAR SEQUENCE DATA; PHYLOGENY; POLYMORPHISM, RESTRICTION FRAGMENT LENGTH; RNA, RIBOSOMAL, 16S;

CHINA;

ARACHIS HYPOGAEA; BRADYRHIZOBIACEAE; BRADYRHIZOBIUM; BRADYRHIZOBIUM CANARIENSE; BRADYRHIZOBIUM ELKANII; BRADYRHIZOBIUM JAPONICUM; BRADYRHIZOBIUM LIAONINGENSE; BRADYRHIZOBIUM YUANMINGENSE; VIGNA RADIATA; VIGNA RADIATA VAR. RADIATA; VIGNA UNGUICULATA;

EID: 79960784704     PISSN: 00084166     EISSN: 14803275     Source Type: Journal    
DOI: 10.1139/w11-008     Document Type: Article

References (55)

1. Allen, O.N., and Allen, E.K. (Editors). 1981. The Leguminosae: a source book of characteristics, uses and nodulation. The University of Wisconsin Press, Madison, Wis., USA.
2. Benhizia, Y., Benhizia, H., Benguedouar, A., Muresu, R., Giacomini, A., and Squartini, A. 2004. Gamma proteobacteria can nodulate legumes of the genus Hedysarum. Syst. Appl. Microbiol. 27(4): 462-468. doi:10.1078/0723202041438527.
3. Chen, W.X., Yan, G.H., and 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(4): 392-397. doi:10.1099/00207713-38-4-392.
4. Chen, W.M., Laevens, S., Lee, T.M., Coenye, T., De Vos, P., Mergeay, M., and Vandamme, P. 2001. Ralstonia taiwanensis sp. nov., isolated from root nodules of Mimosa species and sputum of a cystic fibrosis patient. Int. J. Syst. Evol. Microbiol. 51(Pt 5): 1729-1735.
5. Chen, W.M., James, E.K., Prescott, A.R., Kierans, M., and Sprent, J.I. 2003. Nodulation of Mimosa spp. by the b-proteobacterium Ralstonia taiwanensis. Mol. Plant-Microbe Interact. 16(12): 1051-1061. doi:10.1094/MPMI.2003.16.12.1051.
6. Cheng, G.J., Li, Y.G., and Zhou, J.C. 2006. Cloning and identification of opa22, a new gene involved in nodule formation by Mesorhizobium huakuii. FEMS Microbiol. Lett. 257(1): 152-157. doi:10.1111/j.1574-6968.2006.00158.x.
7. de Lajudie, P., Laurent-Fulele, E., Willems, A., Torck, U., Coopman, R., Collins, M.D., et al. 1998. Allorhizobium undicola gen. nov., sp. nov., nitrogen-fixing bacteria that efficiently nodulate Neptunia natans in Senegal. Int. J. Syst. Bacteriol. 48(4): 1277-1290. doi:10.1099/00207713-48-4-1277.
8. Deya, A A M., Odelson, D.A., Hickey, R.F., and Tidje, J.M. 1995 Bacterial community fingerprinting of amplified 16S and 16S-23S ribosomal DNA gene sequences and restriction endonuclease analysis (ARDRA). In Molecular microbial ecology manual. Edited by D.L. Akkermans, J.D. van Elsas, and F.J. de Bruijn. Kluwer, Dordrecht, Netherlands. pp. 1-8.
9. Dreyfus, B., Garcia, J.L., and Gillis, M. 1988. Characterization of Azorhizobium caulinodans gen. nov., sp. nov., a stem-nodulating nitrogen-fixing bacterium isolated from Sesbania rostrata. Int. J. Syst. Bacteriol. 38(1): 89-98. doi:10.1099/00207713-38-1-89.
10. Felsenstein, J. (Editor). 2004. Inferring phylogenies. Sinauer Associates Inc., Sunderland, Mass., USA.
11. Frank, B. 1889. Uber die pilzsymbiose der leguminosen. Ber. Dtsch. Bot. Ges. 7: 332-346.
12. Gaunt, M.W., Turner, S.L., Rigottier-Gois, L., Lloyd-Macgilp, S.A., and Young, J.P. 2001. Phylogenies of atpD and recA support the small subunit rRNA-based classification of rhizobia. Int. J. Syst. Evol. Microbiol. 51(Pt 6): 2037-2048.
13. Gevers, D., Cohan, F.M., Lawrence, J.G., Spratt, B.G., Coenye, T., Feil, E.J., et al. 2005. Opinion: re-evaluating prokaryotic species. Nat. Rev. Microbiol. 3(9): 733-739. doi:10.1038/nrmicro1236.
14. Jarvis, B.D.W., Van Berkum, P., Chen, W.X., Nour, S.M., Fernandez, M.P., Cleyet-Marel, J.C., and Gillis, M. 1997. Transfer of Rhizobium loti, Rhizobium huakuii, Rhizobium ciceri, Rhizobium mediterraneum, and Rhizobium tianshanense to Mesorhizobium gen. nov. Int. J. Syst. Bacteriol. 47(3): 895-898. doi:10.1099/00207713-47-3-895.
15. Jordan, D.C. 1982. Transfer of Rhizobium japonicum Buchanan 1980 to Bradyrhizobium gen. nov., a genus of slow growing, root nodule bacteria from leguminous plants. Int. J. Syst. Bacteriol. 32(1): 136-139. doi:10.1099/00207713-32-1-136.
16. Jourand, P., Giraud, E., Bena, G., Sy, A., Willems, A., Gillis, M., et al. 2004. Methylobacterium nodulans sp. nov., for a group of aerobic, facultatively methylotrophic, legume root-nodule-forming and nitrogen-fixing bacteria. Int. J. Syst. Evol. Microbiol. 54(6): 2269-2273. doi:10.1099/ijs.0.02902-0.
17. Kimura, M. 1980. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J. Mol. Evol. 16(2): 111-120. doi:10.1007/BF01731581.
18. Kumar, S., Tamura, K., and Nei, M. 2004. MEGA3: Integrated software for Molecular Evolutionary Genetics Analysis and sequence alignment. Brief. Bioinform. 5(2): 150-163. doi:10.1093/bib/5.2.150.0895.
19. Kuykendall, L.D., Saxena, B., Devine, E.E., and Udell, S.E. 1992. Genetic diversity in Bradyrhizobium japonicum Jordan 1982, and a proposal for Bradyrhizobium elkanii sp. nov. Can. J. Microbiol. 38(6): 501-505. doi:10.1139/m92-082.
20. Man, C.X., Wang, H., Chen, W.F., Sui, X.H., Wang, E.T., and Chen, W.X. 2008. Diverse rhizobia associated with soybean grown in the subtropical and tropical regions of China. Plant Soil, 310(1-2): 77-87. doi:10.1007/s11104-008-9631-3.
21. Moulin, L., Munive, A., Dreyfus, B., and Boivin-Masson, C. 2001. Nodulation of legumes by members of the b-subclass of Proteobacteria. Nature, 411(6840): 948-950. doi:10.1038/35082070.
22. Nichols, R. 2001. Gene trees and species trees are not the same. Trends Ecol. Evol. 16(7): 358-364. doi:10.1016/S0169-5347(01)02203-0.
23. Pueppke, S.G., and Broughton, W.J. 1999. Rhizobium sp. Strain NGR234 and R. fredii USDA257 share exceptionally broad, nested host ranges. Mol. Plant-Microbe Interact. 12(4): 293-318. doi:10.1094/MPMI.1999.12.4.293.
24. Ribeiro, R.A., Barcellos, F.G., Thompson, F.L., and Hungria, M. 2009. Multilocus sequence analysis of Brazilian Rhizobium microsymbionts of common bean (Phaseolus vulgaris L.) reveals unexpected taxonomic diversity. Res. Microbiol. 160(4): 297-306. doi:10.1016/j.resmic.2009.03.009.
25. Rivas, R., Willems, A., Subba-Rao, N.S., Mateos, P.F., Dazzo, F.B., Kroppenstedt, R.M., et al. 2003. Description of Devosia neptuniae sp. nov. that nodulates and fixes nitrogen in symbiosis with Neptunia natans, an aquatic legume from India. Syst. Appl. Microbiol. 26(1): 47-53. doi:10.1078/072320203322337308.
26. Rivas, R., Willems, A., Palomo, J.L., Garcia-Benavides, P., Mateos, P.F., Martinez-Molina, E., et al. 2004. Bradyrhizobium betae sp. nov., isolated from roots of Beta vulgaris affected by tumour-like deformations. Int. J. Syst. Evol. Microbiol. 54(4): 1271-1275. doi:10.1099/ijs.0.02971-0.
27. Rodelas, B., Gonzalez-Lopez, J., Martinez-Toledo, M.V., Pozo, C., and Salmeron, V. 1999. Influence of Rhizobium/Azotobacter and Rhizobium/Azospirillum combined inoculation on mineral composition of faba bean (Vicia faba L.). Biol. Fertil. Soils, 29(2): 165-169. doi:10.1007/s003740050540.
28. Santillana, N., Ramirez-Bahena, M.H., Garcia-Fraile, P., Velazquez, E., and Zuniga, 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(3): 239-247. doi:10.1007/s00203-007-0313-y.
29. Sawada, H., Kuykendall, L.D., and Young, J.M. 2003. Changing concepts in the systematics of bacterial nitrogen-fixing legume symbionts. J. Gen. Appl. Microbiol. 49(3): 155-179. doi:10.2323/jgam.49.155.
30. Singh, B.B., Mohan Raj, D.R., Dashiell, K.E., and Jackai, L. (Editors). 1997. Advances in cowpea research. IITA-JIRCAS, Ibadan, Nigeria.
31. Stackebrandt, E., and Goebel, B.M. 1994. Taxonomic note: a place for DNA-DNA reassociation and 16S rRNA sequence analysis in the present species definition in bacteriology. Int. J. Syst. Bacteriol. 44(4): 846-849. doi:10.1099/00207713-44-4-846.
32. Sy, A., Giraud, E., Jourand, P., Garcia, N., Willems, A., de Lajudie, P., et al. 2001. Methylotrophic Methylobacterium bacteria nodulate and fix nitrogen in symbiosis with legumes. J. Bacteriol. 183(1): 214-220. doi:10.1128/JB.183.1.214-220.2001.
33. Turner, S.L., and Young, J.P. 2000. The glutamine synthetases of rhizobia: phylogenetics and evolutionary implications. Mol. Biol. Evol. 17(2): 309-319.
34. van Berkum, P., and Eardly, B.D. 2002. The aquatic budding bacterium Blastobacter denitrificans is a nitrogen-fixing symbiont of Aeschynomene indica. Appl. Environ. Microbiol. 68(3): 1132-1136. doi:10.1128/AEM.68.3.1132-1136.2002.
35. van Berkum, P., Terefework, Z., Paulin, L., Suomalainen, S., Lindstrom, K., and Eardly, B.D. 2003. Discordant phylogenies within the rrn loci of rhizobia. J. Bacteriol. 185(10): 2988-2998. doi:10.1128/JB.185.10.2988-2998.2003.
36. Vandamme, P., and Coenye, T. 2004. Taxonomy of the genus Cupriavidus: a tale of lost and found. Int. J. Syst. Evol. Microbiol. 54(6): 2285-2289. doi:10.1099/ijs.0.63247-0.
37. Vandamme, P., Goris, J., Chen, W.-M., de Vos, P., and Willems, A. 2002. Burkholderia tuberum sp. nov., and Burkholderia phymatum sp. nov., nodulate the roots of tropical legumes. Syst. Appl. Microbiol. 25(4): 507-512. doi:10.1078/07232020260517634.
38. Vincent, J.M. (Editor). 1970. A manual for the practical study of rootnodule bacteria. Blackwell Scientific Publications, Oxford, England. pp. 73-97.
39. Vinuesa, P., and Silva, C. 2004. Species delineation and biogeography of symbiotic bacteria associated with cultivated and wild legumes. In Biological resources and migration. Edited by D. Werner. Springer, Berlin. pp. 143-161.
40. Vinuesa, P., Leon-Barrios, M., Silva, C., Willems, A., Jarabo-Lorenzo, A., Perez-Galdona, R., et al. 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(2): 569-575. doi:10.1099/ijs.0.63292-0.
41. Vinuesa, P., Silva, C., Werner, D., and 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(1): 29-54. doi:10.1016/j.ympev.2004.08.020.
42. Wang, Y., and Zhang, Z. 2000. Comparative sequence analyses reveal frequent occurrence of short segments containing an abnormally high number of non-random base variations in bacterial rRNA genes. Microbiology, 146(Pt 11): 2845-2854.
43. Wang, Y., Zhang, Z., and Ramanan, N. 1997. The actinomycete Thermobispora bispora contains two distinct types of transcriptionally active 16S rRNA genes. J. Bacteriol. 179(10): 3270-3276.
44. Weisburg, W.G., Barns, S.M., Pelletier, D.A., and Lane, D.J. 1991. 16S ribosomal DNA amplification for phylogenetic study. J. Bacteriol. 173(2): 697-703.
45. Wernegreen, J.J., and Riley, M.A. 1999. Comparison of the evolutionary dynamics of symbiotic and housekeeping loci: a case for the genetic coherence of rhizobial lineages. Mol. Biol. Evol. 16(1): 98-113.
46. Willems, A., Coopman, R., and Gillis, M. 2001. Comparison of sequence analysis of 16S-23S rDNA spacer regions, AFLP analysis and DNA-DNA hybridizations in Bradyrhizobium. Int. J. Syst. Evol. Microbiol. 51(Pt 2): 623-632.
47. Wilson, K. 1989. Preparation of genomic DNA from bacteria. In Current protocols in molecular biology. Edited by F.M. Ausubel, R. Brent, R.E. Kingston, D.D. Moore, J.G. Seidman, J.A. Smith, and K. Srtruhl. Greene Publishing Associates/Wiley-Interscience, New York. pp. 2.4.1-2.4.5.
48. Wu, H.B., Guo, Z.T., and Peng, C.H. 2003. Distribution and storage of soil organic carbon in China. Global Biogeochem. Cycles, 17(2): 17.1-17.11. doi:10.1029/2001GB001844.
49. Xu, L.M., Ge, C., Cui, Z., Li, J., and Fan, H. 1995. Bradyrhizobium liaoningense sp. nov., isolated from the root nodules of soybeans. Int. J. Syst. Bacteriol. 45(4): 706-711. doi:10.1099/00207713-45-4-706.
50. Yang, J.K., Xie, F.L., Zou, J., Zhou, Q., and Zhou, J.C. 2005. Polyphasic characteristics of bradyrhizobia isolated from nodules of peanut (Arachis hypogaea) in China. Soil Biol. Biochem. 37(1): 141-153. doi:10.1016/j.soilbio.2004.06.016.
51. Yao, Z.Y., Kan, F.L., Wang, E.T., Wei, G.H., and 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(6): 2219-2230. doi:10.1099/ijs.0.01408-0.
52. Young, J.M. 2003. The genus name Ensifer Casida 1982 takes priority over Sinorhizobium Chen et al. 1988, and Sinorhizobium morelense Wang et al. 2002 is a later synonym of Ensifer adhaerens Casida 1982. Is the combination 'Sinorhizobium adhaerens' (Casida 1982) Willems et al. 2003 legitimate? Request for an opinion. Int. J. Syst. Evol. Microbiol. 53(6): 2107-2110. doi:10.1099/ijs.0.02665-0.
53. Young, J.M., Kuykendall, L.D., Martinez-Romero, E., Kerr, A., and 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(Pt 1): 89-103.
54. Young, J.M., Park, D.C., and Weir, B.S. 2004. Diversity of 16S rDNA sequences of Rhizobium spp. implications for species determinations. FEMS Microbiol. Lett. 238(1): 125-131.
55. Zhang, W.T., Yang, J.K., Yuan, T.Y., and Zhou, J.C. 2007. Genetic diversity and phylogeny of indigenous rhizobia from cowpea [Vigna unguiculata (L.) Walp.]. Biol. Fertil. Soils, 44(1): 201-210. doi:10.1007/s00374-007-0196-8.