Multilocus sequence analysis of Brazilian Rhizobium microsymbionts of common bean (Phaseolus vulgaris L.) reveals unexpected taxonomic diversity

Research in Microbiology

Volumn 160, Issue 4, 2009, Pages 297-306

  Ribeiro, Renan Augusto ^a,b   Barcellos, Fernando Gomes ^a,b   Thompson, Fabiano L ^c   Hungria, Mariangela ^a,b  

^a EMBRAPA CERRADOS   (Brazil)

^b STATE UNIVERSITY OF LONDRINA   (Brazil)

^c FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

Author keywords

16S rRNA; Biological nitrogen fixation; Multilocus sequence analysis; Phaseolus vulgaris; Phylogeny; Rhizobium tropici

Indexed keywords

BACTERIAL PROTEIN; PROTEIN DNAK; PROTEIN GLNII; PROTEIN GLTA; PROTEIN RPOA; RECA PROTEIN; RNA 16S; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL GENE; BACTERIAL STRAIN; BACTERIUM ISOLATE; GENE LOCUS; GENETIC VARIABILITY; NONHUMAN; NUCLEOTIDE SEQUENCE; PHASEOLUS VULGARIS; PHYLOGENY; PRIORITY JOURNAL; RHIZOBIUM; RHIZOBIUM TROPICI; SEQUENCE ANALYSIS; SEQUENCE HOMOLOGY; SYMBIONT; TAXONOMY;

BRAZIL; DNA, BACTERIAL; DNA-DIRECTED RNA POLYMERASES; EVOLUTION, MOLECULAR; GENETIC MARKERS; GENETIC VARIATION; HSP70 HEAT-SHOCK PROTEINS; PHASEOLUS; PHYLOGENY; REC A RECOMBINASES; RHIZOBIUM; RNA, RIBOSOMAL, 16S; SEQUENCE ANALYSIS, DNA; SPECIES SPECIFICITY; SYMBIOSIS;

PHASEOLUS VULGARIS; RHIZOBIUM; RHIZOBIUM TROPICI;

EID: 67349228448     PISSN: 09232508     EISSN: 17697123     Source Type: Journal    
DOI: 10.1016/j.resmic.2009.03.009     Document Type: Article

References (77)

1. Acosta-Durán C., and Martínez-Romero E. Diversity of rhizobia from nodules of the leguminous tree Gliricidia sepium, a natural host of Rhizobium tropici. Arch. Microbiol. 178 (2002) 161-164
2. Aguilar O.M., Lópes M.V., Riccillo P.M., González R.A., Pagano M., Grasso D.H., Pühler A., and Favelukes G. Prevalence of the Rhizobium-etli like allele in genes coding for 16S rRNA among the indigenous rhizobial populations found associated with wild beans from the Southern Andes in Argentina. Appl. Environ. Microbiol. 64 (1998) 3520-3524
3. Aguilar O.M., Riva O., and Peltzer E. Analysis of Rhizobium etli and its symbiosis with wild Phaseolus vulgaris supports coevolution in centers of host diversification. Proc. Natl. Acad. Sci. U.S.A. 101 (2004) 13548-13553
4. Amarger N., Bours M., Revoy F., Allard M.R., and Laguerre G. Rhizobium tropici nodulates field-grown Phaseolus vulgaris in France. Plant Soil 161 (1994) 147-156
5. Amarger N., Macheret V., and Laguerre G. Rhizobium gallicum sp. nov. and Rhizobium giardinii sp. nov., from Phaseolus vulgaris nodules. Int. J. Syst. Bacteriol. 47 (1997) 996-1006
6. Andrade D.S., Murphy P.J., and Giller K.E. The diversity of Phaseolus-nodulating rhizobial populations is altered by liming of acid soils planted with Phaseolus vulgaris L. in Brazil. Appl. Environ. Microbiol. 68 (2002) 4025-4034
7. Anyango B., Wilson K.J., Beynon J.L., and Giller K.E. Diversity of rhizobia nodulating Phaseolus vulgaris L. in two Kenyan soils with contrasting pHs. Appl. Environ. Microbiol. 61 (1995) 4016-4021
8. Bernal G., and Graham P.H. Diversity in the rhizobia associated with Phaseolus vulgaris L. in Ecuador, and comparisons with Mexican bean rhizobia. Can. J. Microbiol. 47 (2001) 526-534
9. Brom S., Martínez E., D'Avila G., and Palácios R. Narrow and broad-host-range symbiotic plasmids of Rhizobium spp. strains that nodulate Phaseolus vulgaris. Appl. Environ. Microbiol. 54 (1988) 1280-1283
10. Dagutat H., and Steyn P.L. Taxonomy and distribution of rhizobia indigenous to South African soils. In: Tikhnovich I.A., Provorov N.A., Romanov V.I., and Newton W.E. (Eds). Nitrogen Fixation: Fundamentals and Applications (1995), Kluwer, Boston 683-686
11. Debouck D.G. Primary diversification of Phaseolus in the Americas: three centers?. Plant Gen. Res. Newsl. 67 (1986) 2-8
12. Eardly B.D., Wang F.S., Whittam T.S., and Selander R.K. Species limits in Rhizobium populations that nodulate the common bean (Phaseolus vulgaris). Appl. Environ. Microbiol. 61 (1995) 507-512
13. Embrapa (Empresa Brasileira de Pesquisa Agropecuária). Agência de informação - Feijão (2006). http://www.agencia.cnptia.embrapa.br/Agencia4/AG01/Abertura.html
14. Ewing B., Hillier L., Wendl M.C., and Green P. Base-calling of automated sequencer traces using phred. I. Accuracy assessment. Genome Res. 8 (1998) 175-185
15. Felsenstein J. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39 (1985) 783-791
16. Fred E.B., Baldwin I.L., and McCoy E. Root Nodule Bacteria of Leguminous Plant (1932), University of Wisconsin Press, Madison
17. Freitas F.O. Evidências genético-arqueológicas sobre a origem do feijão comum no Brasil. Pesq. Agropec. Bras. 41 (2006) 1199-1203
18. Garrity G.M., and Holt J.G. The road map to the manual. In: Boone D.R., Castenholz R.W., and Garrity G.M. (Eds). Bergey's Manual of Systematic Bacteriology. second ed. vol. 1 (2001), Springer, New York 119-166
19. Gaunt M.W., Turner S.L., Rigottier-Gois L., Lloyd-Macgilp S.A., and Young J.P. Phylogenies of atpD and recA support the small subunit rRNA-based classification of rhizobia. Int. J. Syst. Evol. Microbiol. 51 (2001) 2037-2048
20. Gepts P., and Debouck D. Origin, domestication, and evolution of the common bean (Phaseolus vulgaris L.). In: van Schoonhoven A., and Voysest O. (Eds). Common Beans: Research for Crop Improvement (1991), CAB, Wallingford-UK, Cali-Colombia 7-53
21. Germano M.G., Menna P., Mostasso F.L., and Hungria M. RFLP analysis of the RNA operon of a Brazilian collection of bradyrhizobial strains from thirty-three legume species. Int. J. Syst. Evol. Microbiol. 56 (2006) 217-229
22. Gevers D., Cohan F.M., Lawrence J.G., Spratt B.G., Coenye T., Feil E.J., Stackebrandt E., de Peer Y.V., Vandamme P., Thompson F.L., and Swings J. Re-evaluating prokaryotic species. Nat. Rev. Microbiol. 3 (2005) 733-739
23. Giongo A., Passaglia L.M.P., Freire J.R.J., and Sá E.L.S. Genetic diversity and symbiotic efficiency of population of rhizobia of Phaseolus vulgaris L. in Brazil. Biol. Fertil. Soils 43 (2007) 593-598
24. Gordon D., Abajian C., and Green P. Consed: a graphical tool for sequence finishing. Genome Res. 8 (1998) 195-202
25. Grange L., and Hungria M. Genetic diversity of indigenous common bean (Phaseolus vulgaris) rhizobia in two Brazilian ecosystems. Soil Biol. Biochem. 36 (2004) 1389-1398
26. Grange L., Hungria M., Graham P.H., and Martínez-Romero E. New insights into the origins and evolution of rhizobia that nodulate common bean (Phaseolus vulgaris) in Brazil. Soil Biol. Biochem. 39 (2007) 867-876
27. Harris J.K., Kelley S.T., Spiegelman G.B., and Pace N.R. The genetic core of the universal ancestor. Genome Res. 13 (2003) 407-412
28. Hungria M., Andrade D.S., Chueire L.M.O., Probanza A., Guitierrez-Manero F.J., and Megías M. Isolation and characterization of new efficient and competitive bean (Phaseolus vulgaris L.) rhizobia from Brazil. Soil Biol. Biochem. 21 (2000) 1515-1528
29. Hungria M., Campo R.J., and Mendes I.C. Benefits of inoculation of common bean (Phaseolus vulgaris) crop with efficient and competitive Rhizobium tropici strains. Biol. Fertil. Soils 39 (2003) 88-93
30. Hungria M., Franco A.A., and Sprent J.I. New sources of high-temperature tolerant rhizobia for Phaseolus vulgaris L. Plant Soil 149 (1993) 103-109
31. Jordan D.C. Family III, Rhizobiaceae Conn 1938. In: Krieg N.R., and Holt J.G. (Eds). Bergey's Manual of Systematic Bacteriology vol. 1 (1984), Williams & Wilkens Co., Baltimore, USA 234-235
32. Kaplan L. Archeology and domestication in American Phaseolus (beans). Econ. Bot. 19 (1965) 358-368
33. Kaplan L. What is the origin of the common bean?. Econ. Bot. 35 (1980) 240-254
34. Kaschuk G., Hungria M., Andrade D.S., and Campo R.J. 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 (2006) 210-220
35. Kimura M. A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. J. Mol. Evol. 16 (1980) 111-120
36. Kumar S., Tamura K., and Nei M. MEGA3: integrated software for Molecular Evolutionary Genetics Analysis and sequence alignment. Brief. Bioinf. 5 (2004) 150-163
37. Lloret L., and Martinez-Romero E. Evolución y filogenia de Rhizobium. Rev. Latinoam. Microbiol. 47 (2005) 43-60
38. Martens M., Delaere M., Coopman R., de Vos P., Gillis M., and Willems A. Multilocus sequence analysis of Ensifer and related taxa. Int. J. Syst. Evol. Microbiol. 57 (2007) 489-503
39. Martínez E., Palácios R., and Sánchez F. Nitrogen-fixing nodules induced by Agrobacterium tumefaciens harboring Rhizobium phaseoli plasmids. J. Bacteriol. 169 (1987) 2828-2834
40. Martínez E., Pardo M.A., Palacios R., and Cevallos M.A. Reiteration of nitrogen fixation gene sequences and specificity of Rhizobium in nodulation and nitrogen fixation in Phaseolus vulgaris. J. Gen. Microbiol. 131 (1985) 1779-1786
41. Martínez-Romero E., Segovia L., Mercante F.M., Franco A.A., Graham P., and Pardo M.A. Rhizobium tropici, a novel species nodulating Phaseolus vulgaris L. beans and Leucaena sp. trees. Int. J. Syst. Bacteriol. 41 (1991) 417-426
42. Menna P., Hungria M., Barcellos F.G., Bangel E.V., Hess P.N., and Martínez-Romero E. Molecular phylogeny based on the 16S rRNA gene of elite rhizobial strains used in Brazilian commercial inoculants. Syst. Appl. Microbiol. 29 (2006) 315-332
43. Mercante F.M., Cunha C.O., Straliotto R., Ribeiro-Junior W.Q., Vanderleyden J., and Franco A.A. Leucaena leucocephala as a trap-host for Rhizobium tropici strains from the Brazilian "cerrado" region. Rev. Microbiol. 29 (1998) 49-58
44. Michiels J., Dombrecht B., Vermeiren N., Xi C., Luyten E., and Vanderleyden J. Phaseolus vulgaris is a non-selective host for nodulation. FEMS Microbiol. Ecol. 26 (1998) 193-205
45. Mostasso L., Mostasso F.L., Dias B.G., Vargas M.A.T., and Hungria M. Selection of bean (Phaseolus vulgaris L.) rhizobial strains for the Brazilian Cerrados. Field Crops Res. 73 (2002) 261-272
46. 2-fixation with Phaseolus vulgaris constitute a novel biovar (bv. mediterranense) of Sinorhizobium meliloti. Arch. Microbiol. 187 (2007) 79-85
47. 2 with common bean (Phaseolus vulgaris L.). Soil Biol. Biochem. 39 (2007) 1851-1864
48. Quinto C., Flores M., Leemans J., Cevallos M.A., Pardo M.A., Azpiroz R., Girard M.L., Calva E., and Palacios R. Nitrogenase reductase: a functional multigene family in Rhizobium phaseoli. Proc. Natl. Acad. Sci. U.S.A. 82 (1985) 1170-1174
49. Saitou N., and Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4 (1987) 406-425
50. Segovia L., Young J.P.W., and Martínez-Romero E. Reclassification of American Rhizobium leguminosarum biovar phaseoli type I strains as Rhizobium etli sp. nov. Int. J. Syst. Bacteriol. 43 (1993) 374-377
51. Silva C., Vinuesa P., Eguiarte L.E., Souza V., and Martínez-Romero E. Evolutionary genetics and biogeographic structure of Rhizobium gallicum sensu lato, a widely distributed bacterial symbiont of diverse legumes. Mol. Ecol. 14 (2005) 4033-4050
52. Sneath P.H.A., and Sokal R.R. Numerical Taxonomy (1973), W.H. Freeman & Co, San Francisco
53. Soares A.L.L., Ferreira P.A.A., Pereira J.P.A.R., Vale H.M.M., Lima A.S., Andrade M.J.B., and Moreira F.M.S. Eficiência agronômica de rizóbios selecionados e diversidade de populações nativas nodulíferas em Perdões (MG) II - Feijoeiro. Rev. Bras. Ciênc. Solo 30 (2006) 803-811
54. Stackebrandt E., Frederiksen W., Garrity G.M., Grimont P.A.D., Kampfer P., Maiden X., Nesme M.C.J., Rossello-Mora R., Swings J., Truper H.G., Vauterin L., Ward A.C., and Whitman W.B. Report of the ad hoc committee for the re-evaluation of the species definition in bacteriology. Int. J. Syst. Evol. Microbiol. 52 (2002) 1043-1047
55. Stepkowski T., Czaplinska M., Miedzinska K., and Moulin L. The variable part of the dnaK gene as an alternative marker for phylogenetic studies of rhizobia and related alpha Proteobacteria. Syst. Appl. Microbiol. 26 (2003) 483-494
56. Stepkowski T., Moulin L., Krzyžańska A., McInnes A., Law I.J., and Howieson J. European origin of Bradyrhizobium populations infecting lupins and serradella in soils of western Australia and south Africa. Appl. Environ. Microbiol. 71 (2005) 7041-7052
57. Stocco P., Santos J.C.P., Vargas V.P., and Hungria M. Avaliação da biodiversidade de rizóbios simbiontes do feijoeiro (Phaseolus vulgaris L.) em Santa Catarina. Rev. Bras. Cienc. Solo 31 (2008) 1-9
58. Straliotto R., Cunha C.O., Mercante F.M., Franco A.A., and Rumjanek N.G. Diversity of rhizobia nodulating common beans (Phaseolus vulgaris L.) isolated from Brazilian tropical soils. An. Acad. Bras. Ciênc. 71 (1999) 3-11
59. Thompson F.L., Gevers D., Thompson C.C., Dawyndt P., Naser S., Hoste B., Munn C.B., and Swings J. Phylogeny and molecular identification of vibrios on the basis of multilocus sequence analysis. Appl. Environ. Microbiol. 71 (2005) 5107-5115
60. Thompson F.L., and Swings J. Taxonomy of vibrios. In: Thompson F.L., Austin B., and Swings J. (Eds). The Biology of Vibrios (2006), ASM Press, Washington, DC
61. Thompson J.D., Gibson T.J., Plewniak F., Jeanmougin F., and Higgins D.G. The CLUSTAL X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucl. Acids Res. 25 (1997) 4876-4882
62. van Berkum P., Terefework Z., Paulin L., Suomalainen S., Lindström K., and Eardly B.D. Discordant phylogenies within the rrn loci of rhizobia. J. Bacteriol. 185 (2003) 2988-2998
63. Vandamme P., Pot B., Gillis M., de Vos P., Kersters K., and Swings J. Polyphasic taxonomy, a consensus approach to bacterial systematics. Microbiol. Rev. 60 (1996) 407-438
64. Vincent J.M. Manual for the Practical Study of Root Nodule Bacteria (1970), Blackwell Scientific, Oxford, UK (IBP Handbook No. 15)
65. Vinuesa P., Leon-Barrios M., Silva C., Willems A., Jarabo-Lorenzo A., Perez-Galdona R., Werner D., and Martinez-Romero E. 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 (2005) 569-575
66. Weisburg W.G., Barns S.M., Pelletier D.A., and Lane D.J. 16S ribossomal DNA amplification for phylogenetic study. J. Bacteriol. 173 (1991) 697-703
67. Willems A. The taxonomy of rhizobia: an overview. Plant Soil 287 (2006) 3-14
68. Willems A., and Collins D. Phylogenetic analysis of rhizobia and agrobacteria based on 16S rRNA gene sequence. Int. J. Syst. Bacteriol. 43 (1993) 305-313
69. Willems A., Coopman R., and Gillis M. Comparison of sequence analysis of 16S-23S rDNA spacer regions, AFLP analysis and DNA-DNA hybridizations in Bradyrhizobium. Int. J. Syst. Evol. Microbiol. 51 (2001) 623-632
70. Woese C.R. Bacterial evolution. Microbiol. Rev. 51 (1987) 221-271
71. Woese C.R., and George E.F. Phylogenetic structure of the prokaryotic domain: the primary kingdoms. Proc. Natl. Acad. Sci. U.S.A. 74 (1977) 5088-5090
72. Woese C.R., Kandler O., and Wheelis M.L. Towards a natural system of organisms: proposal for the domains Archaea, Bacteria, and Eucarya. Proc. Natl. Acad. Sci. U.S.A. 87 (1990) 4576-4579
73. Young J.M. 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 (2003) 2107-2110
74. Young J.M., Kuykendall L.D., Martínez-Romero E., Kerr A., and Sawada H. A revision of Rhizobium Frank, 1889, with an emended description of the genus, and 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 (2001) 89-103
75. Young J.P.W. Molecular phylogeny of rhizobia and their relatives. In: Palacios R., Mora J., and Newton W.E. (Eds). New Horizons in Nitrogen Fixation (1993), Kluwer Academic Publishers, Dordrecht 587-592
76. Young J.P.W., Downer H.L., and Eardly B.D. Phylogeny of the phototrophic Rhizobium strain BTAi1 by polymerase chain reaction-based sequencing of a 16S rRNA gene segment. J. Bacteriol. 173 (1991) 2271-2277
77. Zeigler D.R. Gene sequences useful for predicting relatedness of whole genomes in bacteria. Int. J. Syst. Evol. Microbiol. 53 (2003) 1893-1900