1887

Abstract

The and genes were characterized in a collection of 83 rhizobial strains which represented 23 recognized species distributed in the genera , , and , as well as unclassified rhizobia from various host legumes. Conserved primers were designed from available nucleotide sequences and were able to amplify and fragments of about 930 bp and 780 bp, respectively, from most of the strains investigated. RFLP analysis of the PCR products resulted in a classification of these rhizobia which was in general well-correlated with their known host range and independent of their taxonomic status. The and fragments were sequenced for representative strains belonging to different genera and species, most of which originated from nodules. Phylogenetic trees were constructed and revealed close relationships among symbiotic genes of the symbionts, irrespective of their 16S-rDNA-based classification. The and phylogenies were generally similar, but cases of incongruence were detected, suggesting that genetic rearrangements have occurred in the course of evolution. The results support the view that lateral genetic transfer across rhizobial species and, in some instances, across and genera plays a role in diversification and in structuring the natural populations of rhizobia.

Loading

Article metrics loading...

/content/journal/micro/10.1099/00221287-147-4-981
2001-04-01
2019-09-23
Loading full text...

Full text loading...

/deliver/fulltext/micro/147/4/1470981a.html?itemId=/content/journal/micro/10.1099/00221287-147-4-981&mimeType=html&fmt=ahah

References

  1. Amarger, N., Bours, M., Revoy, F., Allard, M. R. & Laguerre, G. ( 1994; ). Rhizobium tropici nodulates field-grown Phaseolus vulgaris in France. Plant Soil 161, 147-156.[CrossRef]
    [Google Scholar]
  2. Amarger, N., Macheret, V. & Laguerre, G. ( 1997; ). Rhizobium gallicum sp. nov. and Rhizobium giardinii sp. nov. from Phaseolus vulgaris nodules. Int J Syst Bacteriol 47, 996-1006.[CrossRef]
    [Google Scholar]
  3. Bergersen, F. J., Turner, G. L., Amarger, N., Mariotti, N. & Mariotti, A. ( 1986; ). Strain of Rhizobium lupini determines natural abundance of 15N in root nodules of Lupinus spp. Soil Biol Biochem 18, 97-101.[CrossRef]
    [Google Scholar]
  4. van Berkum, P., Beyene, D. & Eardly, B. D. ( 1996; ). Phylogenetic relationships among Rhizobium species nodulating the common bean (Phaseolus vulgaris L.). Int J Syst Bacteriol 46, 240-244.[CrossRef]
    [Google Scholar]
  5. van Berkum, P., Beyene, D., Bao, G., Campbell, T. A. & Eardly, B. D. ( 1998; ). Rhizobium mongolense sp. nov. is one of three rhizobial genotypes identified which nodulate and form nitrogen-fixing symbioses with Medicago ruthenica [(L.) Ledebour]. Int J Syst Bacteriol 48, 13-22.[CrossRef]
    [Google Scholar]
  6. Chen, W., Wang, E., Wang, S., Li, Y., Chen, X. & Li, Y. ( 1995; ). Characteristics of Rhizobium tianshanense sp. nov., a moderately and slowly growing root nodule bacterium isolated from an arid saline environment in Xianjiang, People’s Republic of China. Int J Syst Bacteriol 45, 153-159.[CrossRef]
    [Google Scholar]
  7. Del Papa, M. F., Balagu , L. J., Castro Sowinski, S. & 9 other authors ( 1999; ). Isolation and characterization of alfalfa-nodulating rhizobia present in acidic soils of central Argentina and Uruguay. Appl Environ Microbiol 65, 1420–1427.
    [Google Scholar]
  8. Dessen, P., Fondrat, C., Valencien, C. & Mugnier, C. ( 1990; ). Bisance: a French service for access to biomolecular sequence databases. Comput Appl Biosci 6, 355-356.
    [Google Scholar]
  9. Dobert, R. C., Breil, B. T. & Triplett, E. W. ( 1994; ). DNA sequence of the common nodulation genes of Bradyrhizobium elkanii and their phylogenetic relationships to those of other nodulating bacteria. Mol Plant–Microbe Interact 7, 564-572.[CrossRef]
    [Google Scholar]
  10. Eardly, B. D., Young, J. P. W. & Selander, R. K. ( 1992; ). Phylogenetic position of Rhizobium sp. strain Or 191, a symbiont of both Medicago sativa and Phaseolus vulgaris, based on partial sequences of the 16S rRNA and nifH genes. Appl Environ Microbiol 58, 1809-1815.
    [Google Scholar]
  11. Felsenstein, J. ( 1989; ). phylip – phylogeny inference package (version 3.2). Cladistics 5, 164-166.
    [Google Scholar]
  12. Garcia-de los Santos, A., Brom, S. & Romero, D. ( 1996; ). Rhizobium plasmids in bacteria-legume interactions. World J Microbiol Biotechnol 12, 119-125.[CrossRef]
    [Google Scholar]
  13. Geniaux, E., Laguerre, G. & Amarger, N. ( 1993; ). Comparison of geographically distant populations of Rhizobium isolated from root nodules of Phaseolus vulgaris. Mol Ecol 2, 295-302.[CrossRef]
    [Google Scholar]
  14. Graham, P. H. ( 1976; ). Identification and classification of root nodule bacteria. In Symbiotic Nitrogen Fixation in Plants , pp. 99-112. Edited by P. S. Nutman. International Biological Programme No. 7. London: Cambridge University Press.
  15. Graham, P. H., Sadowsky, M. J., Keyser, H. H. & 8 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]
  16. Haukka, K., Lindström, K. & Young, J. P. W. ( 1998; ). Three phylogenetic groups of nodA and nifH genes in Sinorhizobium and Mesorhizobium isolated from leguminous trees growing in Africa and Latin America. Appl Environ Microbiol 64, 419-426.
    [Google Scholar]
  17. Hennecke, H., Kaluza, K., Thöny, B., Fuhrmann, M., Ludwig, W. & Stackebrandt, E. ( 1985; ). Concurrent evolution of nitrogenase genes and 16S rRNA in Rhizobium species and other nitrogen fixing bacteria. Arch Microbiol 142, 342-348.[CrossRef]
    [Google Scholar]
  18. Herrera-Cervera, J. A., Caballero-Medallo, J., Laguerre, G., Tichy, H. V., Requena, N., Amarger, N., Martinez-Romero, E., Olivares, J. & Sanjuan, J. ( 1999; ). At least five rhizobial species nodulate Phaseolus vulgaris in a Spanish soil. FEMS Microbiol Ecol 30, 87-97.[CrossRef]
    [Google Scholar]
  19. 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]
  20. 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]
  21. Lagacherie, B., Hugot, R. & Amarger, N. ( 1977; ). Sélection de souches de Rhizobium japonicum d’après leur compétitivité pour l’infection. Ann Agron 28, 379-389.
    [Google Scholar]
  22. Lagacherie, B., Bours, M., Giraud, J. J. & Sommer, G. ( 1983; ). Interactions entre différentes souches de Rhizobium lupini et les espèces ou cultivars de lupin (Lupinus albus, Lupinus luteus et Lupinus mutabilis). Agronomie 3, 809-816.[CrossRef]
    [Google Scholar]
  23. Laguerre, G., Allard, M. R., Revoy, F. & Amarger, N. ( 1994; ). Rapid identification of rhizobia by restriction fragment length polymorphism analysis of PCR-amplified 16S rRNA genes. Appl Environ Microbiol 60, 56-63.
    [Google Scholar]
  24. 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]
  25. Laguerre, G., van Berkum, P., Amarger, N. & Prévost, D. ( 1997; ). Genetic diversity of rhizobial symbionts isolated from legume species within the genera Astragalus, Oxytropis and Onobrychis. Appl Environ Microbiol 63, 4748-4758.
    [Google Scholar]
  26. de Lajudie, P., Willems, A., Pot, B. & 7 other authors ( 1994; ). Polyphasic taxonomy of rhizobia: emendation of the genus Sinorhizobium, and description of Sinorhizobium meliloti comb. nov., Sinorhizobium saheli sp. nov., and Sinorhizobium teranga sp. nov. Int J Syst Bacteriol 44, 715–733.[CrossRef]
    [Google Scholar]
  27. de Lajudie, P., Laurent-Fulele, E., Willems, A., Torck, U., Coopman, R., Collins, M. D., Kersters, K., Dreyfus, B. & Gillis, M. ( 1998a; ). Allorhizobium undicola gen. nov., sp. nov., nitrogen-fixing bacteria that efficiently nodulate Neptunia natans in Senegal. Int J Syst Bacteriol 48, 1277-1290.[CrossRef]
    [Google Scholar]
  28. de Lajudie, P., Willems, A., Nick, G. & 9 other authors ( 1998; b). Characterization of tropical tree rhizobia and description of Mesorhizobium plurifarium sp. nov. Int J Syst Bacteriol 48, 369–382.[CrossRef]
    [Google Scholar]
  29. Lindström, K. ( 1989; ). Rhizobium galegae, a new species of legume root nodule bacteria. Int J Syst Bacteriol 39, 365-367.[CrossRef]
    [Google Scholar]
  30. Lindström, K., Paulin, L., Roos, C. & Suominen, L. ( 1995; ). Nodulation genes of Rhizobium galegae. In Nitrogen Fixation: Fundamentals and Applications. Proceedings of the 10th International Congress on Nitrogen Fixation , pp. 365-370. Edited by I. A. Tikhonovitch, N. A. Provorov, V. I. Romanov & W. E. Nexton. Dordrecht: Kluwer.
  31. Lortet, G., Méar, N., Lorquin, J., Dreyfus, B., de Lajudie, P., Rosenberg, C. & Boivin, C. ( 1996; ). Nod factor thin-layer chromatography profiling as a tool to characterize symbiotic specificity of rhizobial strains: application to Sinorhizobium saheli, S. teranga, and Rhizobium sp. strains isolated from Acacia and Sesbania. Mol Plant–Microbe Interact 9, 736-747.[CrossRef]
    [Google Scholar]
  32. Martinez, E., Pardo, M. A., Palacios, R. & Cevallos, M. A. ( 1985; ). Reiteration of nitrogen fixation gene sequences and specificity to Rhizobium in nodulation and nitrogen fixation in Phaseolus vulgaris. J Gen Microbiol 131, 1779-1786.
    [Google Scholar]
  33. Martinez-Romero, E. & Caballero-Mellado, J. ( 1996; ). Rhizobium phylogenies and bacterial genetic diversity. Crit Rev Plant Sci 15, 113-140.[CrossRef]
    [Google Scholar]
  34. Martinez-Romero, E., Segovia, L., Mercante, F. M., Franco, A. A., Graham, P. & Pardo, M. A. ( 1991; ). Rhizobium tropici, a novel species nodulating Phaseolus vulgaris L. beans and Leucaena sp. trees. Int J Syst Bacteriol 41, 417-426.[CrossRef]
    [Google Scholar]
  35. Michiels, J., Dombrecht, B., Vermeiren, N., Xi, C., Luyten, E. & Venderleyden, J. ( 1998; ). Phaseolus vulgaris is a non-selective host for nodulation. FEMS Microbiol Ecol 26, 193-205.[CrossRef]
    [Google Scholar]
  36. Moulin, L., Debellé, F., Giraud, E., Mangin, B., Dénarié, J. & Boivin-Masson, C. ( 2000; ). The nodA sequence of rhizobia gives clues on structural features of Nod factors. In Nitrogen Fixation: From Molecules to Crop Productivity , pp. 204. Edited by F. O. Pedrosa, M. Hungria, M. G. Yates & W. E. Newton. Dordrecht: Kluwer.
  37. Perret, X., Staehelin, C. & Broughton, W. J. ( 2000; ). Molecular basis of symbiotic promiscuity. Microbiol Mol Biol Rev 64, 180-201.[CrossRef]
    [Google Scholar]
  38. Poupot, R., Martinez-Romero, E. & Promé, J. C. ( 1993; ). Nodulation factors from Rhizobium tropici are sulfated or non-sulfated chitopentasaccharides containing an N-methyl-N-acylglucosamine terminus. Biochemistry 32, 10430-10435.[CrossRef]
    [Google Scholar]
  39. Poupot, R., Martinez-Romero, E., Gautier, N. & Promé, J. C. ( 1995; ). Wild type Rhizobium etli, a bean symbiont, produces acetyl-fucosylated, N-methylated, and carbamoylated nodulation factors. J Biol Chem 270, 6050-6055.[CrossRef]
    [Google Scholar]
  40. Prévost, D., Macheret, V. & Laguerre, G. ( 2000; ). Phylogenetic comparisons of symbiotic (nodC and nifH) and 16S rDNA genes in strains of Rhizobium, Mesorhizobium and Bradyrhizobium isolated from Astragalus, Oxytropis and Onobrychis spp. In Nitrogen Fixation: From Molecules to Crop Productivity , pp. 205. Edited by F. O. Pedrosa, M. Hungria, M. G. Yates & W. E. Newton. Dordrecht: Kluwer.
  41. Pueppke, S. G. & Broughton, W. J. ( 1999; ). Rhizobium sp. strain NGR234 and R. fredii USDA257 share exceptionally broad, nested host ranges. Mol Plant–Microbe Interact 12, 293-318.[CrossRef]
    [Google Scholar]
  42. Romero, D., Davila, G. & Palacios, R. ( 1998; ). The dynamic genome of Rhizobium. In Bacterial Genomes: Physical Structure and Analysis , pp. 153-161. Edited by F. J. de Bruijn, J. R. Lupski & G. M. Weinstock. New York: Chapman & Hall, International Thompson Publishing.
  43. Segovia, L., Young, J. P. W. & Martinez-Romero, E. ( 1993; ). Reclassification of American Rhizobium leguminosarum biovar phaseoli type I strains as Rhizobium etli sp. nov. Int J Syst Bacteriol 43, 374-377.[CrossRef]
    [Google Scholar]
  44. Sessitsch, A., Ramirez-Saad, H., Hardarson, G., Akkermans, A. D. I. & de Vos, W. M. ( 1997; ). Classification of Austrian rhizobia and the Mexican isolate FL27 obtained from Phasolus vulgaris L. as Rhizobium gallicum. Int J Syst Bacteriol 47, 1097-1101.[CrossRef]
    [Google Scholar]
  45. Sullivan, J. T. & Ronson, C. W. ( 1998; ). Evolution of rhizobia by acquisition of a 500-kb symbiosis island that integrates into a phe-tRNA gene. Proc Natl Acad Sci USA 95, 5145-5149.[CrossRef]
    [Google Scholar]
  46. Sullivan, J. T., Patrick, H. N., Lowther, W. L., Scott, D. B. & Ronson, C. W. ( 1995; ). Nodulating strains of Rhizobium loti arise through chromosomal symbiotic gene transfer in the environment. Proc Natl Acad Sci USA 92, 8985-8989.[CrossRef]
    [Google Scholar]
  47. Sullivan, J. T., Eardly, B. D., van Berkum, P. & Ronson, C. W. ( 1996; ). Four unnamed species of nonsymbiotic rhizobia isolated from the rhizosphere of Lotus corniculatus. Appl Environ Microbiol 62, 2818-2825.
    [Google Scholar]
  48. Thompson, J. D., Higgins, C. W. & Gibson, T. J. ( 1994; ). clustal w: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position specific gap penalties and weight matrix choice. Nucleic Acids Res 22, 4673-4680.[CrossRef]
    [Google Scholar]
  49. Turner, S. L. & Young, J. P. W. ( 2000; ). The glutamine synthetases of rhizobia: phylogenetics and evolutionary implications. Mol Biol Evol 17, 309-319.[CrossRef]
    [Google Scholar]
  50. Ueda, T., Suga, Y., Yahiro, N. & Matsuguchi, T. ( 1995; ). Phylogeny of Sym plasmids of rhizobia by PCR-based sequencing of a nodC segment. J Bacteriol 177, 468-472.
    [Google Scholar]
  51. Wang, E. T., van Berkum, P., Beyene, D., Sui, X. H., Dorado, O., Chen, W. X. & Martinez-Romero, E. ( 1998; ). Rhizobium huautlense sp. nov., a symbiont of Sesbania herbacea that has a close phylogenetic relationship with Rhizobium galegae. Int J Syst Bacteriol 48, 687-699.[CrossRef]
    [Google Scholar]
  52. Wang, E. T., Rogel, A., Garcia-de los Santos, A., Martinez-Romero, J., Cevallos, M. A. & Martinez-Romero, E. ( 1999a; ). Rhizobium etli bv. mimosae, a novel biovar isolated from Mimosa affinis. Int J Syst Bacteriol 49, 1479-1491.[CrossRef]
    [Google Scholar]
  53. Wang, E. T., van Berkum, P., Sui, X. H., Beyene, D., Chen, W. X. & Martinez-Romero, E. ( 1999b; ). Diversity of rhizobia associated with Amorpha fruticosa isolated from Chinese soils and description of Mesorhizobium amorphae sp. nov. Int J Syst Bacteriol 49, 51-65.[CrossRef]
    [Google Scholar]
  54. Wernegreen, J. J. & 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, 98-113.[CrossRef]
    [Google Scholar]
  55. Xu, L. M., Ge, C., Cui, Z. & Fan, H. ( 1995; ). Bradyrhizobium liaoningense sp. nov. isolated from the root nodules of soybeans. Int J Syst Bacteriol 45, 706-711.[CrossRef]
    [Google Scholar]
  56. Yang, G. P., Debell , F., Savagnac, A. & 9 other authors ( 1999; ). Structure of the Mesorhizobium huakuii and Rhizobium galegae Nod factors: a cluster of phylogenetically related legumes are nodulated by rhizobia producing Nod factors with α,β-unsaturated N-acyl substitutions. Mol Microbiol 31, 227–237.
    [Google Scholar]
  57. Young, J. P. W. ( 1985; ). Rhizobium population genetics: enzyme polymorphism in isolates from peas, clover, beans and lucerne grown at the same site. J Gen Microbiol 131, 2399-2408.
    [Google Scholar]
  58. Young, J. P. W. ( 1992; ). Phylogenetic classification of nitrogen-fixing organisms. In Biological Nitrogen Fixation , pp. 43-86. Edited by G. Stacey, R. H. Burris & H. J. Evans. New York: Chapman & Hall.
  59. Young, J. P. W. & Haukka, K. E. ( 1996; ). Diversity and phylogeny of rhizobia. New Phytol 133, 87-94.[CrossRef]
    [Google Scholar]
  60. Zhang, X. X., Turner, S. L., Guo, X. W., Yang, H. J., Debellé, F., Yang, G. P., Dénarié, J., Young, J. P. W. & Li, F. D. ( 2000; ). The common nodulation genes of Astragalus sinicus rhizobia are conserved despite chromosomal diversity. Appl Environ Microbiol 66, 2988-2995.[CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/00221287-147-4-981
Loading
/content/journal/micro/10.1099/00221287-147-4-981
Loading

Data & Media loading...

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