1887

INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY logo

Volume 61, Issue 12

Phylogeny of nodulation and nitrogen-fixation genes in : supporting evidence for the theory of monophyletic origin, and spread and maintenance by both horizontal and vertical transfer Free

Abstract

Bacteria belonging to the genus are capable of establishing symbiotic relationships with a broad range of plants belonging to the three subfamilies of the family Leguminosae ( = Fabaceae), with the formation of specialized structures on the roots called nodules, where fixation of atmospheric nitrogen takes place. Symbiosis is under the control of finely tuned expression of common and host-specific nodulation genes and also of genes related to the assembly and activity of the nitrogenase, which, in strains investigated so far, are clustered in a symbiotic island. Information about the diversity of these genes is essential to improve our current poor understanding of their origin, spread and maintenance and, in this study, we provide information on 40 strains, mostly of tropical origin. For the nodulation trait, common (), -specific () and host-specific () nodulation genes were studied, whereas for fixation ability, the diversity of was investigated. In general, clustering of strains in all and trees was similar and the group could be clearly separated from other rhizobial genera. However, the congruence of and genes with ribosomal and housekeeping genes was low. and were not detected in three strains by amplification or hybridization with probes using and type strains, indicating the high diversity of these genes or that strains other than photosynthetic must have alternative mechanisms to initiate the process of nodulation. For a large group of strains, the high diversity of genes (with an emphasis on ), the low relationship between genes and the host legume, and some evidence of horizontal gene transfer might indicate strategies to increase host range. On the other hand, in a group of five symbionts of , the high congruence between and ribosomal/housekeeping genes, in addition to shorter sequences and the absence of , highlights a co-evolution process. Additionally, in a group of strains that were symbionts of soybean, vertical transfer seemed to represent the main genetic event. In conclusion, clustering of and gives additional support to the theory of monophyletic origin of the symbiotic genes in and, in addition to the analysis of and , indicates spread and maintenance of and genes through both vertical and horizontal transmission, apparently with the dominance of one or other of these events in some groups of strains.

  • Published Online:
Funding
This study was supported by the:
  • CNPq (Conselho Nacional de Desenvolvimento Científico e Tecnológico, Brazil
  • CNPq-PNPD (Award 558455/2008-5)
  • CNPq/MCT/MAPA (Award 577933/2008)
  • CPNq-Universal (Award 470162/2009)
  • CNPq-Repensa (Award 562008/2010-1)
© 2011 IUMS
Loading

Article metrics loading...

/content/journal/ijsem/10.1099/ijs.0.028803-0
2011-12-01
2024-04-19
Loading full text...

Full text loading...

/deliver/fulltext/ijsem/61/12/3052.html?itemId=/content/journal/ijsem/10.1099/ijs.0.028803-0&mimeType=html&fmt=ahah

References

  1. Angus A. A., Hirsch A. M. 2010; Insights into the history of the legume-betaproteobacterial symbiosis. Mol Ecol 19:28–30 [View Article][PubMed]
     [Google Scholar]
  2. Bala A., Murphy P., Giller K. E. 2003; Distribution and diversity of rhizobia nodulating agroforestry legumes in soils from three continents in the tropics. Mol Ecol 12:917–929 [View Article][PubMed]
     [Google Scholar]
  3. Barcellos F. G., Menna P., da Silva Batista J. S., Hungria M. 2007; Evidence of horizontal transfer of symbiotic genes from a Bradyrhizobium japonicum inoculant strain to indigenous diazotrophs Sinorhizobium (Ensifer) fredii and Bradyrhizobium elkanii in a Brazilian Savannah soil. Appl Environ Microbiol 73:2635–2643 [View Article][PubMed]
     [Google Scholar]
  4. 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 [View Article][PubMed]
     [Google Scholar]
  5. Broughton W. J., Jabbouri S., Perret X. 2000; Keys to symbiotic harmony. J Bacteriol 182:5641–5652 [View Article][PubMed]
     [Google Scholar]
  6. Dixon R., Kahn D. 2004; Genetic regulation of biological nitrogen fixation. Nat Rev Microbiol 2:621–631 [View Article][PubMed]
     [Google Scholar]
  7. Dobert R. C., Breil B. T., Triplett E. W. 1994; DNA sequence of the common nodulation genes of Bradyrhizobium elkanii and their phylogenetic relationship to those of other nodulating bacteria. Mol Plant Microbe Interact 7:564–572 [View Article][PubMed]
     [Google Scholar]
  8. 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[PubMed]
     [Google Scholar]
  9. Felsenstein J. 1985; Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791 [View Article]
     [Google Scholar]
  10. Freiberg C., Fellay R., Bairoch A., Broughton W. J., Rosenthal A., Perret X. 1997; Molecular basis of symbiosis between Rhizobium and legumes. Nature 387:394–401 [View Article][PubMed]
     [Google Scholar]
  11. Giraud E., Moulin L., Vallenet D., Barbe V., Cytryn E., Avarre J. C., Jaubert M., Simon D., Cartieaux F. et al. other authors 2007; Legumes symbioses: absence of Nod genes in photosynthetic bradyrhizobia. Science 316:1307–1312 [View Article][PubMed]
     [Google Scholar]
  12. Göttfert M., Röthlisberger S., Kündig C., Beck C., Marty R., Hennecke H. 2001; Potential symbiosis-specific genes uncovered by sequencing a 410-kilobase DNA region of the Bradyrhizobium japonicum chromosome. J Bacteriol 183:1405–1412 [View Article][PubMed]
     [Google Scholar]
  13. 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[PubMed]
     [Google Scholar]
  14. 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 [View Article]
     [Google Scholar]
  15. Kaluza K., Hahn M., Hennecke H. 1985; Repeated sequences similar to insertion elements clustered around the nif region of the Rhizobium japonicum genome. J Bacteriol 162:535–542[PubMed]
     [Google Scholar]
  16. Kaneko T., Nakamura Y., Sato S., Minamisawa K., Uchiumi T., Sasamoto S., Watanabe A., Idesawa K., Iriguchi M. et al. other authors 2002; Complete genomic sequence of nitrogen-fixing symbiotic bacterium Bradyrhizobium japonicum USDA110. DNA Res 9:189–197 [View Article][PubMed]
     [Google Scholar]
  17. 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 [View Article][PubMed]
     [Google Scholar]
  18. Koonin E. V., Makarova K. S., Aravind L. 2001; Horizontal gene transfer in prokaryotes: quantification and classification. Annu Rev Microbiol 55:709–742 [View Article][PubMed]
     [Google Scholar]
  19. 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]
  20. Lerouge P., Roche P., Faucher C., Maillet F., Truchet G., Promé J. C., Dénarié J. 1990; Symbiotic host-specificity of Rhizobium meliloti is determined by a sulphated and acylated glucosamine oligosaccharide signal. Nature 344:781–784 [View Article][PubMed]
     [Google Scholar]
  21. Lloret L., Martínez-Romero E. 2005; [Evolution and phylogeny of rhizobia]. Rev Latinoam Microbiol 47:43–60 (in Spanish) [PubMed]
     [Google Scholar]
  22. López-Lara I. M., Blok-Tip L., Quinto C., Garcia M. L., Stacey G., Bloemberg G. V., Lamers G. E., Lugtenberg B. J., Thomas-Oates J. E., Spaink H. P. 1996; NodZ of Bradyrhizobium extends the nodulation host range of Rhizobium by adding a fucosyl residue to nodulation signals. Mol Microbiol 21:397–408 [View Article][PubMed]
     [Google Scholar]
  23. Menna P., Hungria M., Barcellos F. G., Bangel E. V., Hess P. N., Martínez-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 [View Article][PubMed]
     [Google Scholar]
  24. Menna P., Barcellos F. G., Hungria M. 2009a; 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 59:2934–2950 [View Article][PubMed]
     [Google Scholar]
  25. Menna P., Pereira A. A., Bangel E. V., Hungria M. 2009b; rep-PCR of tropical rhizobia for strain fingerprinting, biodiversity appraisal and as a taxonomic and phylogenetic tool. Symbiosis 48:120–130 [View Article]
     [Google Scholar]
  26. Moulin L., Béna G., Boivin-Masson C., Stępkowski T. 2004; Phylogenetic analyses of symbiotic nodulation genes support vertical and lateral gene co-transfer within the Bradyrhizobium genus. Mol Phylogenet Evol 30:720–732 [View Article][PubMed]
     [Google Scholar]
  27. Mutch L. A., Tamimi S. M., Young J. P. W. 2003; Genotypic characterization of rhizobia nodulating Vicia faba from the soils of Jordan: a comparison with UK isolates. Soil Biol Biochem 35:709–714 [View Article]
     [Google Scholar]
  28. Nieuwkoop A. J., Banfalvi Z., Deshmane N., Gerhold D., Schell M. G., Sirotkin K. M., Stacey G. 1987; A locus encoding host range is linked to the common nodulation genes of Bradyrhizobium japonicum. . J Bacteriol 169:2631–2638[PubMed]
     [Google Scholar]
  29. Norris D. O. 1965; Acid production by Rhizobium: a unifying concept. Plant Soil 22:143–166 [View Article]
     [Google Scholar]
  30. Ochman H., Lawrence J. G., Groisman E. A. 2000; Lateral gene transfer and the nature of bacterial innovation. Nature 405:299–304 [View Article][PubMed]
     [Google Scholar]
  31. 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]
  32. Sambrook J., Russell D. W. 2001 Molecular Cloning: a Laboratory Manual, 3rd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press;
     [Google Scholar]
  33. Scott K. F. 1986; Conserved nodulation genes from the non-legume symbiont Bradyrhizobium sp. (Parasponia). Nucleic Acids Res 14:2905–2919 [View Article][PubMed]
     [Google Scholar]
  34. Sprent J. I. 2007; Evolving ideas of legume evolution and diversity: a taxonomic perspective on the occurrence of nodulation. New Phytol 174:11–25 [View Article][PubMed]
     [Google Scholar]
  35. Stacey G., Luka S., Sanjuan J., Banfalvi Z., Nieuwkoop A. J., Chun J. Y., Forsberg L. S., Carlson R. 1994; nodZ, a unique host-specific nodulation gene, is involved in the fucosylation of the lipooligosaccharide nodulation signal of Bradyrhizobium japonicum . J Bacteriol 176:620–633[PubMed]
     [Google Scholar]
  36. Steenkamp E. T., Stępkowski T., Przymusiak A., Botha W. J., Law I. J. 2008; Cowpea and peanut in southern Africa are nodulated by diverse Bradyrhizobium strains harboring nodulation genes that belong to the large pantropical clade common in Africa. Mol Phylogenet Evol 48:1131–1144 [View Article][PubMed]
     [Google Scholar]
  37. Stępkowski T., Świderska A., Miedzinska K., Czaplińska M., Świderski M., Biesiadka J., Legocki A. B. 2003; Low sequence similarity and gene content of symbiotic clusters of Bradyrhizobium sp. WM9 (Lupinus) indicate early divergence of “lupin” lineage in the genus Bradyrhizobium. . Antonie van Leeuwenhoek 84:115–124 [View Article][PubMed]
     [Google Scholar]
  38. Stępkowski T., Moulin L., Krzyzańska 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 [View Article][PubMed]
     [Google Scholar]
  39. Stępkowski T., Hughes C. E., Law I. J., Markiewicz L., Gurda D., Chlebicka A., Moulin L. 2007; Diversification of lupine Bradyrhizobium strains: evidence from nodulation gene trees. Appl Environ Microbiol 73:3254–3264 [View Article][PubMed]
     [Google Scholar]
  40. Sterner J. P., Parker M. A. 1999; Diversity and relationships of bradyrhizobia from Amphicarpaea bracteata based on partial nod and ribosomal sequences. Syst Appl Microbiol 22:387–392[PubMed] [CrossRef]
     [Google Scholar]
  41. Turner S. L., Young J. P. 2000; The glutamine synthetases of rhizobia: phylogenetics and evolutionary implications. Mol Biol Evol 17:309–319[PubMed] [CrossRef]
     [Google Scholar]
  42. Vinuesa P., Rojas-Jiménez K., Contreras-Moreira B., Mahna S. K., Prasad B. N., Moe H., Selvaraju S. B., Thierfelder H., Werner D. 2008; Multilocus sequence analysis for assessment of the biogeography and evolutionary genetics of four Bradyrhizobium species that nodulate soybean on the Asiatic continent. Appl Environ Microbiol 74:6987–6996 [CrossRef]
     [Google Scholar]
  43. You Z., Marutani M., Borthakur D. 2002; Diversity among Bradyrhizobium isolates nodulating yardlong bean and sunnhemp in Guam. J Appl Microbiol 93:577–584 [View Article][PubMed]
     [Google Scholar]
  44. Young J. P. W. 1992; Phylogenetic classification of nitrogen-fixing organisms. In Biological Nitrogen Fixation pp. 43–79 Edited by Stacey G., Burris H. R., Evans H. J. New York: Chapman and Hall;
     [Google Scholar]
  45. Young J. P. W., Haukka K. E. 1996; Diversity and phylogeny of rhizobia. New Phytol 133:87–94 [View Article]
     [Google Scholar]
  46. Zehr J. P., Wyman M., Miller V., Duguay L., Capone D. G. 1993; Modification of the Fe protein of nitrogenase in natural populations of Trichodesmium thiebautii . Appl Environ Microbiol 59:669–676[PubMed]
     [Google Scholar]
  47. Zhao C. T., Wang E. T., Chen W. F., Chen W. X. 2008; Diverse genomic species and evidences of symbiotic gene lateral transfer detected among the rhizobia associated with Astragalus species grown in the temperate regions of China. FEMS Microbiol Lett 286:263–273 [View Article][PubMed]
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/ijsem/10.1099/ijs.0.028803-0
Loading
Phylogeny of nodulation and nitrogen-fixation genes in Bradyrhizobium: supporting evidence for the theory of monophyletic origin, and spread and maintenance by both horizontal and vertical transfer
Int J Syst Evol Microbiol 61, 3052 (2011); https://doi.org/10.1099/ijs.0.028803-0
/content/journal/ijsem/10.1099/ijs.0.028803-0
/content/journal/ijsem/10.1099/ijs.0.028803-0
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF

Most cited Most Cited RSS feed

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