Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Letter
  • Published:

Nodulation of legumes by members of the β-subclass of Proteobacteria

An Erratum to this article was published on 30 August 2001

Abstract

Members of the Leguminosae form the largest plant family on Earth, with around 18,000 species. The success of legumes can largely be attributed to their ability to form a nitrogen-fixing symbiosis with specific bacteria known as rhizobia, manifested by the development of nodules on the plant roots in which the bacteria fix atmospheric nitrogen, a major contributor to the global nitrogen cycle. Rhizobia described so far belong exclusively to the α-subclass of Proteobacteria, where they are distributed in four distinct phylogenetic branches1,2. Although nitrogen-fixing bacteria exist in other proteobacterial subclasses, for example Herbaspirillum and Azoarcus from the phylogenetically distant β-subclass, none has been found to harbour the nod genes essential for establishing rhizobial symbiosis3,4. Here we report the identification of proteobacteria from the β-subclass that nodulate legumes. This finding shows that the ability to establish a symbiosis with legumes is more widespread in bacteria than anticipated to date.

This is a preview of subscription content, access via your institution

Access options

Buy this article

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Unrooted 16S rDNA tree of Proteobacteria (purple bacteria).
Figure 2: Nodules of Macroptilium atropurpureum, three weeks after root inoculation with Burkholderia sp. strain STM678.
Figure 3: Unrooted NodA tree showing the close phylogenetic relationship between the NodA of strain STM678 and those of α-rhizobia.

Similar content being viewed by others

References

  1. Young, J. P. W. & Haukka, K. E. Diversity and phylogeny of rhizobia. New Phytol. 133, 87–94 (1996).

    Article  Google Scholar 

  2. Sy, A. et al. Methylotrophic Methylobacterium nodulate and fix nitrogen in symbiosis with legumes. J. Bacteriol. 183, 214–220 (2001).

    Article  CAS  Google Scholar 

  3. Lerouge, P. et al. Symbiotic host-specificity of Rhizobium meliloti is determined by a sulphated and acylated glucosamine oligosaccharide signal. Nature 344, 781–784 (1990).

    Article  ADS  CAS  Google Scholar 

  4. Spaink, H. P. et al. A novel highly unsaturated fatty acid moiety of lipo-oligosaccharide signals determines host specificity of Rhizobium. Nature 354, 125–130 (1991).

    Article  ADS  CAS  Google Scholar 

  5. van Berkum, P. & Eartly, B. D. in The Rhizobiaceae (eds Spaink, H. P., Kondorosi, A. & Hooykaas, P. J. J.) 1–24 (Kluwer Academic, Dordrecht, 1998).

    Book  Google Scholar 

  6. Deschodt, C. C. & Strijdom, B. W. Effective nodulation of Aspalathus linearis spp. linearis by rhizobia from other Aspalathus species. Phytophylactica 8, 103–104 (1976).

    Google Scholar 

  7. Dénarié, J., Debellé, F. & Promé, J. C. Rhizobium lipo-chitooligosaccharide nodulation factors: signaling molecules mediating recognition and morphogenesis. Annu. Rev. Biochem. 65, 503–535 (1996).

    Article  Google Scholar 

  8. Perret, X., Staehelin, C. & Broughton, W. J. Molecular basis of symbiotic promiscuity. Microbiol. Mol. Biol. Rev. 64, 180–201 (2000).

    Article  CAS  Google Scholar 

  9. Zhang, X. X. et al. The common nodulation genes of Astragalus sinicus rhizobia are conserved despite chromosomal diversity. Appl. Environ. Microbiol. 66, 2988–2995 (2000).

    Article  CAS  Google Scholar 

  10. Boone, C., Olsthoorn, M. M. A., Dakora, F. D., Spaink, H. P. & Thomas-Oates, J. Structural characterisation of lipo-chitin oligosaccharides isolated from Bradyrhizobium aspalati, microsymbionts of commercially important South African legumes. Carbohydr. Res. 317, 155–163 (1999).

    Article  CAS  Google Scholar 

  11. Polhill, R. M., Raven, P. H. & Stirton, C. H. in Advances in Legume Systematics Part 1 (eds Polhill, R. M. & Raven, P. H.) 1–26 (Royal Botanic Gardens, Kew, 1981).

    Google Scholar 

  12. Thompson, J. D., Gibson, T. J., Plewniak, F., Jeanmougin, F. & Higgins, D. G. The CLUSTALX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 25, 4876–4882 (1997).

    Article  CAS  Google Scholar 

  13. Swofford, D. L. PAUP. Phylogenetic Analysis Using Parsimony (and other Methods) Version 4 (Sinauer Associates, Sunderland, Massachusetts, 1998).

  14. Quandt, J. & Hynes, M. F. Versatile suicide vectors which allow direct selection for gene replacement in Gram-negative bacteria. Gene 127, 15–21 (1993).

    Article  CAS  Google Scholar 

  15. Kokotek, W. & Lotz, W. Construction of a lac-Z-kanamycin-resistance cassette, useful for site-directed mutagenesis and as a promoter probe. Gene 84, 467–471 (1989).

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank H. P. Spaink for providing strain STM678, M. Neyra for providing the 23S rRNA primers, Y. Prin for help in microscopy studies and C. Huttel for sending plant material. We also thank J. Cullimore and J. Batut for comments and suggestions.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Catherine Boivin-Masson.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Moulin, L., Munive, A., Dreyfus, B. et al. Nodulation of legumes by members of the β-subclass of Proteobacteria. Nature 411, 948–950 (2001). https://doi.org/10.1038/35082070

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/35082070

This article is cited by

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing