1887

Abstract

Symbiotic relationships between legumes and nitrogen-fixing soil micro-organisms are of ecological importance in plant communities worldwide. For example, nutrient-poor Australian soils are often dominated by shrubby legumes (e.g. species of ). However, relatively few studies have quantified patterns of diversity, host-specificity and effectiveness of these ecologically important plant–microbe interactions. In this study, 16S rRNA gene sequence and PCR-RFLP analyses were used to examine bacterial strains isolated from the root nodules of two widespread south-eastern Australian legumes, and , across nearly 60 sites. The results showed that there was extensive genetic diversity in microbial populations, including a broad range of novel genomic species. While previous studies have suggested that most native Australian legumes nodulate primarily with species of the genus , our results indicate significant associations with members of other root-nodule-forming bacterial genera, including , , , , and . Genetic analyses also revealed a diverse suite of non-nodulating bacterial endophytes, only a subset of which have been previously recorded. Although the ecological roles of these endosymbionts are not well understood, they may play both direct and indirect roles in promoting plant growth, nodulation and disease suppression.

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2011-02-01
2020-01-22
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References

  1. Andrews, J. H. & Harris, R. F. ( 2000; ). The ecology and biogeography of microorganisms on plant surfaces. Annu Rev Phytopathol 38, 145–180.[CrossRef]
    [Google Scholar]
  2. Bai, Y., Zhou, X. & Smith, D. ( 2003; ). Enhanced soybean plant growth due to coinoculation of Bacillus strains with Bradyrhizobium japonicum. Crop Sci 43, 1774–1781.[CrossRef]
    [Google Scholar]
  3. Barnet, Y. M. & Catt, P. C. ( 1991; ). Distribution and characteristics of root-nodule bacteria isolated from Australian Acacia spp. Plant Soil 135, 109–120.[CrossRef]
    [Google Scholar]
  4. Benhizia, Y., Benhizia, H., Benguedouar, A., Muresu, R., Giacomini, A. & Squartini, A. ( 2004; ). Gamma proteobacteria can nodulate legumes of the genus Hedysarum. Syst Appl Microbiol 27, 462–468.[CrossRef]
    [Google Scholar]
  5. Bernhardt, P. ( 1989; ). The floral biology of Australian Acacia. In Advances in Legume Biology, pp. 263–281. Edited by Stirton, C. H. & Zarucchi, J. L.. St Louis, MO. : Missouri Botanic Gardens.
    [Google Scholar]
  6. Brosius, J., Palmer, M. L., Kennedy, P. J. & Noller, H. F. ( 1978; ). Complete nucleotide sequence of a 16S ribosomal RNA gene from Escherichia coli. Proc Natl Acad Sci U S A 75, 4801–4805.[CrossRef]
    [Google Scholar]
  7. Chakravorty, S., Danica Helba, D., Burdayb, M. N. N. & Allanda, D. ( 2007; ). A detailed analysis of 16S ribosomal RNA gene segments for the diagnosis of pathogenic bacteria. J Microbiol Methods 69, 330–339.[CrossRef]
    [Google Scholar]
  8. Chen, W.-P. & Kuo, T. T. ( 1993; ). A simple and rapid method for the preparation of Gram-negative bacterial genomic DNA. Nucleic Acids Res 21, 2260.[CrossRef]
    [Google Scholar]
  9. Chen, W. M., Laevens, S., Lee, T. M., Coenye, T., de Vos, P., Mergeay, M. & 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, 1729–1735.[CrossRef]
    [Google Scholar]
  10. Cowan, R. S. ( 1996; ). Flora of Victoria. Melbourne. : Inkata Press.
    [Google Scholar]
  11. de Lajudie, P., Willems, A., Pot, B., Dewettinck, D., Maestrojuan, G., Neyra, M., Collins, M. D., Dreyfus, B., Kersters, K. & Gillis, M. ( 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]
  12. de Lajudie, P., Fulele-Laurent, E., Willems, A., Torck, U., Coopman, R., Collins, M. D., Kersters, K., Dreyfus, B. & Gillis, M. ( 1998; ). 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]
  13. Dreyfus, B., Garcia, J. L. & 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, 89–98.[CrossRef]
    [Google Scholar]
  14. Eck, R. V. & Dayhoff, M. O. ( 1966; ). Atlas of Protein Sequence and Structure. Silver Springs, MD. : National Biomedical Research Foundation.
    [Google Scholar]
  15. Farrand, S. K., van Berkum, P. B. & Oger, P. ( 2003; ). Agrobacterium is a definable genus of the family Rhizobiaceae. Int J Syst Evol Microbiol 53, 1681–1687.[CrossRef]
    [Google Scholar]
  16. Felsenstein, J. ( 1985; ). Confidence limits on phylogenies: An approach using the bootstrap. Evolution 39, 783–791.[CrossRef]
    [Google Scholar]
  17. Jackson, S. M. ( 2000; ). Habitat relationships of the mahogany glider, Petaurus gracilis, and the sugar glider, Petaurus breviceps. Wildl Res 27, 39–48.[CrossRef]
    [Google Scholar]
  18. Jenkins, M. B. ( 2003; ). Rhizobial and bradyrhizobial symbionts of mesquite from the Sonoran Desert: salt tolerance, facultative halophily and nitrate respiration. Soil Biol Biochem 35, 1675–1682.[CrossRef]
    [Google Scholar]
  19. Khanna, P. K. ( 1997; ). Comparison of growth and nutrition of young monocultures and mixed stands of Eucalyptus globulus and Acacia mearnsii. For Ecol Manage 94, 105–113.[CrossRef]
    [Google Scholar]
  20. Kwon, S.-W., Park, J.-Y., Kim, J.-S., Kang, J.-W., Cho, Y.-H., Lim, C.-K., Parker, M. A. & Lee, G.-B. ( 2005; ). Phylogenetic analysis of the genera Bradyrhizobium, Mesorhizobium, Rhizobium and Sinorhizobium on the basis of 16S rRNA gene and internally transcribed spacer region sequences. Int J Syst Evol Microbiol 55, 263–270.[CrossRef]
    [Google Scholar]
  21. Lafay, B. & Burdon, J. J. ( 1998; ). Molecular diversity of rhizobia occurring on native shrubby legumes in southeastern Australia. Appl Environ Microbiol 64, 3989–3997.
    [Google Scholar]
  22. Lafay, B. & Burdon, J. J. ( 2001; ). Small-subunit rDNA genotyping of rhizobia nodulating Australian Acacia spp. Appl Environ Microbiol 67, 396–402.[CrossRef]
    [Google Scholar]
  23. Li, J. H., Wang, E. T., Chen, W. F. & Chen, W. X. ( 2008; ). Genetic diversity and potential for promotion of plant growth detected in nodule endophytic bacteria of soybean grown in Heilongjiang province of China. Soil Biol Biochem 40, 238–246.[CrossRef]
    [Google Scholar]
  24. Marsudi, N. D. S., Glenn, A. R. & Dilworth, M. J. ( 1999; ). Identification and characterisation of fast- and slow-growing root nodule bacteria from South-Western Australian soils able to nodulate Acacia saligna. Soil Biol Biochem 31, 1229–1238.[CrossRef]
    [Google Scholar]
  25. Martens, M., Delaere, M., Coopman, R., De Vos, P., Gillis, M. & Willems, A. (( 2007; ). ). Multilocus sequence analysis of Ensifer and related taxa. Int J Syst Evol Microbiol 57, 489–503.[CrossRef]
    [Google Scholar]
  26. Martinez-Romero, E. & Caballero-Mellado, J. ( 1996; ). Rhizobium phylogenies and bacterial genetic diversity. Crit Rev Plant Sci 15, 113–140.[CrossRef]
    [Google Scholar]
  27. Maslin, B. R. ( 2001; ). Introduction to Acacia. In Flora of Australia, pp. 3–13. Edited by Orchard, A. E. & Wilson, A. J. G.. Melbourne. : CSIRO.
    [Google Scholar]
  28. Moulin, L., Muniv, A., Dreyfus, B. & Boivin-Masson, C. ( 2001; ). Nodulation of legumes by members of the β-subclass of proteobacteria. Nature 411, 948–950.[CrossRef]
    [Google Scholar]
  29. Muresu, R., Polone, E., Sulas, L. & other authors ( 2008; ). Coexistence of predominately nonculturable rhizobia with diverse, endophytic bacterial taxa within nodules of wild legumes. FEMS Microbiol Ecol 63, 383–400.[CrossRef]
    [Google Scholar]
  30. Nei, M. & Kumar, S. ( 2000; ). Molecular Evolution and Phylogenetics. New York. : Oxford University Press.
    [Google Scholar]
  31. Nour, S. M., Cleyet-Marel, J.-C., Beck, D., Effosse, A. & Fernandez, M. P. ( 1994; ). Genotypic and phenotypic diversity of Rhizobium isolated from chickpea (Cicer arietinum L.). Can J Microbiol 40, 345–354.[CrossRef]
    [Google Scholar]
  32. Polhill, R. M., Raven, P. H. & Stirton, C. H. ( 1981; ). Evolution and systematics of the Leguminosae. In Advances in Legume Systematics, pp. 1–26. Edited by Polhill, R. M. & Raven, P. H.. Kew. : Royal Botanic Gardens.
    [Google Scholar]
  33. Rivas, R., Velazquez, E., Willems, A., Vizcaino, N., Subba-Rao, N. S., Mateos, P. F., Gillis, M., Dazzo, F. B. & Martinez-Molina, E. ( 2002; ). A new species of Devosia that forms a unique nitrogen-fixing root-nodule symbiosis with the aquatic legume Neptunia natans (L.f.) Druce. Appl Environ Microbiol 68, 5217–5222.[CrossRef]
    [Google Scholar]
  34. Rzhetsky, A. & Nei, M. ( 1992; ). A simple method for estimating and testing minimum-evolution trees. Mol Biol Evol 9, 945–967.
    [Google Scholar]
  35. Saitou, N. & Nei, M. ( 1987; ). The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4, 406–425.
    [Google Scholar]
  36. Schmid, M. & Hartmann, A. ( 2003; ). Molecular phylogeny and ecology of root associated diazotrophic α- and β-proteobacteria. In Associative and Endophytic Nitrogen-fixing Bacteria and Cyanobacterial Associations, pp. 21–36. Edited by Elmerich, C. & Newton, W. E.. Dordrecht. : Kluwer Academic.
    [Google Scholar]
  37. Schmid, M., Baldani, J. I. & Hartmann, A. ( 2006; ). The genus Herbaspirillum. In The Prokaryotes: a Handbook on the Biology of Bacteria, 3rd edn, vol. 5, pp. 141–150. Edited by Dworkin, M., Falkow, S., Rosenberg, E., Schleifer, K. H. & Stackebrandt, E.. New York. : Springer.
    [Google Scholar]
  38. Schoenborn, L., Yates, P. S., Grinton, B. E., Hugenholtz, P. & Janssen, P. H. ( 2004; ). Liquid serial dilution is inferior to solid media for isolation of cultures representative of the phylum-level diversity of soil bacteria. Appl Environ Microbiol 70, 4363–4366.[CrossRef]
    [Google Scholar]
  39. Sharpe, D. J. & Goldingay, R. L. ( 1998; ). Feeding behaviour of the squirrel glider at Bungawalbin Nature Reserve, north-eastern New South Wales. Wildl Res 25, 243–254.[CrossRef]
    [Google Scholar]
  40. Sheu, S.-Y., Chen, W.-M. & Lin, G.-H. ( 2007; ). Characterization and application of a rolling-circle-type plasmid from Cupriavidus taiwanensis. Plasmid 57, 275–285.[CrossRef]
    [Google Scholar]
  41. Simms, E. L., Taylor, D. L., Povich, J., Shefferson, R. P., Sachs, J. L., Urbina, M. & Tausczik, Y. ( 2006; ). An empirical test of partner choice mechanisms in a wild legume-rhizobium interaction. Proc Biol Sci 273, 77–81.[CrossRef]
    [Google Scholar]
  42. Sprent, J. I. ( 2001; ). Nodulation in Legumes. Kew. : Royal Botanical Gardens.
    [Google Scholar]
  43. Stackebrandt, E., Frederiksen, W., Garrity, G. M., Grimont, P. A. D., Kämpfer, P., Maiden, M. C. J., Nesme, X., Rosselló-Mora, R., Swings, J. & other authors ( 2002; ). Report of the ad hoc committee for the re-evaluation of the species definition in bacteriology. Int J Syst Evol Microbiol 52, 1043–1047.[CrossRef]
    [Google Scholar]
  44. Sturz, A. V., Christie, B. R., Matheson, B. G. & Nowak, J. ( 1997; ). Biodiversity of endophytic bacteria which colonize red clover nodules, roots, stems and foliage and their influence on growth. Biol Fertil Soils 25, 13–19.[CrossRef]
    [Google Scholar]
  45. Tamura, K., Nei, M. & Kumar, S. ( 2004; ). Prospects for inferring very large phylogenies by using the neighbor-joining method. Proc Natl Acad Sci U S A 101, 11030–11035.[CrossRef]
    [Google Scholar]
  46. Tamura, K., Dudley, J., Nei, M. & Kumar, S. ( 2007; ). mega4: molecular evolutionary genetics analysis (mega) software version 4.0. Mol Biol Evol 24, 1596–1599.[CrossRef]
    [Google Scholar]
  47. Thrall, P. H., Millsom, D. A., Jeavons, A. C., Waayers, M., Harvey, G. R., Bagnall, D. J. & Brockwell, J. ( 2005; ). Seed inoculation with effective root-nodule bacteria enhances revegetation success. J Appl Ecol 42, 740–751.[CrossRef]
    [Google Scholar]
  48. Thrall, P. H., Slattery, J. F., Broadhurst, L. M., Young, A. G. & Bickford, S. ( 2007; ). Geographic patterns of symbiont abundance and adaptation in native Australian Acacia-rhizobia interactions. J Appl Ecol 95, 1110–1122.
    [Google Scholar]
  49. Thrall, P. H., Broadhurst, L. M., Hoque, M. S. & Bagnall, D. J. ( 2009; ). Diversity and salt tolerance of native Acacia rhizobia isolated from saline and non-saline soils. Austral Ecol 34, 950–963.[CrossRef]
    [Google Scholar]
  50. Thums, M., Klaassen, M. & Hume, I. D. ( 2005; ). Seasonal changes in the diet of the long-nosed bandicoot (Perameles nasuta) assessed by analysis of faecal scats and of stable isotopes in blood. Aust J Zool 53, 87–93.[CrossRef]
    [Google Scholar]
  51. Trujillo, M. E., Willems, A., Abril, A., Planchuelo, A.-M., Rivas, R., Ludeña, D., Mateos, P. F., Martínez-Molina, E. & Velázquez, E. ( 2005; ). Nodulation of Lupinus albus by strains of Ochrobactrum lupini sp. nov. Appl Environ Microbiol 71, 1318–1327.[CrossRef]
    [Google Scholar]
  52. Valverde, A., Velazquez, E., Gutierrez, C., Cervantes, E., Ventosa, A. & Igual, J. M. ( 2003; ). Herbaspirillum lusitanum sp. nov., a novel nitrogen-fixing bacterium associated with root nodules of Phaseolus vulgaris. Int J Syst Evol Microbiol 53, 1979–1983.[CrossRef]
    [Google Scholar]
  53. Valverde, A., Velazquez, E., Fernandez-Santos, F., Vizcaino, N., Rivas, R., Mateos, P. F., Martinez-Molina, E., Igual, J.-M. & Willems, A. ( 2005; ). Phyllobacterium trifolii sp. nov., nodulating Trifolium and Lupinus in Spanish soils. Int J Syst Evol Microbiol 55, 1985–1989.[CrossRef]
    [Google Scholar]
  54. Vandamme, P., Goris, J., Chen, W. M., de Vos, P. & Willems, A. ( 2002; ). Burkholderia tuberum sp. nov. and Burkholderia phymatum sp. nov. nodulate the roots of tropical legumes. Syst Appl Microbiol 25, 507–512.[CrossRef]
    [Google Scholar]
  55. Verma, S. C., Chowdhury, S. P. & Tripathi, A. K. ( 2004; ). Phylogeny based on 16S rDNA and nifH sequences of Ralstonia taiwanensis strains isolated from nitrogen-fixing nodules of Mimosa pudica, in India. Can J Microbiol 50, 313–322.[CrossRef]
    [Google Scholar]
  56. Vincent, J. ( 1970; ). A Manual for the Practical Study of the Root-nodule Bacteria. IBP Handbook No. 15. Oxford. : Blackwell.
    [Google Scholar]
  57. Weir, B. S., Turner, S. J., Silvester, W. B., Park, D.-C. & Young, J. M. ( 2004; ). Unexpectedly diverse Mesorhizobium strains and Rhizobium leguminosarum nodulate native legume genera of New Zealand, while introduced legume weeds are nodulated by Bradyrhizobium species. Appl Environ Microbiol 70, 5980–5987.[CrossRef]
    [Google Scholar]
  58. Willems, A. & Collins, M. D. ( 1993; ). Phylogenetic analysis of rhizobia and agrobacteria based on 16S rRNA gene sequences. Int J Syst Bacteriol 43, 305–313.[CrossRef]
    [Google Scholar]
  59. Young, J. M., Kuykendall, L. D., Martinez-Romero, E., Kerr, A. & 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, 89–103.
    [Google Scholar]
  60. Zakhia, F., Jeder, H., Willems, A., Gillis, M., Dreyfus, B. & de Lajudie, P. ( 2006; ). Diverse bacteria associated with root nodules of spontaneous legumes in Tunisia and first report for nifH-like gene within the genera Microbacterium and Starkeya. Microb Ecol 51, 375–393.[CrossRef]
    [Google Scholar]
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