Skip to main content

Advertisement

SpringerLink
Log in

Genetic Diversity of Acacia seyal Del. Rhizobial Populations Indigenous to Senegalese Soils in Relation to Salinity and pH of the Sampling Sites

  • Published:
Microbial Ecology Aims and scope Submit manuscript

Abstract

The occurrence and the distribution of rhizobial populations naturally associated to Acacia seyal Del. were characterized in 42 soils from Senegal. The diversity of rhizobial genotypes, as characterized by polymerase chain reaction restriction fragment length polymorphism (RFLP) analysis of 16S–23S rDNA, performed on DNA extracted from 138 nodules resulted in 15 clusters. Results indicated the widespread occurrence of compatible rhizobia associated to A. seyal in various ecogeographic areas. However, the clustering of rhizobial populations based on intergenic spacer (IGS) RFLP profiles did not reflect their geographic origin. Four genera were discriminated on the basis of 16S rRNA gene sequences of the strains representative for the IGS-RFLP profiles. The majority of rhizobia associated to A. seyal were affiliated to Mesorhizobium and Sinorhizobium 64 and 29%, respectively, of the different IGS-RFLP profiles. Our results demonstrate the coexistence inside the nodule of plant-pathogenic non-N2-fixing Agrobacterium and Burkholderia strains, which induced the formation of ineffective nodules, with symbiotic rhizobia. Nodulation was recorded in saline soils and/or at low pH values or in alkaline soils, suggesting adaptability of natural rhizobial populations to major ecological environmental stress and their ability to establish symbiotic associations within these soil environments. These results contribute to the progressing research efforts to uncover the biodiversity of rhizobia and to improve nitrogen fixation in agroforestry systems in sub-Saharan Africa.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Figure 1
Figure 2
Figure 3
Figure 4

Similar content being viewed by others

References

  1. Allen, ON, Allen, EK (1981) The Leguminosae: A Source Book of Characteristics, Uses and Nodulation. The University of Wisconsin Press, Madison

    Google Scholar 

  2. Altschul, SF, Madden, TL, Schäffer, AA, Zhang, J, Zhang, Z, Miller, W, Lipman, DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25: 3389–3402

    Article  PubMed  CAS  Google Scholar 

  3. Ba, S, Willems, A, de Lajudie, P, Roche, P, Jeder, H, Quatrini, P, Neyra, M, Ferro, M, Prome, JC, Gillis, M, Boivin-Masson, C, Lorquin, J (2002) Symbiotic and taxonomic diversity of rhizobia isolated from Acacia tortilis subsp. raddiana in Africa. Syst Appl Microbiol 25: 130–145

    Article  PubMed  CAS  Google Scholar 

  4. Bala, A, Giller, KE (2001) Symbiotic specificity of tropical tree rhizobia for host legumes. New Phytol 149: 495–507

    Article  Google Scholar 

  5. Bordeleau, LM, Prévost, D (1994) Nodulation and nitrogen fixation in extreme environments. Plant Soil 161: 115–125

    Article  CAS  Google Scholar 

  6. Ben Romdhane, S, Nasr, H, Samba-Mbaye, R, Neyra, M, Ghorbal, MH (2005) Diversity of Acacia tortilis rhizobia revealed by PCR/RFLP on crushed root nodules in Tunisia. Ann Microbiol 55: 249–258

    CAS  Google Scholar 

  7. Ben Romdhane, S, Nasr, H, Samba-Mbaye, R, Neyra, M, Ghorbal, MH, de Lajudie, P (2006) Genetic diversity of Acacia tortilis ssp. raddiana rhizobia in Tunisia assessed by 16S and 16S–23S rDNA genes analysis. J Appl Microbiol 100: 436–445

    Article  PubMed  CAS  Google Scholar 

  8. Carter, JM, Gardner, WK, Gibson, AH (1994) Improved growth and yield of faba bean (Vicia faba cv. Fiord) by inoculation with strains of Rhizobium leguminosarum biovar viceae in acid soils in South-west Victoria. Aust J Agric Res 45: 613–623

    Article  Google Scholar 

  9. de Lajudie, P, Willems, A, Nick, G, Moreau, F, Molouba, F, Hoste, B, Torck, U, Neyra, M, Collins, MD, Lindstorm, K, Dreyfus, B, Gillis, M (1998) Characterization of tropical tree rhizobia and description of Mesorhizobium plurifarium sp. nov. Int J Syst Bacteriol 48: 369–382

    PubMed  Google Scholar 

  10. de Lajudie, P, Willems, A, Nick, G, Mohamed, SH, Torck, U, Coopman, R, Filali-Maltouf, A, Kersters, K, Dreyfus, B, Lindström, K, Gillis, M (1999) Agrobacterium bv.1 strains isolated from nodules of tropical legumes. Syst Appl Microbiol 22: 119–132

    Google Scholar 

  11. Diouf, D, Duponnois, R, Ba, AT, Neyra, M, Lesueur, D (2005) Symbiosis of Acacia auriculiformis and A. mangium with mycorrhizal fungi and Bradyrhizobium sp. improves salt tolerance in greenhouse conditions. Funct Plant Biol 32: 1143–1152

    Article  CAS  Google Scholar 

  12. Diouf, D, Forestier, S, Neyra, M, Lesueur, D (2003) Optimization of inoculation of Leucaena leucocephala and Acacia mangium with rhizobium under greenhouse conditions. Ann For Sci 60: 1–6

    Article  Google Scholar 

  13. Dolédec, S, Chessel, D (1987) Rythmes saisonniers et composantes stationnelles en milieu aquatique I-Description d’un plan d’observations complet par projection de variables. Acta Oecol 8: 403–426

    Google Scholar 

  14. Dommergues, YR (1995) Nitrogen fixation by trees in relation to soil nitrogen economy. Fert Res 42: 215–230

    Article  CAS  Google Scholar 

  15. Don, RH, Cox, PT, Wainwright, BJ, Baker, K, Mattick, JS (1991) Touchdown PCR to circumvent spurious priming during gene amplification. Nucleic Acids Res 19: 4008

    Article  PubMed  CAS  Google Scholar 

  16. Doran, JC, Turnbull, JW (1997) Australian Trees and Shrubs: Species for Land Rehabilitation and Farm Planting in the Tropics. ACIAR Monograph No. 24. ACIAR, Canberra

  17. Dreyfus, BL, Dommergues, YR (1981) Nodulation of Acacia species by fast and slow growing tropical strains of Rhizobium. Appl Environ Microbiol 41: 97–99

    PubMed  Google Scholar 

  18. Felsenstein, J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39: 783–791

    Article  Google Scholar 

  19. Gibson, AH (1980) Methods for legumes in glasshouses and controlled environment cabinets. In: Bergersen, FJ (Ed.) Methods for Evaluating Biological Nitrogen Fixation. Wiley-Interscience, Chichester, pp 139–184

    Google Scholar 

  20. Giri, B, Kapoor, R, Mukerji, KG (2003) Influence of arbuscular mycorrhizal fungi and salinity on growth, biomass, and mineral nutrition of Acacia auriculiformis. Biol Fertil Soils 38: 170–175

    Article  Google Scholar 

  21. Hall, JB (1994) Acacia seyal—multipurpose tree of the Sahara desert. NFTA 94-07. FACT Net. Winrock International, Little Rock

    Google Scholar 

  22. Khbaya, B, Neyra, M, Normand, P, Zerhari, K, Filali-Maltouf, A (1998) Genetic diversity and phylogeny of rhizobia that nodulate Acacia spp. in Morocco assessed by analysis of rRNA genes. Appl Environ Microbiol 64: 4912–4917

    PubMed  CAS  Google Scholar 

  23. 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

    Article  PubMed  CAS  Google Scholar 

  24. Krasova-Wade, T, Ndoye, I, Braconnier, S, Sarr, B, de Lajudie, P, Neyra, M (2003) Diversity of indigeneous bradyrhizobia associated with three cowpea cultivars (Vigna unguiculata (L.) Walp.) grown under limited and favorable water conditions in Senegal (West Africa). Afr J Biotechnol 2: 13–22

    CAS  Google Scholar 

  25. Kwon, SW, Park, JY, Kim, JS, Kang, JW, Cho, YH, Lim, CK, Parker, MA, Lee, GB (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

    Article  PubMed  CAS  Google Scholar 

  26. Laguerre, G, Allard, MR, 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

    PubMed  CAS  Google Scholar 

  27. Mahler, RA, Bezdicek, DF (1978) Diversity of Rhizobium leguminosarum in the Palouse of eastern Washington. Appl Environ Microbiol 36: 780–782

    PubMed  CAS  Google Scholar 

  28. Menna, P, Hungria, M, Barcellos, FG, Bangel, EV, Hess, PN, Martinez-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

    Article  PubMed  CAS  Google Scholar 

  29. Mhamdi, R, Laguerre, G, Aouani, ME, Mars, M, Amarger, N (2002) Different species and symbiotic genotypes of field rhizobia can nodulate Phaseolus vulgaris in Tunisian soils. FEMS Microbiol Ecol 41: 77–84

    Article  CAS  PubMed  Google Scholar 

  30. Mhamdi, R, Mrabet, M, Laguerre, G, Tiwari, R, Aouani, ME (2005) Colonization of Phaseolus vulgaris nodules by Agrobacterium-like strains. Can J Microbiol 51: 105–111

    Article  PubMed  CAS  Google Scholar 

  31. Mohammed, SH, Smouni, A, Neyra, M, Kharchaf, D, Filali-Maltouf, A (2000) Phenotypic characteristics of root-nodulating bacteria isolated from Acacia spp. grown in Libya. Plant Soil 224: 171–183

    Article  Google Scholar 

  32. Moreira, FMS, Gillis, M, Pot, B, Kersters, K, Franco, AA (1993) Characterization of rhizobia isolated from different divergence groups of tropical Leguminosae by comparative polyacrylamide gel electrophoresis of their total proteins. Syst Appl Microbiol 16: 135–146

    Google Scholar 

  33. Mpepereki, S, Makonese, F, Wollum, AG (1997) Physiological characterization of indigenous rhizobia nodulating Vigna unguiculata in Zimbabwean soils. Symbiosis 22: 275–292

    Google Scholar 

  34. Ndoye, I, Gueye, M, Danso, SKA, Dreyfus, B (1995) Nitrogen fixation in Faidherbia albida, Acacia raddiana, Acacia senegal and Acacia seyal estimated using 15N isotope dilution technique. Plant Soil 172: 175–180

    Article  CAS  Google Scholar 

  35. Normand, P, Cournoyer, B, Nazaret, S, Simonet, P (1992) Analysis of a ribosomal RNA operon in the actinomycete Frankia. Gene 111: 119–124

    Article  PubMed  CAS  Google Scholar 

  36. Normand, P, Ponsonnet, C, Nesme, X, Neyra, M, Simonet, P (1996) ITS analysis of prokariotes. In: Akkermans, ADL, van Elsas, JD, et De Bruijn, FJ (Eds.) Molecular Microbial Ecology Manual. Kluwer, Dordrecht

  37. Odee, DW, Sutherland, JM, Makatiani, ET, McInroy, SG, Sprent, JI (1997) Phenotypic characteristics and composition of rhizobia associated with woody legumes growing in diverse Kenya conditions. Plant Soil 188: 65–75

    Article  CAS  Google Scholar 

  38. Perriere, G, Gouy, M (1996) www-query: an on-line retrieval system for biological sequence banks. Biochimie 78: 364–369

    Article  PubMed  CAS  Google Scholar 

  39. Ponsonnet, C, Nesme, X (1994) Identification of Agrobacterium strains by PCR-RFLP analysis of pTi and chromosomal regions. Arch Microbiol 16: 300–309

    Google Scholar 

  40. Rouvier, C, Prin, Y, Reddell, P, Normand, P, Simonet, P (1996) Genetic diversity among Frankia strains nodulating members of the family Casuarinaceae in Australia revealed by PCR and restriction fragment length polymorphism analysis with crushed root nodules. Appl Environ Microbiol 62: 979–985

    PubMed  CAS  Google Scholar 

  41. Saitou, N, Nei, M (1987) The neighbor-joining method: a new method for constructing phylogenetic trees. Mol Biol Evol 4: 406–425

    PubMed  CAS  Google Scholar 

  42. Sarr, A, Neyra, M, Ould-Houeibib, MA, Ndoye, I, Oihabi, A, Lesueur, D (2005) Characterization of native rhizobial populations present in soils from natural forests of Acacia senegal and Acacia nilotica in Trarza and Gorgol regions from Mauritania and the Senegal River Valley. Microb Ecol 50: 152–162

    Article  PubMed  Google Scholar 

  43. Segovia, L, Pinero, D, Palacios, R, Martinez-Romero, E (1991) Genetic structure of a soil population of nonsymbiotic Rhizobium leguminosarum. Appl Environ Microbiol 57: 426–433

    PubMed  CAS  Google Scholar 

  44. Singleton, PW, El-Swaifi, SA, Bohlool, BB (1982) Effect of salinity on Rhizobium growth and survival. Appl Environ Microbiol 44: 884–890

    PubMed  Google Scholar 

  45. Sullivan, JT, Bertrand, DE, Van Berkum, P, Ronson, CW (1996) Four unnamed species of nonsymbiotic rhizobia isolated from the rhizosphere of Lotus corniculatus. Appl Environ Microbiol 62: 2818–2825

    PubMed  CAS  Google Scholar 

  46. Sutherland, JM, Odee, DW, Muluvi, GM, Mcinroy, SG, Patel, A (2000) Single and multi-strain rhizobial inoculation of African acacias in nursery conditions. Soil Biol Biochem 32: 323–333

    Article  CAS  Google Scholar 

  47. Sy, A, Giraud, E, Jourand, P, Garcia, N, Willems, A, de Lajudie, P, Prin, Y, Neyra, M, Gillis, M, Boivin-Masson, C, Dreyfus, B (2001) Methylotrophic Methylobacterium bacteria nodulate and fix nitrogen in symbiosis with legumes. J Bacteriol 183: 214–220

    Article  PubMed  CAS  Google Scholar 

  48. Thiao, M, Neyra, M, Isidore, E, Sylla, S, Lesueur, D (2004) Diversity and effectiveness of rhizobium from Gliricidia sepium native to Reunion Island, Kenya and New Caledonia. World J Microbiol 20: 703–709

    Article  CAS  Google Scholar 

  49. Thioulouse, J, Chessel, D, Dolédec, S, Olivier, JM (1997) ADE-4: a multivariate analysis and graphical display software. Stat Comput 7: 75–83

    Article  Google Scholar 

  50. Thompson, JD, Gibson, TJ, Plewniak, F, Jeanmougin, F, Higgins, DG (1997) The CLUSTAL X windows interface: flexible strategies multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25: 4876–4882

    Article  PubMed  CAS  Google Scholar 

  51. Van Berkum, P, Fuhrmann, JJ (2000) Evolutionary relationships among the soybean bradyrhizobia reconstructed from 16S rRNA gene and internally transcribed spacer region sequence divergence. Int J Syst Evol Microbiol 50: 2165–2172

    PubMed  Google Scholar 

  52. Vincent, JM (1970) A Manual for the Practical Study of Root-Nodule Bacteria. International Biological Programme. Handbook no. 15. Blackwell, Oxford

    Google Scholar 

  53. Von Maydel, LHJ (1983) Trees and Shrubs of the Sahel, their Characteristics and Uses. GTZ, Verlag Josef Margraf, Eschborn

  54. Willems, A, Coopman, R, Gillis, M (2001) Comparison of sequence analysis of 16S–23S rDNA spacer regions, AFLP analysis and DNA–DNA hybridizations in Bradyrhizobium. Int J Syst Evol Microbiol 51: 623–632

    PubMed  CAS  Google Scholar 

  55. Zakhia, F, de Lajudie, P (2001) Taxonomy of rhizobia. Agronomie 21: 569–576

    Article  Google Scholar 

  56. 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

    Article  PubMed  Google Scholar 

  57. Zahran, HH (1999) Rhizobium-legume symbiosis and nitrogen fixation under severe conditions and in arid climate. Microb Mol Biol Rev 63: 968–989

    CAS  Google Scholar 

  58. Zeng, N (2003) Drought in the Sahel. Science 302: 999–1000

    Article  PubMed  CAS  Google Scholar 

  59. Zerhari, K, Aurag, J, Khbaya, B, Kharchaf, D, Filali-Maltouf, A (2000) Phenotypic characteristics of rhizobia isolates nodulating Acacia species in the arid and Saharan regions of Morocco. Lett Appl Microbiol 30: 351–357

    Article  PubMed  CAS  Google Scholar 

  60. Zhang, X, Harper, R, Karsisto, M, Lindström, K (1991) Diversity of Rhizobium bacteria isolated from the root nodules of leguminous trees. Int J Syst Bacteriol 41: 104–113

    Article  Google Scholar 

Download references

Acknowledgments

This work was supported by the Agence Universitaire de la Francophonie (PCSI project no. 6314PS512) and by the Institut de Recherche pour le Développement (Jeune Equipe Associée à l’IRD /Equipe de Recherche sur les Symbioses project). D. Diouf is indebted to IRD, France, for a fellowship “Bourse d’Echange Scientifique de Courte Durée.” The authors are grateful to Dr. C. Chaintreuil for technical help and Dr. Mayécor Diouf for discussions on statistical analyses.

Author information

Authors and Affiliations

  1. Département de Biologie Végétale, Université Cheikh Anta Diop, BP 5005, Dakar, Senegal

    Diegane Diouf & Amadou T. Ba

  2. Laboratoire Commun de Microbiologie IRD/ISRA/UCAD, Centre de Recherche de Bel-Air, BP 1386 - CP 18524, Dakar, Senegal

    Diegane Diouf & Ramatoulaye Samba-Mbaye

  3. CIRAD-Foret, UPR 80 “ETP” Tropical Soil Biology and Fertility Institute (TSBF), CIAT c/o World Agroforestry Centre (ICRAF), P.O. Box 30677, Nairobi, Kenya

    Didier Lesueur

  4. IRD, UMR 113 IRD/CIRAD/AGRO-M/UM2, USC INRA 1242 Laboratoire des Symbioses Tropicales et Méditerranéennes, Campus International de Baillarguet, TA 10/J 34398, Montpellier Cedex 5, France

    Bernard Dreyfus, Philippe de Lajudie & Marc Neyra

Authors
  1. Diegane Diouf
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ramatoulaye Samba-Mbaye
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Didier Lesueur
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Amadou T. Ba
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Bernard Dreyfus
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Philippe de Lajudie
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Marc Neyra
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Diegane Diouf.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Diouf, D., Samba-Mbaye, R., Lesueur, D. et al. Genetic Diversity of Acacia seyal Del. Rhizobial Populations Indigenous to Senegalese Soils in Relation to Salinity and pH of the Sampling Sites. Microb Ecol 54, 553–566 (2007). https://doi.org/10.1007/s00248-007-9243-0

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-007-9243-0

Keywords

Search

Navigation