Skip to main content

Advertisement

SpringerLink
Log in

Genetic diversity and salt tolerance of Sinorhizobium populations from two Tunisian soils

  • Original Article
  • Published:
Annals of Microbiology Aims and scope Submit manuscript

Abstract

Leguminous plants are promising pioneer-species for colonization of marginal areas and soils undergoing desertification. They derive part of their colonization abilities from their symbiotic interaction with nitrogen-fixing bacteria known as rhizobia. In this work, we analyzed total and culturable rhizobium communities from two Tunisian soils in close proximity to each other: one non-salty and cultivated and the other uncultivated and salty. The taxonomic diversity of the Rhizobiaceae family, evaluated by terminal restriction fragment length polymorphism (T-RFLP) on total soil DNA, revealed a high diversity of ribotypes and soil-based differentiation of the communities. We then used PCR-RFLP of the intergenic space and salt tolerance to characterize the genetic and phenotypic polymorphism of 150 Sinorhizobium isolates trapped on Medicago truncatula. In the salty soil, two different species, Sinorhizobium meliloti and Sinorhizobium medicae, were trapped; by contrast, only isolates of S. meliloti were trapped from the agricultural soil. Moreover, isolates from the salty soil were more tolerant to NaCl, and strains growing up to 1 M NaCl were found. No relationships between genotypic profiles and salt tolerance phenotypes were found.

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

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Badri Y, Zribi K, Badri M, Huget T, Aouni ME (2003) Sinorhizobium meliloti nodutes Medicago laciniata in Tunisian soils. Czech J Genet Plant Breed 39:178–183

    Google Scholar 

  • Ben Romdhane S, Tajini F, Trabelsi M, Aouani ME, Mhamdi R (2007) Competition for nodule formation between introduced strains of Mesorhizobium ciceri and the native populations of rhizobia nodulating chickpea (Cicer arietinum) in Tunisia. World J Microbiol Biotechnol 23:1195–1201

    Article  Google Scholar 

  • Bernard T, Pocard JA, Perroud B, Le Rudulier D (1986) Variations in the response of salt-stressed Rhizobium strains to betaines. Arch Microbiol 143:359–364

    Article  CAS  Google Scholar 

  • Biondi EG, Pilli E, Giuntini E, Roumiantseva ML, Andronov EE, Onichtchouk OP, Kurchak ON, Simarov BV, Dzyubenko NI, Mengoni A, Bazzicalupo M (2003) Genetic relationship of Sinorhizobium meliloti and Sinorhizobium medicae strains isolated from Caucasian region. FEMS Microbiol Lett 220:207–213

    Article  CAS  PubMed  Google Scholar 

  • Brockwell J (1980) Experiments with crop and pasture legumes: principles and practice. In: Bergersen FJ (ed) Methods for evaluating biological nitrogen fixation. Wiley, Chichester, pp 417–488

    Google Scholar 

  • Brockwell J, Bottomley PJ, Thies JE (1988) Manipulation of rhizobia microflora for improving legume productivity and soil fertility: a critical assessment. Plant Soil 174:143–180

    Article  Google Scholar 

  • Bromfield ESP, Barran LR, Wheatcroft R (1995) Relative genetic structure of a population of Rhizobium meliloti isolated directly from soil and from nodules of alfalfa (Medicago sativa) and sweet clover (Melilotus alba). Mol Ecol 4:183–188

    Article  Google Scholar 

  • Elboutahiri N, Thami-Alami I, Udupa SM (2010) Phenotypic and genetic diversity in Sinorhizobium meliloti and S. medicae from drought and salt affected regions of Morocco. BMC Microbiol 10:15

    Article  PubMed  Google Scholar 

  • Fujihara S, Yoneyama T (1994) Response of Rhizobium fredii P220 to osmotic shock: interrelationships between K1, Mg21, glutamate and homospermidine. Microbiology 140:1909–1916

    Article  CAS  Google Scholar 

  • Gouffi K, Pica N, Pichereau V, Blanco C (1999) Disaccharides as a new class of non accumulated osmoprotectants for Sinorhizobium meliloti. Appl Environ Microbiol 65:1491–1500

    CAS  PubMed  Google Scholar 

  • Kuykendall LD, Abdel-Waheb SM, Hashem FM, van Berkum P (1994) Symbiotic competence and genetic diversity of Rhizobium strains used as inoculants for alfalfa and berseem clover. Lett Appl Microbiol 9:477–482

    Article  Google Scholar 

  • Laguerre G, Mavingui P, Allard MR, Charnay MP, Louvrier P, Mazurier SI, 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

    CAS  PubMed  Google Scholar 

  • Lal B, Khanna S (1995) Selection of salt tolerant Rhizobium isolates of Acacia nilotica. World J Microbiol Biotechnol 10:637–639

    Article  Google Scholar 

  • Lane DJ (1991) 16 S/23 S rRNA sequencing. In: Stackebrandt E, Goodfellow M (eds) Nucleic acid techniques in bacterial systematics. Wiley, Chichester, pp 115–175

    Google Scholar 

  • Mahdhi M, Nzoué A, Gueye F, Merabet C, de Lajudie P, Mars M (2007) Phenotypic and genotypic diversity of Genista saharae microsymbionts from the infra-arid region of Tunisia. Lett Appl Microbiol 45:604–609

    Article  CAS  PubMed  Google Scholar 

  • Mengoni A, Giuntini E, Bazzicalupo M (2007) Application of terminal-restriction fragment length polymorphism for molecular analysis of soil bacterial communities. In: Varma A, Oelmuller R (eds) Soil biology, vol 11, Advanced techniques in soil microbiology. Springer, Berlin, pp 295–305

    Google Scholar 

  • 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. Microb Ecol 41:77–84

    Article  CAS  Google Scholar 

  • Miller KJ, Wood JM (1996) Osmoadaptation by rhizosphere bacteria. Annu Rev Microbiol 50:101–136

    Article  CAS  PubMed  Google Scholar 

  • Mnasri B, Mrabet M, Laguerre G, Aouani ME, Mhamdi R (2007) Salt-tolerant rhizobia isolated from a Tunisian oasis that are highly effective for symbiotic N2-fixation with Phaseolus vulgaris constitute a novel biovar (bv. mediterranense) of Sinorhizobium meliloti. Arch Microbiol 187:79–85

    Article  CAS  PubMed  Google Scholar 

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

    Google Scholar 

  • Øvreås L, Torsvik V (1998) Microbial diversity and community structure in two different agricultural soil communities. Microb Ecol 36:303–315

    Article  PubMed  Google Scholar 

  • Palmer KM, Young JPW (2000) Higher diversity of Rhizobium leguminosarum biovar viciae populations in arable soils than in grass soils. Appl Environ Microbiol 66:2445–2450

    Article  CAS  PubMed  Google Scholar 

  • Payakapong W, Tittabutr P, Teaumroong N, Boonkerd N, Paul WS, Borthakur D (2006) Identification of two clusters of genes involved in salt tolerance in Sinorhizobium sp. strain BL3. Symbiosis 41:47–53

    CAS  Google Scholar 

  • Pocard JA, Vincent N, Boncompagni E, Smith LT, Poggi MC, Le Rudulier D (1997) Molecular characterization of the bet genes encoding glycine betaine synthesis in Sinorhizobium meliloti 102F34. Microbiology 143:1369–1379

    Article  CAS  PubMed  Google Scholar 

  • Provorov NA, Tikhonovich IA (2003) Genetic resources for improving nitrogen fixation in legume-rhizobia symbiosis. Genet Resour Crop Evol 50:89–99

    Article  CAS  Google Scholar 

  • Rohlf FJ (1990) NTSYS-pc Numerical taxonomy and multivariate analysis system. Version 2.02. Exeter Software, New York

  • Saleena LM, Rangarajan S, Nair S (2002) Diversity of Azospirillum strains isolated from rice plants grown in saline and non saline sites of coastal agricultural ecosystem. Microb Ecol 44:271–277

    Article  CAS  PubMed  Google Scholar 

  • Shamseldin A, Nyalwidhe J, Werner DA (2006) Proteomic approach towards the Analysis of salt tolerance in Rhizobium etli and Sinorhizobium meliloti strains. Curr Microbiol 52:333–339

    Article  CAS  PubMed  Google Scholar 

  • Shyu C, Soule T, Bent SJ, Foster JA, Forney LJ (2007) MiCA: a web-based tool for the analysis of microbial communities based on Terminal-Restriction Fragment Length Polymorphisms of 16 S and 18 S rRNA Genes. Microb Ecol 53:562–570

    Article  CAS  PubMed  Google Scholar 

  • Subbian P, Lal R, Subramanian KS (2000) Cropping systems effects on soil quality in semi-arid tropics. J Sustain Agric 16:7–38

    Article  Google Scholar 

  • Talebi Bedaf M, Bahar M, Saeidi G, Mengoni A, Bazzicalupo M (2008) Diversity of Sinorhizobium strains nodulating Medicago sativa from different Iranian regions. FEMS Microbiol Lett 288:40–46

    Article  Google Scholar 

  • Talibart R, Jebbar H, Gouffi K, Pichereau V, Gouesbet G, Blanco C, Bernard T, Pocord JA (1997) Transient accumulation of glycine and dynamics of endogenous osmolytes in salt stressed cultures of Sinorhizobium meliloti. Appl Environ Microbiol 63:4657–4663

    CAS  PubMed  Google Scholar 

  • Tate RL (1995) Soil microbiology (symbiotic nitrogen fixation. Wiley, New York, pp 307–333

    Google Scholar 

  • Tom-Petersen A, Leser TD, Marsh TL, Nybroe O (2003) Effect of copper amendment on the bacterial community in agricultural soil analysed by T-RFLP. FEMS Microbiol Ecol 46:53–62

    Article  CAS  PubMed  Google Scholar 

  • Trabelsi D, Mengoni A, Aouani ME, Mhamdi R, Bazzicalupo M (2009) Genetic diversity and salt tolerance of bacterial communities from two Tunisian soils. Ann Microbiol 59:1–8

    Article  Google Scholar 

  • Vance CP (1998) Legume symbiotic nitrogen fixation: agronomic aspets. In: Spaink HP, Kondorosi A, Hooykaas PJJ (eds) The Rhizobiaceae. Kluwer, Dortrecht, pp 509–530

    Google Scholar 

  • Villegas MC, Rome S, Mauré L, Domergue O, Gardan L, Bailly X, Cleyet-Marel JC, Brunel B (2006) Nitrogen fixing sinorhizobia with Medicago laciniata constitute a novel biovar (bv. Medicaginis) of S.meliloti. Syst Appl Microbiol 29:526–538

    Article  Google Scholar 

  • Vincent JM (1970) A Manual for practical study of root-nodule bacteria. IBP handbook 15. Blackwell Scientific Publications, Oxford, UK, ISBN 632-06410-2

    Google Scholar 

  • Zahran H (1999) Rhizobium-legume symbiosis and nitrogen fixation under severe conditions and in an arid climate. Microbiol Mol Biol Rev 63:968–989

    CAS  PubMed  Google Scholar 

  • Zakhia F, Jeder H, Domergue O, Willems A, Cleyet-Marel JC, Gillis M, Dreyfus B, de Lajudie P (2004) Characterisation of wild legume nodulating bacteria (LNB) in the infra-arid zone of Tunisia. Syst Appl Microbiol 27:380–395

    Article  PubMed  Google Scholar 

  • Zhang X, Kosier B, Priefer UB (2001) Genetic diversity of indigenous Rhizobium leguminosarum bv. viciae isolates nodulating two different host plants during soil restoration with alfalfa. Mol Ecol 10:2297–2305

    Article  CAS  PubMed  Google Scholar 

  • Zribi K, Mhamdi R, Huguet T, Aouani ME (2004) Distribution and genetic diversity of rhizobia nodulating natural populations of Medicago truncatula in Tunisian soils. Soil Biol Biochem 36:903–908

    Article  CAS  Google Scholar 

  • Zribi K, Badri Y, Van Berkum B, Aouani ME (2007) Medicago ciliaris growing in Tunisian soils is preferentially nodulated by Sinorhizobium medicae. Aust J Soil Res 45:473–477

    Article  Google Scholar 

Download references

Acknowledgments

This work was partially supported by the University of Firenze (Italy) “Scambi culturali e cooperazione interuniversitaria internazionale (cap.f.s.2.16.04).

Author information

Authors and Affiliations

  1. Laboratoire des Légumineuses, Centre de Biotechnologie de Borj-Cedria, BP 901, Hammam-Lif, 2050, Tunisia

    Darine Trabelsi, Mohammed Elarbi Aouani & Ridha Mhamdi

  2. Department of Evolutionary Biology, University of Firenze, via Romana 17, 50125, Florence, Italy

    Alessio Mengoni & Marco Bazzicalupo

Authors
  1. Darine Trabelsi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Alessio Mengoni
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Mohammed Elarbi Aouani
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Marco Bazzicalupo
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Ridha Mhamdi
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Darine Trabelsi.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Trabelsi, D., Mengoni, A., Aouani, M.E. et al. Genetic diversity and salt tolerance of Sinorhizobium populations from two Tunisian soils. Ann Microbiol 60, 541–547 (2010). https://doi.org/10.1007/s13213-010-0084-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13213-010-0084-6

Keywords

Search

Navigation