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Rhizobial diversity associated with the spontaneous legume Genista saharae in the northeastern Algerian Sahara

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Abstract

Genista saharae is an indigenous shrub legume that spontaneously grows in the northeastern Algerian Sahara. It is known for efficient dune fixation and soil preservation against desertification, due to its drought tolerance and its contribution to sustainable nitrogen resources implemented by biological N2-fixation. In this study, the root nodule bacteria of G. saharae were investigated using phenotypic and phylogenetic characterization. A total of 57 rhizobial strains were isolated from nodules from several sites in the hyper-arid region of Metlili and Taibet (east Septentrional Sahara). They all nodulate G. saharae species but they differed in their symbiotic efficiency and effectiveness. The genetic diversity was assessed by sequencing three housekeeping genes (atpD, recA and 16S rRNA). The majority of isolates (81 %) belonged to the genus Ensifer (previously Sinorhizobium), represented mainly by the species Ensifer meliloti. The next most abundant genera were Neorhizobium (17 %) with 3 different species: N. alkalisoli, N. galegae and N. huautlense and Mesorhizobium (1.75 %) represented by the species M. camelthorni. Most of the isolated strains tolerated up to 4 % (w/v) NaCl and grew at 45 °C. This study is the first report on the characterization of G. saharae microsymbionts in the Algerian Sahara.

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References

  • Amrani S, Noureddine NE, Bhatnagar T, Argandoña M, Nieto JJ, Vargas C (2010) Phenotypic and genotypic characterization of rhizobia associated with Acacia saligna (Labill.) Wendl. in nurseries from Algeria. Syst Appl Microbiol 33:44–51. doi:10.1016/j.syapm.2009.09.003

    Article  CAS  PubMed  Google Scholar 

  • Berrada H, Nouioui I, Iraqui Houssaini M, El Ghachtouli N, Gtari M, Fikri Benbrahim K (2012) Phenotypic and genotypic characterizations of rhizobia isolated from root nodules of multiple legume species native of Fez, Morocco. Afr J Microbiol Res 6:5314–5324. doi:10.5897/AJMR11.1505

    CAS  Google Scholar 

  • Bertrand H, Plassard C, Pinochet X, Touraine B, Normand P, Cleyet-Marel JC (2000) Stimulation of the ionic transport system in Brassica napus by a plant growth-promoting rhizobacterium (Achromobacter sp.). Can J Microbiol 46:229–236. doi:10.1139/cjm-46-3-229

    Article  CAS  PubMed  Google Scholar 

  • Brockwell J, Searle SD, Jeavons AC, Waayers M (2005) Nitrogen fixation in Acacias: an untapped resource for sustainable plantations, farm forestry and land reclamation. Australian Centre for International Agricultural Research, Canberra

    Google Scholar 

  • Chehma A, Faye B, Bastianelli D (2010) Valeurs nutritionnelles des plantes vivaces des Parcours sahariens algériens pour dromadaires. Fourrages 204:263–268

    Google Scholar 

  • Chen WP, Kuo TT (1993) A simple and rapid method for the preparation of gram-negative bacterial genomic DNA. Nucleic Acids Res 21:2260. doi:10.1093/nar/21.9.2260

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen WM, Zhu WF, Bontemps C, Young JPW, Wei GH (2011) Mesorhizobium camelthorni sp. nov., isolated from Alhagi sparsifolia. Int J Syst Evol Microbiol 61:574–579. doi:10.1099/ijs.0.022947-0

    Article  CAS  PubMed  Google Scholar 

  • Cox MM (2003) The bacterial RecA protein as a motor protein. Annu Rev Microbiol 57:551–577. doi:10.1146/annurev.micro.57.030502.09095

    Article  CAS  PubMed  Google Scholar 

  • Fernando GA, Jesus M (1998) Biodiversity of rhizobia nodulating Genista monspessulana and Genista linifolia in Spain. N Z J Agric Res 41:585–594. doi:10.1080/00288233.1998.9513342

    Article  Google Scholar 

  • Gaunt MW, Turner SL, Rigottier-Gois L, Lloyd-Macgilps SA, Young JP (2001) Phylogenies of atpD and recA support the small subunit rRNA-based classification of rhizobia. Int J Syst Evol Microbiol 51:2037–2048. doi:10.1099/00207713-51-6-2037

    Article  CAS  PubMed  Google Scholar 

  • Ghosh W, Roy P (2006) Mesorhizobium thiogangeticum sp. nov., a novel sulfur-oxidizing chemolithoautotroph from rhizosphere soil of an Indian tropical leguminous plant. Int J Syst Evol Microbiol 56:91–97. doi:10.1099/ijs.0.63967-0

    Article  CAS  PubMed  Google Scholar 

  • Kalita M, Malek W (2004) Phenotypic and genomic characteristics of Rhizobia isolated from Genista tinctoria root nodules. Syst Appl Microbiol 27:707–715

    Article  CAS  PubMed  Google Scholar 

  • Karanja NK, Wood M (1988) Selecting Rhizobium phaseoli strains for use with beans (Phaseolus vulgaris L.) in Kenya: infectiveness and tolerance of acidity and aluminium. Plant Soil 112:7–13. doi:10.1007/BF02181746

    Article  CAS  Google Scholar 

  • Le Houérou HN (1990) Définition et limites bioclimatiques du Sahara. Sécheresse 1:246–259

    Google Scholar 

  • Le Houérou HN (1997) Biodiversité végétale et diversité génétique en Afrique. Sécheresse 2:117–122

    Google Scholar 

  • Lloyd AT, Sharp PM (1993) Evolution of the recA gene and the molecular phylogeny of bacteria. J Mol Evol 37:399–407. doi:10.1007/BF00178869

    Article  CAS  PubMed  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. doi:10.1111/j.1472-765X.2007.02233.x

    Article  CAS  PubMed  Google Scholar 

  • Martens M, Delaere M, Coopman R, De Vos P, Gillis G, Willems A (2007) Multilocus sequence analysis of Ensifer and related taxa. Int J Syst Evol Microbiol 57:489–503. doi:10.1099/ijs.0.64344-0

    Article  CAS  PubMed  Google Scholar 

  • Martens M, Dawyndt P, Coopman R, Gillis M, De Vos P, Willems A (2008) Advantages of multilocus sequence analysis for taxonomic studies: a case study using 10 housekeeping genes in the genus Ensifer (including former Sinorhizobium). Int J Syst Evol Microbiol 58:200–214. doi:10.1099/ijs.0.65392-0

    Article  CAS  PubMed  Google Scholar 

  • Maynaud G, Willems A, Soussou S, Vidal C, Mauré L, Moulin L et al (2012) Molecular and phenotypic characterization of strains nodulating Anthyllis vulneraria in mine tailings, and proposal of Aminobacter anthyllidis sp. nov., the first definition of Aminobacter as legume-nodulating bacteria. Syst Appl Microbiol 35:65–72. doi:10.1016/j.syapm.2011.11.002

    Article  CAS  PubMed  Google Scholar 

  • Merabet C, Martens M, Mahdhi M, Zakhia F, Sy A, Le Roux C et al (2010) Multilocus Sequence analysis of root nodule isolates from Lotus arabicus (Senegal), Lotus creticus, Argyrolobium uniflorum and Medicago sativa (Tunisia) and description of Ensifer numidicus sp. nov. and Ensifer garamanticus sp. nov. Int J Syst Evol Microbiol 60:664–674. doi:10.1099/ijs.0.012088-0

    Article  CAS  PubMed  Google Scholar 

  • Meriane D, Kaabache M (2012) Ecology, biology and biometry of an endemic fabaceae: genista saharae cosson and durieu. J Life Sci 6:501

    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. doi:10.1007/s00203-006-0173-x

    Article  CAS  PubMed  Google Scholar 

  • Mousavi SA, Österman J, Wahlberg N, Nesme X, Lavire C et al (2014) Phylogeny of the Rhizobium–Allorhizobium–Agrobacterium clade supports the delineation of Neorhizobium gen. nov. Syst Appl Microbiol 37:208–15. doi:10.1016/j.syapm.2013.12.007

    Article  CAS  PubMed  Google Scholar 

  • Nedjraoui D (2001) Country Pasture/Forage Resource Profiles: Algeria

  • Nicholas KB, Nicholas HB (1997) GeneDoc: a tool for editing and annotating multiple sequence alignments. Pittsburgh Supercomputing Center, Pittsburgh

    Google Scholar 

  • OZENDA P (1991) Flore du Sahara, 3ème édition complétée, Paris, Centre national de la recherche scientifique (CNRS)

  • Quezel P (1978) Analyses of the flora Mediterranean and Saharan Africa. Ann Mo Bot Gard 56:479–534

    Article  Google Scholar 

  • Rejili M, Mahdhi M, Fterich A, Dhaoui S, Guefrachi I, Abdeddayem R et al (2012) Symbiotic nitrogen fixation of wild legumes in Tunisia: soil fertility dynamics, field nodulation and nodules effectiveness. Agric Ecosyst Environ 157:60–69. doi:10.1016/j.agee.2012.01.015

    Article  Google Scholar 

  • Rivas R, García-Fraile P, Velázquez E (2009) Taxonomy of bacteria nodulating legumes. Microbiol Insights 2:51–69

    Google Scholar 

  • Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB et al (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541. doi:10.1128/AEM.01541-09

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sharma SR, Rao NK, Gokhale TS, Ismail S (2013) Isolation and characterization of salt-tolerant rhizobia native to the desert soils of United Arab Emirates. Emir J Food Agric 25:102–108. doi:10.9755/ejfa.v25i2.7590

    Google Scholar 

  • Szeto WW, Zimmerman JL, Ausubel SV, FMA (1984) Rhizobium meliloti symbiotic regulatory gene. Cell 36:1035–43. doi:10.1078/0723202042369965

    Article  CAS  PubMed  Google Scholar 

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–27339. doi:10.1093/molbev/msr121

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882. doi:10.1093/nar/25.24.4876

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Udvardi M, Poole PS (2013) Transport and metabolism in legume-rhizobia symbioses. Annu Rev Plant Biol 64:781–785. doi:10.1146/annurev-arplant-050312-120235

    Article  CAS  PubMed  Google Scholar 

  • Vincent JM (1970) A manual for practical study of root nodule bacteria. IBP Handbook 15. Blackwell Sci. Publ. Oxford

  • Wawrik B, Kerkhof L, Zylstra GJ, Kukor JJ (2005) Identification of unique type II polyketide synthase genes in soil. Appl Environ Microbiol 71:2232–2238. doi:10.1128/AEM.71.5.2232-2238.2005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zahran HH (1999) Rhizobium-legume symbiosis and nitrogen fixation under severe conditions and in an arid climate. Microbiol Mol Biol Rev 63:968–89

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zakhia F, Jeder H, Domergue O, Willems A, Cleyet-Marel JC, Gillis M et al (2004) Characterisation of wild legume nodulating bacteria (LNB) in the infra-arid zone of Tunisia. Syst Appl Microbiol 27:380–395. doi:10.1078/0723-2020-00273

    Article  PubMed  Google Scholar 

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Acknowledgments

We would like to gratefully acknowledge Prof. Ahmed Boutarfaya and Prof. Samia Bissati, (both from the University of Kasdi Merbah-Ouargla) for their support and encouragement.

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Authors and Affiliations

  1. Laboratoire Génie de l’eau et de l’Environnement en Milieu Saharien, Université Kasdi Merbah Ouargla, BP 511, 30 000, Ouargla, Algeria

    Khaled Chaïch

  2. Laboratoire de Microbiologie, Faculté des Sciences, Université d’Oran Es-Sénia, Oran, Algeria

    Abdelkader Bekki

  3. Laboratoire de Biologie des Systèmes Microbiens (LBSM), Ecole Normale Supérieure de Kouba, BP 92, 16308, Vieux-Kouba, Alger, Algeria

    Noureddine Bouras

  4. Département de Biologie, Faculté des Sciences de la Nature et de la Vie et Sciences de la Terre, Université de Ghardaïa, BP 455, Ghardaïa, 47000, Algeria

    Noureddine Bouras

  5. Field Crop Development Centre, Alberta Agriculture and Rural Development, 6000 C & E Trail, Lacombe, AB, T4L 1 W8, Canada

    Michael D. Holtz

  6. IRD-INRA, Laboratoire des Symbioses Tropicales et Méditerranéennes (LSTM), Campus International de Baillarguet TA A-82/J, F-34398, Montpellier Cedex 5, France

    Souhir Soussou, Lucette Mauré, Brigitte Brunel, Philippe de Lajudie & Jean-Claude Cleyet-Marel

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  1. Khaled Chaïch
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  9. Jean-Claude Cleyet-Marel
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Correspondence to Noureddine Bouras.

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Funding statement

This work was supported by the Ministère de l’Enseignement Supérieur et de la Recherche Scientifique (MESRS) of Algeria. The funder had no role in study design, data collection and analyses, preparation of the manuscript or decision to publish.

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The authors declare that there are no personal, financial or any other conflicts of interest to declare.

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This article does not contain any studies with human participants and/or animals performed by any of the authors. The formal consent is not required in this study.

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Chaïch, K., Bekki, A., Bouras, N. et al. Rhizobial diversity associated with the spontaneous legume Genista saharae in the northeastern Algerian Sahara. Symbiosis 71, 111–120 (2017). https://doi.org/10.1007/s13199-016-0414-y

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