Abstract
This study focused on the genetic, symbiotic and phenotypic diversity of a collection of 12 Vachellia seyal and Prosopis juliflora rhizobial strains that were isolated from soils influenced by the roots of the grass Sporobolus robustus. Phylogenetic trees were constructed based on data from the 16S rRNA gene, from a multi-locus sequence analysis (MLSA) of the housekeeping genes recA, atpD, glnA and gyrB, as well as from the symbiotic genes nodA, nodC and nifH. Most of the mesorhizobial strains were clustered with the M. plurifarium type strain ORS 1032T and the 16S rRNA gene was as discriminatory as the other housekeeping genes. The Ensifer collection was closely related to E. alkalisoli YIC 4027T and E. fredii LMG 6217T using 16S rRNA and MLSA. Amplification of the Rhizobium collection was only observed with the 16S rRNA gene, where the strains were clustered with Rhizobium sp. 1B, Rhizobium sp. SEMIA 6411, Rhizobium sp. AS1-101a and Rhizobium sp. ORS 3441. The phylogeny of the nifH gene from Mesorhizobium and Ensifer strains were similar to those of nodulation genes (nodA and nodC). The nodA-nodC and nifH gene phylogenies were not consistent with those of 16S rRNA and the housekeeping genes. Ensifer genospecies tolerated high salinity better than the other genotypes after testing on a salt content gradient up to 49‰. We conclude that the rhizosphere of Sporobolus tussocks harbors a rhizobial microbiota, which could be capable of helping V. seyal and P. juliflora to grow better in saline soils.
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References
Alexandre A, Laranjo M, Young JPW, Oliveira S (2008) dnaJ is a useful phylogenetic marker for alphaproteobacteria. Int J Syst Evol Microbiol 58:2839–2849
Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J MolBiol 215(3):403–410
Andrews M, De Meyer S, James EK, Stepkowski T, Hodge S, Simon MF et al (2018) Horizontal transfer of symbiosis genes within and between rhizobial genera: occurrence and importance. Genes 9:321
Bakhoum N, Galiana A, Le Roux C, Kane A, Duponnois R, Ndoye F, Fall D, Noba K, Sylla SN, Diouf D (2014) Phylogeny of nodulation genes and symbiotic diversity of Acacia senegal (L.) Willd. And A. seyal (Del.) Mesorhizobium strains from different regions of Senegal. Microb Ecol 69:641–651
Barcellos FG, Menna P, da Silva Batista JS, Hungria M (2007) Evidence of horizontal transfer of symbiotic genes from a Bradyrhizobium japonicum inoculant strain to indigenous diazotrophs Sinorhizobium (Ensifer) fredii and Bradyrhizobium elkanii in a Brazilian Savannah soil. Appl Environ Microbiol 73:2635–2643
Benidire L, Lahrouni M, Daoui K, el Abidine FZ, Carmona RG, Göttfert M, Oufdou K (2018) Phenotypic and genetic diversity of Moroccan rhizobia isolated from Vicia faba and study of genes that are likely to be involved in their osmotolerance. Syst Appl Microbiol 41(1):51–61
Beukes CW, Boshoff FS, Phalane FL, Hassen AI, le Roux MM, Stepkowski T et al (2019) Both alpha-and beta-rhizobia occupy the root nodules of Vachellia karroo in South Africa. Front Microbiol 10:1195
Bouhnik O, ElFaik S, Alami S, Talbi C, Lamin H, Abdelmoumen H, Tortosa Muñoz G, J. Bedmar E, Missbah el Idrissi M (2019) Ensifer fredii symbiovar vachelliae nodulates endemic Vachellia gummifera in semiarid Moroccan areas. Syst Appl Microbiol 42(5):125999
Choudhary S, Tak N, Bissa G, Chouhan B, Choudhary P, Sprent JI, James EK, Gehlot HS (2020) The widely distributed legume tree Vachellia (Acacia) nilotica subsp. indica is nodulated by genetically diverse Ensifer strains in India. Symbiosis 80(1):15–31
Cordero I, Ruiz-Díez B, de la Peña TC, Balaguer L, Lucas MM, Rincón A, Pueyo JJ (2016) Rhizobial diversity, symbiotic effectiveness and structure of nodules of Vachellia macracantha. Soil Biol Biochem 96:39–54
Dang X, Xie Z, Liu W, Sun Y, Liu X, Zhu Y, Staehelin C (2019) The genome of Ensifer alkalisoli YIC4027 provides insights for host specificity and environmental adaptations. BMC Genomics 20(1):643
De Lajudie P, Fulele-Laurent E, Willems A, Torck U, Coopman R, Collins MD, 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
Diedhiou S, Dossa EL, Badiane AN, Diedhiou I, Sène M, Dick RP (2009) Decomposition and spatial microbial heterogeneity associated with native shrubs in soils of agroecosystems in semi-arid Senegal. Pedobiologia 52:273–286
Diouf D, Fall D, Chaintreuil C, Ba AT, Dreyfus B, Neyra M, Ndoye I, Moulin L (2010) Phylogenetic analyses of symbiotic genes and characterization of functional traits of Mesorhizobium spp. strains associated with the promiscuous species Acacia seyal Del. J Appl Microbiol 108(3):818–830
Diouf D, Samba-Mbaye R, Lesueur D, Ba AT, Dreyfus B, de Lajudie P, Neyra M (2007) 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
Diouf F, Diouf D, Klonowska A, Le Queré A, Bakhoum N, Fall D, Neyra M, Parrinello H, Diouf M, Ndoye I, Moulin L (2015) Genetic and genomic diversity studies of acacia symbionts in Senegal reveal new species of Mesorhizobium with a putative geographical pattern. PLoS One 10(2):e0117667
Dobert RC, Breil BT, Triplett EW (1994) DNA sequence of the common nodulation genes of Bradyrhizobium elkanii and their phylogenetic relationship to those of other nodulating bacteria. Mol Plant-Microbe Interact 7:564–572
Dommergues YR (1995) Nitrogen fixation by trees in relation to soil nitrogen economy. Fertilizer Research 42(1–3):215–230
Dossa EL, Diedhiou S, Compton J, Assigbetse K, Dick RP (2010) Spatial patterns of P fractions and chemical properties in soils of two native shrub communities in Senegal. Plant Soil 327:185–198
Eardly BD, Nour SM, van Berkum P, Selander RK (2005) Rhizobial 16S rRNA and dnaK genes: mosaicism and the uncertain phylogenetic placement of Rhizobium galegae. Appl Environ Microbiol 71:1328–1335
Estrella MJ, Muñoz S, Soto MJ, Ruiz O, Sanjuán J (2009) Genetic diversity and host range of rhizobia nodulating Lotus tenuis in typical soils of the Salado River basin (Argentina). Appl Environ Microbiol 75(4):1088–1098
Fall F, Le Roux C, Bâ AM, Fall D, Bakhoum N, Faye MN, Diouf D (2019) The rhizosphere of the halophytic grass Sporobolus robustus Kunth hosts rhizobium genospecies that are efficient on Prosopis juliflora (Sw.) DC and Vachellia seyal (Del.) PJH hurter seedlings. Syst Appl Microbiol 42:232–239
Gaunt MW, Turner SL, Rigottier-Gois L, Lloyd-Macgilp 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
Giraud E, Moulin L, Vallenet D, Barbe V, Cytryn E, Avarre JC, Jaubert M, Simon D, Cartieaux F, Prin Y, Bena G, Hannibal L, Fardoux J, Kojadinovic M, Vuillet L, Lajus A, Cruveiller S, Rouy Z, Mangenot S, Segurens B, Dossat C, Franck WL, Chang WS, Saunders E, Bruce D, Richardson P, Normand P, Dreyfus B, Pignol D, Stacey G, Emerich D, Vermeglio A, Medigue C, Sadowsky M (2007) Legumes symbioses: absence of nod genes in photosynthetic bradyrhizobia. Science 316(5829):1307–1312
Lan R, Reeves PR (2000) Intraspecies variation in bacterial genomes: the need for a species genome concept. Trends Microbiol 8:96–401
Laranjo M, Alexandre A, Rivas R, Velazquez E, Young JP, Oliveira S (2008) Chickpea rhizobia symbiosis genes are highly conserved across multiple Mesorhizobium species. FEMS Microbiol Ecol 66:391–400
Li Y, Li X, Liu Y, Wang ET, Ren C, Liu W, Xu H, Wu NJ, Li Y, Zhan X, Xie Z (2016) Genetic diversity and community structure of rhizobia nodulating Sesbania cannabina in saline–alkaline soils. System Appl Microbiol 39(3):195–202
Lorite MJ, Donate-Correa J, del Arco-Aguilar M, Pérez Galdona R, Sanjuán J, León-Barrios M (2010) Lotus endemic to the Canary Islands are nodulated by diverse and novel rhizobial species and symbiotypes. Syst Appl Microbiol 33:282–290
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
Martens M, Delaere M, Coopman R, De Vos P, Gillis M et al (2007) Multilocus sequence analysis of Ensifer and related taxa. Int J Syst Evol Microbiol 57:489–503
Moulin L, Bena G, Boivin-Masson C, Stepkowski T (2004) Phylogenetic analyses of symbiotic nodulation genes support vertical and lateral gene co-transfer within the Bradyrhizobium genus. Mol Phylogenet Evol 30:720–732
Normand P, Cournoyer B, Simonet P, Nazaret S (1992) Analysis of a ribosomal RNA operon in the actinomycete Frankia. Gene 111:119–124
Olsen GJ, Woese CR (1993) Ribosomal RNA: a key to phylogeny. FASEB J 7:113–123
Perret X, Staehelin C, Broughton WJ (2000) Molecular basis of symbiotic promiscuity. Microbiol Mol Biol Rev 64:180–201
Poly F, Ranjard L, Nazaret S, Gourbiere F, Jocteur-Monrozier LJ (2001) Comparison of nifH gene pools in soils and soil microenvironments with contrasting properties. Appl Environ Microbiol 67:2255–2262
Sankhla IS, Tak N, Meghwal RR, Choudhary S, Alkesh T, Rathi S, Sprent JI, James EK, Gehlot HS (2017) Molecular characterization of nitrogen fixing microsymbionts from root nodules of Vachellia (Acacia) jacquemontii, a native legume from the Thar Desert of India. Plant Soil 410:21–40
Sarita S, Sharma PK, Priefer UB, Prell J (2005) Direct amplification of rhizobial nodC sequences from soil total DNA and comparison to nodC diversity of root nodule isolates. FEMS Microbiol Ecol 54(1):1–11
Stackebrandt E, Frederiksen W, Garrity GM, Grimont PAD, Kampfer P, Maiden MCJ, Nesme X, Rossello-Mora R, Swings J et al (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
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
Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30(12):2725–2729
Thompson JD, Higgins DG, Gibson TJ (1994) ClustalW: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680
Turner SL, Young JPW (2000) The glutamine synthetases of rhizobia: phylogenetics and evolutionary implications. Mol Biol Evol 17:309–319
Vandamme P, Pot B, Gillis M, de Vos P, Kersters K, Swings J (1996) Polyphasic taxonomy, a consensus approach to bacterial systematics. Microbiol Rev 60:407–438
Vincent JM (1970) A manual for the practical study of root-nodule Bacteria IBP handbook no. 15, Blackwell, Edinburgh, U.K.
Vinuesa P, Silva C, Lorite MJ, Izaguirre-Mayoral ML, Bedmar EJ, Martinez-Romero E (2005) Molecular systematics of rhizobia based on maximum likelihood and Bayesian phylogenies inferred from rrs, atpD, recA and nifH sequences, and their use in the classification of Sesbania microsymbionts from Venezuelan wetlands. Syst Appl Microbiol 28:702–716
Zhang JJ, Lou K, Jin X, Mao PH, Wang ET, Tian CF, Sui XH, Chen WF, Chen WX (2012) Distinctive Mesorhizobium populations associated with Cicer arietinum L. in alkaline soils of Xinjiang, China. Plant Soil 353:123–134
Zhao CT, Wang ET, Chen WF, Chen WX (2008) Diverse genomic species and evidences of symbiotic gene lateral transfer detected among the rhizobia associated with Astragalus species grown in the temperate regions of China. FEMS Microbiol Lett 286(2):263–273
Acknowledgments
We thank Joël Fardoux (LSTM, Montpellier) for his valuable technical assistance. This work was funded by the International Foundation for Science (IFS). The authors wish to thank Peter Biggins and the Editor-in-Chief of Symbiosis for reviewing the English of the manuscript.
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Fall, F., Le Roux, C., Bâ, A.M. et al. The leguminous trees Vachellia seyal (Del.) and Prosopis juliflora (Swartz) DC and their association with rhizobial strains from the root-influence zone of the grass Sporobolus robustus Kunth. Symbiosis 84, 61–69 (2021). https://doi.org/10.1007/s13199-021-00763-7
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DOI: https://doi.org/10.1007/s13199-021-00763-7