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Recent changes to the classification of symbiotic, nitrogen-fixing, legume-associating bacteria: a review

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Abstract

The Rhizobia are collectively comprised of gram negative soil bacteria that have the ability to form symbiotic nitrogen-fixing root and/or stem nodules in association with leguminous plants. The taxonomy of these bacteria is continually in a state of flux, in large part due to rapid development of refined molecular biology techniques. The isolation and characterization of new, and often different, legumes-nodulating bacteria on a variety of plant hosts has resulted in the naming of many new rhizobial species. Here we update the taxonomy of the legume-nodulating bacteria and describe newly identified rhizobia capable of nodulating edible legumes and legume trees. In 1990, there was only one bacterial species that was known to nodulate common bean worldwide (Rhizobium leguminosarum sv. phaseoli), one species that nodulated faba bean (Rhizobium leguminosarum sv. viciae), and two species that nodulated soybean (Bradyrhizobium japonicum and Rhizobium fredii). Today, nearly 14, 11, 6, 5, 5, 4, 3 and 2 species have been defined that are capable of nodulating common bean, soybean, cowpea, chickpea, peanut, lentils, faba bean and pea, respectively. The recent use of whole genome based taxonomy (genomotaxonomy) will surely change how we define this important group of bacteria. The identification of several rhizobial species that are able to nodulate and fix nitrogen with edible legumes may enhance the production of these crops and can compensate for worldwide deficiencies in human nutritional needs in the future.

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References

  • Achouak W, Christen R, Barakat M, Martel MH, Heulin T (1999) Burkholderia caribensis sp. nov., an exopolysaccharide-producing bacterium isolated from vertisol microaggregates in Martinique. Int J Syst Bacteriol 49:787–794

    Article  CAS  PubMed  Google Scholar 

  • Amarger N, Macheret V, Laguerre G (1997) Rhizobium gallicum sp. nov. and Rhizobium giardinii sp. nov., from Phaseolus vulgaris. Int J Syst Bacteriol 47:996–1006

    Article  CAS  PubMed  Google Scholar 

  • Ardley JK, Parker MA, De Meyer SE, Trengove RD, O’Hara GW, Reeve WG, Yates RJ, Dilworth MJ, Willems A, Howieson JG (2012) Microvirga lupini sp. nov., Microvirga lotononidis sp. nov. and Microvirga zambiensis sp. nov. are alphaproteobacterial root-nodule bacteria that specifically nodulate and fix nitrogen with geographically and taxonomically separate legume hosts. Int J Syst Evol Microbiol 62:2579–2588

    Article  CAS  PubMed  Google Scholar 

  • Berge O, Lodhi A, Brandelet G, Santaella C, Roncato MA, Christen R, Heulin T, Achouak W (2009) Rhizobium alamii sp. nov., an exopolysaccharide producing species isolated from legume and non-legume rhizospheres. Int J Syst Evol Microbiol 59:367–372

    Article  CAS  PubMed  Google Scholar 

  • Berrada H, Fikri-Benbrahim K (2014) Taxonomy of the Rhizobia: current perspectives. Brit Microbiol Res J 4:616–639

    Article  Google Scholar 

  • Bibi F, Chung EJ, Khan A, Jeon C, Chung YR (2012) Rhizobium halophytocola sp. nov., isolated from the root of a coastal dune plant. Int J Syst Evol Microbiol 62:1997–2003

    Article  CAS  PubMed  Google Scholar 

  • Boonsnongcheep P, Prathanturarug S, Takahashi Y, Matsumoto A (2016) Rhizobium puerariae sp. nov., an endophytic bacterium from the root nodules of medicinal plant Pueraria candollei var. candollei. Int J Syst Evol Microbiol 66:1236–1241

    Article  CAS  Google Scholar 

  • Casida JRLE (1982) Ensifer adhaerens gen. nov., sp. nov.: a bacterial predator of bacteria in Soil. Int J Syst Bacteriol 32:339–345

    Article  Google Scholar 

  • Chahboune R, Carro L, Peix A, Barrijal S, Velazquez E, Bedmar EJ (2011) Bradyrhizobium cytisi sp. nov., isolated from effective nodules of Cytisus villosus. Int J Syst Evol Microbiol 61:2922–2927

    Article  PubMed  Google Scholar 

  • Chahboune R, Carro L, Peix A, Ramirez-Bahena MH, Barrijal S, Velazquez E, Bedmare EJ (2012) Bradyrhizobium rifense sp. nov. isolated from effective nodules of Cytisus villosus grown in the Moroccan Rif. Syst Appl Microbiol 35:302–305

    Article  CAS  PubMed  Google Scholar 

  • Chang YL, Wang JY, Wang ET, Liu HC, Sui XH, Chen WX (2011) Bradyrhizobium lablabi sp. nov., isolated from effective nodules of Lablab purpureus and Arachis hypogaea. Int J Syst Evol Microbiol 61:2496–2502

    Article  PubMed  Google Scholar 

  • Chen WX, Li GS, Qi YL, Wang E, Yuan HL, Li JT (1991) Rhizobium huakuii sp. nov. isolated from the root of Astragalus sinucus. Int J Syst Bacteriol 41:275–280

    Article  Google Scholar 

  • Chen W, Wang E, Wang S, Li Y, Chen X, Li AY (1995) Characteristics of Rhizobium tianshanense sp. nov., a moderately and slowly growing root nodule bacterium isolated from an arid saline environment in Xinjiang, People’s Republic of China. Int J Syst Bacteriol 45:153–159

    Article  CAS  PubMed  Google Scholar 

  • Chen WX, Tan ZY, Gao JL, Li Y, Wang ET (1997) Rhizobium hainanense sp. nov., isolated from tropical legumes. Int J Syst Bacteriol 47:870–873

    Article  CAS  PubMed  Google Scholar 

  • Chen WM, Laevens S, Lee TM, 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

    Article  CAS  PubMed  Google Scholar 

  • Chen WM, James EK, Coenye T, Chou JH, Barrios E, de Faria SM, Elliott GN, Sheu SY, Sprent JI, Vandamme P (2006) Burkholderia mimosarum sp. nov., isolated from root nodules of Mimosa spp. from Taiwan and South America. Int J Syst Evol Microbiol 56:1847–1851

    Article  CAS  PubMed  Google Scholar 

  • Chen WM, de Faria SM, James EK, Elliott GN, Lin KY, Chou JH, Sheu SY, Cnockaert M, Sprent JI, Vandamme P (2007) Burkholderia nodosa sp. nov., isolated from root nodules of the woody Brazilian legumes Mimosa bimucronata and Mimosa scabrella. Int J Syst Evol Microbiol 57:1055–1059

    Article  CAS  PubMed  Google Scholar 

  • Chen WM, de Faria SM, Chou JH, James EK, Elliott GN, Sprent JI, Bontemps C, Young JP, Vandamme P (2008) Burkholderia sabiae sp. nov., isolated from root nodules of Mimosa caesalpiniifolia. Int J Syst Evol Microbiol 58:2174–2179

    Article  CAS  PubMed  Google Scholar 

  • Chen WM, Zhu WF, Bontemps CJ, Young PW, Wei GH (2010) Mesorhizobium alhagi sp. nov., isolated from wild Alhagi sparsifolia in north-western China. Int J Syst Evol Microbiol 60:958–962

    Article  CAS  PubMed  Google Scholar 

  • Chen WM, Zhu WF, Bontemps C, Young JP, Wei GH (2011) Mesorhizobium camelthorni sp. nov., isolated from Alhagi sparsifolia. Int J Syst Evol Microbiol 61:574–579

    Article  CAS  PubMed  Google Scholar 

  • Chen W, Sheng XF, He LY, Huang Z (2015) Rhizobium yantingense sp. nov., a mineral-weathering bacterium. Int J Syst Evol Microbiol 65:412–417

    Article  CAS  PubMed  Google Scholar 

  • Coenye T, Laevens S, Willems A, Ohlen M, Hannant W, Govan JRW, Gillis M, Falsen E, Vandamme P (2001) Burkholderia fungorum sp. nov. and Burkholderia caledonica sp. nov., two new species isolated from the environment, animals and human clinical samples. Int J Syst Evol Microbiol 51:1099–1107

    Article  CAS  PubMed  Google Scholar 

  • da Silva K, Florentino LA, da Silva KB, de Brandt E, Vandamme P, de Souza Moreir FM (2012) Cupriavidus necator isolates are able to fix nitrogen in symbiosis with different legume species. Syst Appl Microbiol 35:175–182

    Article  PubMed  CAS  Google Scholar 

  • da Silva K, De Meyer SE, Rouws LFM, Farias Eliane NC, dos Santos MAO, O’Hara G, Ardley JK, Willems A, Pitard RM, Zilli JE (2014) Bradyrhizobium ingae sp. nov., isolated from effective nodules of Inga laurina grown in Cerrado soil. Int J Syst Evol Microbiol 64:3395–3401

    Article  PubMed  CAS  Google Scholar 

  • Dall’Agnol RF, Ribeiro RA, Ormeno-Orrillo E, Rogel MA, Delamuta JRM, Andrade DS, Esperanza-Martinez R, Mariangela H (2013) Rhizobium freirei sp. nov., a symbiont of Phaseolus vulgaris that is very effective at fixing nitrogen. Int J Syst Evol Microbiol 63:4167–4173

    Article  PubMed  Google Scholar 

  • Dall’Agnol RF, Ribeiro RA, Delamuta JRM, Ormeno-Orrillo E, Rogel MA, Andrade DS, Martıinez-Romero E, Hungria M (2014) Rhizobium paranaense sp. nov., an effective N 2 -fixing symbiont of common bean (Phaseolus vulgaris L.) with broad geographical distribution in Brazil. Int J Syst Evol Microbiol 64:3222–3229

    Article  PubMed  Google Scholar 

  • De Bruijn FJ (1992) Use of repetitive (repetitive extragenic palindromic and enterobacterial repetitive intergeneric consensus) sequences and the polymerase chain reaction to fingerprint the genomes of Rhizobium meliloti isolates and other soil bacteria. Appl Environ Microbiol 58:2180–2187

    PubMed  PubMed Central  Google Scholar 

  • de Lajudie P, Willems A, Pot B, Dewettinck D, Maestrojuan G, Neyra M, Collins MD, 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

    Article  Google Scholar 

  • de Lajudie P, Laurent-Fulele E, WiIlems A, Torck U, Coopman R, Colin MD, Kersters K, Dreyfuslt B, Gillis M (1998a) Allorhizobium undicola gen. nov., sp. nov., nitrogen-fixing bacteria that efficiently nodulate Neptunia natans in Senegal. Int J Syst Bacteriol 48:1277–1290

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • De Meyer SE, Cnockaert M, Ardley JK, Maker G, Yates R, Howieson JC, Vandamme P (2013) Burkholderia sprentiae sp. nov., isolated from Lebeckia ambigua root nodules. Int J Syst Evol Microbiol 63:3950–3957

    Article  PubMed  CAS  Google Scholar 

  • De Meyer S, Cnockaert M, Ardley JK, Ben-Erik VW, Vandamme PA, Howieson JG (2014) Burkholderia dilworthii sp. nov., isolated from Lebeckia ambigua root nodules from South Africa. Int J Syst Evol Microbiol 64:1090–1095

    Article  PubMed  CAS  Google Scholar 

  • De Meyer SE, Tan HW, Heenan PB, Andrews M, Willems A (2015) Mesorhizobium waimense sp. nov. isolated from Sophora longicarinata root nodules and Mesorhizobium cantuariense sp. nov. isolated from Sophora microphylla root nodules. Int J Syst Evol Microbiol 65:3419–3426

    Article  PubMed  CAS  Google Scholar 

  • De Meyer SE, Tan HW, Andrews M, Heenan PB, Willem A (2016) Mesorhizobium calcicola sp. nov., Mesorhizobium waitakense sp. nov., Mesorhizobium sophorae sp. nov., Mesorhizobium newzealandense sp. nov. and Mesorhizobium kowhaii sp. nov. isolated from Sophora root nodules in New Zealand. Int J Syst Evol Microbiol 66:786–795

    Article  CAS  Google Scholar 

  • Degefu T, Wolde-Meskel E, Liu B, Cleenwerck I, Willems A, Frostegard A (2013) Mesorhizobium shonense sp. nov., Mesorhizobium hawassense sp. nov. and Mesorhizobium abyssinicae sp. nov., isolated from root nodules of different agroforestry legume trees. Int J Syst Evol Microbiol 63:1746–1753

    Article  CAS  PubMed  Google Scholar 

  • Delamuta JRM, Ribeiro RA, Ormeno-Orrillo E, Melo IS, Martinez-Romero E, Hungria M (2013) Polyphasic evidence supporting the reclassification of Bradyrhizobium japonicum group Ia strains as Bradyrhizobium diazoefficiens sp. nov. Int J Syst Evol Microbiol 63:3342–3351

    Article  CAS  PubMed  Google Scholar 

  • Delamuta JRM, Ribeiro RA, Ormeno-Orrillo E, Parma MM, Melo IS, Martıinez-Romero R, Hungria M (2015) Bradyrhizobium tropiciagri sp. nov. and Bradyrhizobium embrapense sp. nov., nitrogen-fixing symbionts of tropical forage legumes. Int J Syst Evol Microbiol 65:4424–4433

    Article  CAS  PubMed  Google Scholar 

  • Diange EA, Lee SS (2013) Rhizobium halotolerans sp. nov., isolated from Chloroethylenes contaminated soil. Curr Microbiol 66:599–605

    Article  CAS  PubMed  Google Scholar 

  • Dreyfus B, Garcia JL, 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

    Article  CAS  Google Scholar 

  • Duran D, Rey L, Mayo J, Zuniga-Davila D, Imperial J, Ruiz-Argueso T, Martinez-Romero E, Ormeno-Orrillo E (2014) Bradyrhizobium paxllaeri sp. nov. and Bradyrhizobium icense sp. nov., nitrogen-fixing rhizobial symbionts of Lima bean (Phaseolus lunatus L.) in Peru. Int J Syst Evol Microbiol 64:2072–2078

    Article  PubMed  Google Scholar 

  • Durán D, Rey L, Navarro A, Busquets A, Imperial J, Ruiz-Argüeso T (2014) Bradyrhizobium valentinum sp. nov., isolated from effective nodules of Lupinus mariae-josephae, a lupine endemic of basic-lime soils in Eastern Spain. Syst Appl Microbiol 37:336–341

    Article  PubMed  CAS  Google Scholar 

  • Eckhardt MM, Baldwin IL, Fred EB (1931) Studies of the root-nodule organism of Lupinus. J Bacteriol 21:273–285

    CAS  PubMed  PubMed Central  Google Scholar 

  • Finan TM (2002) Evolving insights: symbiosis islands and horizontal gene transfer. J Bacteriol 184:2855–2856

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Flores-Félix JD, Carro L, Velázquez E, Valverde Á, Castillo CE, García-Fraile P, Rivas R (2013) Phyllobacterium endophyticum sp. nov., isolated from nodules of Phaseolus vulgaris. Int J Syst Evol Microbiol 63:821–826

    Article  PubMed  CAS  Google Scholar 

  • Frank B (1889) Ueber die Pilzsymbiose der Leguminosen. Berichte der Deutschen Botanishen Gesellschaft 7:332–346

    Google Scholar 

  • Gao JL, Turner SL, Ka FL, Wang ET, Tan ZY, Qiu YH, Gu J, Terefework ZJ, Young PW, Lindstrom K, Chen WX (2004) Mesorhizobium septentrionale sp. nov. and Mesorhizobium temperatum sp. nov., isolated from Astragalus adsurgens growing in the northern regions of China. Int J Syst Evol Microbiol 54:2003–2012

    Article  CAS  PubMed  Google Scholar 

  • Garcia-Fraile P, Rivas R, Willems A, Peix A, Martens M, Martinez-Molina E, Mateos PF, Velazquez E (2007) Rhizobium cellulosilyticum sp. nov., isolated from sawdust of Populus alba. Int J Syst Evol Microbiol 57:844–848

    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

    Article  CAS  PubMed  Google Scholar 

  • Graham PH, Sadowsky MJ, Keyser HH, Barnet YM, Bradley RS, Cooper JE, De Ley DJ, Jarvis BDW, Roslycky EB, Strijdom BW, Young JPW (1991) Proposed minimal standards for the description of new genera and species of root- and stem-nodulating Bacteria. Int J Syst Bacteriol 41:582–587

    Article  Google Scholar 

  • Gronemeyer JL, Chimwamurombe P, Reinhold-Hurek B (2015a) Bradyrhizobium subterraneum sp. nov., a symbiotic nitrogen-fixing bacterium from root nodules of groundnuts. Int J Syst Evol Microbiol 65:3241–3247

    Article  PubMed  CAS  Google Scholar 

  • Gronemeyer JL, Hurek T, Reinhold-Hurek B (2015b) Bradyrhizobium kavangense sp. nov., a symbiotic nitrogen-fixing bacterium from root nodules of traditional Namibian pulses. Int J Syst Evol Microbiol 65:4886–4894

    Article  CAS  Google Scholar 

  • Gronemeyer JL, Hurek T, Bunger W, Reinhold-Hurek B (2016) Bradyrhizobium vignae sp. nov., a nitrogen-fixing symbiont isolated from effective nodules of Vigna and Arachis. Int J Syst Evol Microbiol 66:62–69

    Article  PubMed  CAS  Google Scholar 

  • Gu CT, Wang ET, Tian CF, Han TX, Chen WF, Sui XH, Chen WX (2008) Rhizobium miluonense sp. nov., a symbiotic bacterium isolated from Lespedeza root nodules. Int J Syst Evol Microbiol 58:1364–1368

    Article  CAS  PubMed  Google Scholar 

  • Gu T, Sun LN, Zhang J, Sui XH, Li SP (2014) Rhizobium flavum sp. nov., a triazophos-degrading bacterium isolated from soil under the long-term application of triazophos. Int J Syst Evol Microbiol 64:2017–2022

    Article  CAS  PubMed  Google Scholar 

  • Guan SH, Chen WF, Wang ET, Lu YL, Yan XR, Zhang XX, Chen WX (2008) Mesorhizobium caraganae sp. nov., a novel rhizobial species nodulated with Caragana spp. in China. Int J Syst Evol Microbiol 58:2646–2653

    Article  CAS  PubMed  Google Scholar 

  • Gubry-Rangin C, Béna G, Cleyet-Mare JC, Brune B (2013) Definition and evolution of a new symbiovar, sv. rigiduloides, among Ensifer meliloti efficiently nodulating Medicago species. Syst Appl Microbiol 36:490–496

    Article  PubMed  Google Scholar 

  • Guerrouj K, Ruiz-Diez B, Chahboune R, Ramirez-Bahena MH, Abdelmoumen H, Quinones MA, El Idrissi MM, Velazquez E, Fernandez-Pascual M, Bedmar EJ, Peixd A (2013) Definition of a novel symbiovar (sv. retamae) within Bradyrhizobium retamae sp. nov., nodulating Retama sphaerocarpa and Retama monosperma. Syst Appl Microbiol 36:218–223

    Article  CAS  PubMed  Google Scholar 

  • Gyaneshwar P, Hirsch AM, Moulin L, Chen WM, Elliott GN, Bontemps C, los Santos PE, Gross E, dos Reis FB, Sprent JI, Young JPW, James EK (2011) Legume-nodulating betaproteobacteria: diversity, host Range, and future prospects. Molec Plant Microbe Interact 24:1276–1288

    Article  CAS  Google Scholar 

  • Han T, Han LL, Wu LJ, Chen WF, Sui XH, Gu JG, Wang ET, Chen WX (2008a) Mesorhizobium gobiense sp. nov. and Mesorhizobium tarimense sp. nov., isolated from wild legumes growing in desert soils of Xinjiang, China. Int J Syst Evol Microbiol 58:2610–2618

    Article  CAS  PubMed  Google Scholar 

  • Han TX, Wang ET, Wu LJ, Chen WF, Gu JG, Gu CT, Tian CF, Chen WX (2008b) Rhizobium multihospitium sp. nov., isolated from multiple legume species native of Xinjiang, China. Int J Syst Evol Microbiol 58:1693–1699

    Article  CAS  PubMed  Google Scholar 

  • Hou BC, Wang ET, Li Y Jr, Jia RZ, Chen WF, Gao Y, Dong RJ, Chen WX (2009) Rhizobium tibeticum sp. nov., isolated from Trigonella archiducisnicoli (Sirj) Vassilcz. Int J Syst Evol Microbiol 59:3051–3057

    Article  CAS  PubMed  Google Scholar 

  • Huber TA, Agarwal AK, Keister DL (1984) Extracellular polysaccharide composition, explanta nitrogenase activity, and DNA homology in Rhizobium japonicum. J Bacteriol 158:1168–1171

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hunter WJ, Kuykendall LD, Manter DK (2007) Rhizobium selenireducens sp. nov.: a selenite-reducing a-Proteobacteria isolated from a bioreactor. Curr Microbiol 55:455–460

    Article  CAS  PubMed  Google Scholar 

  • Ishii S, Sadowsky MJ (2009) Applications of the rep-PCR DNA fingerprinting technique to study microbial diversity, ecology and evolution. Environ Microbiol 11:733–740

    Article  CAS  PubMed  Google Scholar 

  • Islam MS, Kawasaki H, Muramatsu Y, Nakagawa Y, Seki T (2008) Bradyrhizobium iriomotense sp. nov., isolated from a tumor-like root of the legume Entada koshunensis from Iriomote Island in Japan. Bioscience. Biotechnol Biochem 72:1416–1429

    Article  CAS  Google Scholar 

  • Jarvis BDW, Pankhurst CE, Patel JJ (1982) Rhizobium loti, a new species of legume root nodule bacteria. Int J Syst Bacteriol 32:378–380

    Article  Google Scholar 

  • Jarvis BDW, Van Berkum P, Chen WX, Nour SM, Fernandez MP, Cleyet-Marel JC, Gillis M (1997) Transfer of Rhizobium loti, Rhizobium huakuii, Rhizobium ciceri, Rhizobium mediterraneum, and Rhizobium tianshanense to Mesorhizobium gen. nov. Int J Syst Bacteriol 47:895–898

    Article  Google Scholar 

  • Jiao YS, Yan H, Ji ZJ, Liu YH, Sui XH, Zhang XX, Wang ET, Chen WX, Chen WF (2015) Phyllobacterium sophorae sp. nov., a symbiotic bacterium isolated from root nodules of Sophora flavescens. Int J Syst Evol Microbiol 65:399–406

    Article  CAS  PubMed  Google Scholar 

  • Jordan DC (1982) Transfer of Rhizobium japonicum Buchanan 1980 to Bradyrhizobium gen. nov., a genus of slow-growing, root nodule bacteria from leguminous plants. Int J Syst Bacteriol 32:136–139

    Article  Google Scholar 

  • Jordan DC (1984) Family III. Rhizobiaceae Conn 1938. In: Krieg NR, Holt JC (eds) Bergey’s manual of systematic bacteriology 321AL, vol 1. The Williams and Wilkins Co., Baltimore, pp 234–236

    Google Scholar 

  • Jourand P, Giraud E, Bena G, Sy A, Willems A, Gillis M, Dreyfus B, de Lajudie P (2004) Methylobacterium nodulans sp. nov., for a group of aerobic, facultatively methylotrophic, legume root-nodule-forming and nitrogen-fixing bacteria. Int J Syst Evol Microbiol 54:2269–2273

    Article  CAS  PubMed  Google Scholar 

  • Kaiya S, Rubaba O, Yoshida N, Yamada T, Hiraishi A (2012) Characterization of Rhizobium naphthalenivorans sp. nov. with special emphasis on aromatic compound degradation and multilocus sequence analysis of housekeeping genes. J Gen Appl Microbiol 58:211–224

    Article  CAS  PubMed  Google Scholar 

  • Kaur J, Verma M, La R (2011) Rhizobium rosettiformans sp. nov., isolated from a hexachlorocyclohexane dump site, and reclassification of Blastobacter aggregates Hirsch and Muller 1986 as Rhizobium aggregatum comb. nov. Int J Syst Evol Microbiol 61:1218–1225

    Article  CAS  PubMed  Google Scholar 

  • Kesari V, Ramesh AM, Rangan L (2013) Rhizobium pongamiae sp. nov. from root nodules of Pongamia pinnata. BioMed Res Int Article ID 165198

  • Khalid R, Zhang YJ, Ali S, Sui XH, Zhang XX, Amara U, Chen WX, Rifat H (2014) Rhizobium pakistanensis sp. nov., isolated from groundnut (Arachis hypogaea) nodules grown in rainfed Pothwar, Pakistan. Antonie Van Leeuwenhoek 107:281–290

    Article  PubMed  CAS  Google Scholar 

  • Kimes NE, López-Pérez M, Flores-Félix JD, Ramírez-Bahena MH, Igual JM, Peix A, Rodriguez-Valera F, Velázquez E (2015) Pseudorhizobium pelagicum gen. nov., sp. nov. isolated from a pelagic Mediterranean zone. Syst Appl Microbiol 38:293–299

    Article  PubMed  Google Scholar 

  • Kittiwongwattana C, Thawai C (2013) Rhizobium paknamense sp. nov., isolated from lesser duckweeds (Lemna aequinoctialis). Int J Syst Evol Microbiol 63:3823–3828

    Article  CAS  PubMed  Google Scholar 

  • Kittiwongwattana C, Thawai C (2014) Rhizobium lemnae sp. nov., a bacterial endophyte of Lemna aequinoctialis. Int J Syst Evol Microbiol 64:2455–2460

    Article  CAS  PubMed  Google Scholar 

  • Kuykendall LD, Saxena B (1992) Genetic diversity in Bradyrhizobium japonicum Jordan 1982 and a proposal for Bradyrhizobium elkanii sp. nov. Can J Microbiol 38:501–505

    Article  CAS  Google Scholar 

  • Lang E, Schumann P, Adler S, Spröer C, Sahin N (2013) Azorhizobium oxalatiphilum sp. nov., and emended description of the genus Azorhizobium. Int J Syst Evol Microbiol 63:1505–1511

    Article  CAS  PubMed  Google Scholar 

  • Li YH, Wang R, Zhang XX, Young JPW, Wang ET, Sui XH, Chen WX (2015) Bradyrhizobium guangdongense sp. nov. and Bradyrhizobium guangxiense sp. nov., isolated from effective nodules of peanut in China. Int J Syst Evol Microbiol 65:4655–4661

    Article  CAS  PubMed  Google Scholar 

  • Lin DX, Wang ET, Tang H, Han TX, He YR, Guan SH, Chen WX (2008) Shinella kummerowiae sp. nov., a symbiotic bacterium isolated from root nodules of the herbal legume Kummerowia stipulacea. Int J Syst Evol Microbiol 58:1409–1413

    Article  CAS  PubMed  Google Scholar 

  • Lin DX, Chen WF, Wang FQ, Hu D, Wang ET, Sui XH, Chen WX (2009) Rhizobium mesosinicum sp. nov., isolated from root nodules of three different legumes. Int J Syst Evol Microbiol 59:1919–1923

    Article  PubMed  Google Scholar 

  • Lin SY, Hsu YH, Liu YC, Hung MH, Hameed A, Lai WA, Yen WS, Young CC (2014) Rhizobium straminoryzae sp. nov., isolated from the surface of rice straw. Int J Syst Evol Microbiol 64:2962–2968

    Article  CAS  PubMed  Google Scholar 

  • Lindstrom K (1989) Rhizobium galegae, a new species of legume root nodule bacteria. Int J Syst Bacteriol 39:365–367

    Article  Google Scholar 

  • Liu TY Jr, Liu YL, Sui XX, Zhang XH, Wang XX, Chen ETWX, Chen WF, Puławska J (2012) Rhizobium cauense sp. nov., isolated from root nodules of the herbaceous legume Kummerowia stipulacea grown in campus lawn soil. Syst Appl Microbiol 35:415–420

    Article  CAS  PubMed  Google Scholar 

  • Lloret L, Ormeno-Orrillo E, Rincon R, Martinez-Romero J, Rogel-Hernandez MA, Martinez-Romero E (2007) Ensifer mexicanus sp. nov. a new species nodulating Acacia angustissima (Mill.) Kuntze in Mexico. Syst Appl Microbiol 30:280–290

    Article  CAS  PubMed  Google Scholar 

  • Lopez-Lopez A, Rogel MA, Ormeno-Orrillo E, Martinez-Romero J, Martinez-Romero E (2010) Phaseolus vulgaris seed-borne endophytic community with novel bacterial species such as Rhizobium endophyticum sp. nov. Syst Appl Microbiol 33:322–327

    Article  PubMed  Google Scholar 

  • Lopez-Lopez A, Rogel-Hernandez MA, Barois I, Ortiz-Ceballos AL, Martinez J, Ormeno-Orrillo E, Martinez-Romero E (2012) Rhizobium grahamii sp. nov. from nodules of Dalea termatea, Leucocephala and clitoria termatea and Rhizobium mesoamericanum sp. nov. from nodules of Phaseolus vulgaris, Siratro, cowpea and Mimosa pundica. Int J Syst Evol Microbiol 62:2264–2271

    Article  CAS  PubMed  Google Scholar 

  • Lu YL, Chen WF, Wang ET, Han LL, Zhang XX, Chen WX, Han SZ (2009a) Mesorhizobium shangrilense sp. nov., isolated from root nodules of Caragana species. Int J Syst Evol Microbiol 59:3012–3018

    Article  CAS  PubMed  Google Scholar 

  • Lu YL, Chen WF, Han LL, Wang ET, Chen WX (2009b) Rhizobium alkalisoli sp. nov., isolated from Caragana intermedia growing in saline-alkaline soils in the north of China. Int J Syst Evol Microbiol 59:3006–3011

    Article  CAS  Google Scholar 

  • Lu JK, Dou YJ, Zhu YJ, Wang SK, Sui XH, Kang LH (2014) Bradyrhizobium ganzhouense sp. nov., an effective symbiotic bacterium isolated from Acacia melanoxylon R. Br. nodules. Int J Syst Evol Microbiol 64:1900–1905

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mantelin S, Saux MFL, Zakhia F, Bena G, Bonneau S, Jeder H, de Lajudie P, Cleyet-Mare JC (2006) Emended description of the genus Phyllobacterium and description of four novel species associated with plant roots: Phyllobacterium bourgognense sp. nov., Phyllobacterium ifriqiyense sp. nov., Phyllobacterium leguminum sp. nov. and Phyllobacterium brassicacearum sp. nov. Int J Syst Evol Microbiol 56:827–839

    Article  CAS  PubMed  Google Scholar 

  • Martinez-Hidalgo P, Ramirez-Bahena MH, Flores-Felix JD, Rivas R, Igual JM, Mateos PF, Martinez-Molina E, Leon-Barrios M, Velazquez E (2015) Revision of the taxonomic status of type strains of Mesorhizobium loti and reclassification of strain USDA 3471T as the type strain of Mesorhizobium erdmanii sp. nov. and ATCC 33669T as the type strain of Mesorhizobium jarvisii sp. nov. Int J Syst Evol Microbiol 65:1703–1708

    Article  CAS  PubMed  Google Scholar 

  • Martinez-Romero E, Segovia L, Mercante FM, Franco AA, Graham P, Pardo MA (1991) Rhizobium tropici, a novel species nodulating Phaseolus vulgaris L. beans and Leucaena sp. trees. Int J Syst Bacteriol 41:417–426

    Article  CAS  PubMed  Google Scholar 

  • Mavengere NR, Ellis AG, Le Roux JJ (2014) Burkholderia aspalathi sp. nov., isolated from root nodules of the South African legume Aspalathus abietina Thunb. Int J Syst Evol Microbiol 64:1906–1912

    Article  PubMed  Google Scholar 

  • Maynaud G, Willems A, Soussou S, Vidal C, Mauré L, Moulin L, Cleyet-Marel JC, Brunelc B (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

    Article  CAS  PubMed  Google Scholar 

  • Merabet C, Martens M, Mahdhi M, Zakhia F, Sy A, Le Roux C, Domergue O, Coopman R, Bekki A, Mars M, Willems A, de Lajudie P (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

    Article  CAS  PubMed  Google Scholar 

  • Mergaert P, Van Montagu M, Holsters M (1997) Molecular mechanisms of Nod factor diversity. Mol Microbiol 25:811–817

    Article  CAS  PubMed  Google Scholar 

  • Mnsari B, Liu TY, Saidi S, Chen WF, Chen XW, Zhang XX, Mahmdi R (2014) Rhizobium azibense sp. nov., a nitrogen fixing bacterium isolated from root-nodules of Phaseolus vulgaris. Int J Syst Evol Microbiol 64:1501–1506

    Article  CAS  Google Scholar 

  • Molouba F, Lorquin J, Willems A, Hoste B, Giraud E, Dreyfus B, Gillis M, de Lajudie P, Masson-Boivin C (1999) Photosynthetic Bradyrhizobia from Aeschynomene spp. are specific to stem-nodulated species and form a separate 16S Ribosomal DNA restriction fragment length polymorphism group. Appl Environ Microbiol 65:3084–3094

    CAS  PubMed  PubMed Central  Google Scholar 

  • Moreira de Souza FM, Cruz L, de Faria SM, Marsh T, Martinez-Romero E, de Pedrosa OF, Pitard RM, Young JP (2006) Azorhizobium doebereinerae sp. nov. microsymbiont of Sesbania virgata (Caz.) Pers. Syst Appl Microbiol 29:197–206

    Article  CAS  Google Scholar 

  • Mousavi SA, Willems A, Nesme X, de Lajudie P, Lindström K (2015) Revised phylogeny of Rhizobiaceae: proposal of the delineation of Pararhizobium gen. nov., and 13 new species combinations. Syst Appl Microbiol 38:84–90

    Article  PubMed  Google Scholar 

  • Nakatsukasa H, Uchiumi T, Kucho K, Suzuki A, Higashi S, Abe M (2008) Transposon mediation allows a symbiotic plasmid of Rhizobium leguminosarum bv. trifolii to become a symbiosis island in Agrobacterium and Rhizobium. J Gen Appl Microbiol 54:107–118

    Article  CAS  PubMed  Google Scholar 

  • Nandasena KG, O’Hara GW, Tiwari RP, Willems A, Howieson JG (2009) Mesorhizobium australicum sp. nov. and Mesorhizobium opportunistum sp. nov., isolated from Biserrula pelecinus L. in Australia. Int J Syst Evol Microbiol 59:2140–2147

    Article  CAS  PubMed  Google Scholar 

  • Nick G, de Lajudie P, Eardly BD, Suomalainen S, Paulin L, Zhang XP, Gillis M, Lindström K (1999) Sinorhizobium arboris sp. nov. and Sinorhizobium kostiense sp. nov., isolated from leguminous trees in Sudan and Kenya. Int J Syst Bacteriol 49:1359–1368

    Article  CAS  PubMed  Google Scholar 

  • Nour SM, Fernandez MP, Normand P, Cleyet-Marel JC (1994) Rhizobium ciceri sp. nov., consisting of strains that nodulate chickpea (Cicer arietinum L.). Int J Syst Bacteriol 44:511–522

    Article  CAS  PubMed  Google Scholar 

  • Nour SM, Cleyet-Marel JC, Normand P, Fernandez MP (1995) Genomic Heterogeneity of strains nodulating Chickpeas (Cicer arietinum L.) and description of Rhizobium mediterraneum sp. nov. Int J Syst Evol Microbiol 45:640–648

    CAS  Google Scholar 

  • Ogasawara M, Suzuki T, Mutoh I, Annapurna K, Arora NK, Nishimura Y, Maheshwari DK (2003) Sinorhizobium indiaense sp. nov. and Sinorhizobium abri sp. nov. isolated from tropical legumes, Sesbania rostrata and Abrus precatorius, respectively. Symbiosis 34:53–68

    Google Scholar 

  • Ormeno-Orrillo E, Servín-Garciduenas L, Rogel MA, González V, Peralta H, Mora J, Martinez-Romero J, Martínez-Romero E (2015) Taxonomy of rhizobia and agrobacteria from the Rhizobiaceae family in light of genomics. Syst Appl Microbiol 38:287–291

    Article  PubMed  Google Scholar 

  • Panday D, Schumann P, Das SK (2011) Rhizobium pusense sp. nov., isolated from the rhizosphere of chickpea (Cicer arietinum L.). Int J Syst Evol Microbiol 61:2632–2639

    Article  PubMed  Google Scholar 

  • Peix A, Ramirez-Bahena MH, Flores-Felix JD, de la Vega PA, Rivas R, Mateos PF, Igual JM, Martinez-Molina E, Trujillo ME, Velazquez E (2015) Revision of the taxonomic status of the species Rhizobium lupini and reclassification as Bradyrhizobium lupini comb. nov. Int J Syst Evol Microbiol 65:1213–1219

    Article  CAS  PubMed  Google Scholar 

  • Peng G, Yuan Q, Li H, Zhang W, Tan Z (2008) Rhizobium oryzae sp. nov., isolated from the wild rice Oryza alta. Int J Syst Evol Microbiol 58:2158–2163

    Article  CAS  PubMed  Google Scholar 

  • Pongsilp N, Neung T, Achara N, Natakorn B, Sadowsky MJ (2002) Genetic structure of indigenous non-nodulating and nodulating populations of Bradyrhizobium in soil from Thailand. Symbiosis 33:39–58

    CAS  Google Scholar 

  • Puławska J, Willems A, De Meyer SE, Sule S (2012a) Rhizobium nepotum sp. nov. isolated from tumors on different plant species. Syst Appl Microbiol 35:215–220

    Article  PubMed  Google Scholar 

  • Puławska J, Willems A, Sobiczewski P (2012b) Rhizobium skierniewicense sp. nov., isolated from tumours on chrysanthemum and cherry plum. Int J Syst Evol Microbiol 62:895–899

    Article  PubMed  CAS  Google Scholar 

  • Puławska J, Kuzmanović N, Willems A, Pothier JF (2016) Pararhizobium polonicum sp. nov. isolated from tumors on stone fruit rootstocks. Syst Appl Microbiol 39:164–169

    Article  PubMed  Google Scholar 

  • Qin W, Deng ZS, Xu L, Wang NN, Wei GH (2012) Rhizobium helanshanense sp. nov., a bacterium that nodulates Sphaerophysa salsula (Pall.) DC. in China. Arch Microbiol 194:371–378

    Article  CAS  PubMed  Google Scholar 

  • Quan ZX, Bae HS, Baek JH, Chen WF, Im WT, Lee ST (2005) Rhizobium daejeonense sp. nov. isolated from a cyanide treatment bioreactor. Int J Syst Evol Microbiol 55:2543–2549

    Article  CAS  PubMed  Google Scholar 

  • Radl V, Simões-Araújo JL, Leite J, Passos SR, Martins LM, Xavier GR, Rumjanek NG, Baldani JI, Zilli JE (2014) Microvirga vignae sp. nov., a root nodule symbiotic bacterium isolated from cowpea grown in semi-arid Brazil. Int J Syst Evol Microbiol 64:725–7230

    Article  PubMed  Google Scholar 

  • Ramana CV, Parag B, Girija KR, Ram BR, Ramana VV, Sasikala C (2013) Rhizobium subbaraonis sp. nov., an endolithic bacterium isolated from beach sand. Int J Syst Evol Microbiol 63:581–585

    Article  CAS  PubMed  Google Scholar 

  • Ramirez-Bahena MH, Garcia-Fraile P, Peix A, Valverde A, Rivas R, Igual JM, Mateos PF, Martinez-Molina E, Velazquez E (2008) Revision of the taxonomic status of the species Rhizobium leguminosarum (Frank 1879) Frank 1889AL, Rhizobium phaseoli Dangeard 1926AL and Rhizobium trifolii Dangeard 1926AL. R. trifolii is a later synonym of R. leguminosarum. Reclassification of the strain R. leguminosarum DSM 30132 (5NCIMB 11478) as Rhizobium pisi sp. nov. Int J Syst Evol Microbiol 58:2484–2490

    Article  CAS  PubMed  Google Scholar 

  • Ramirez-Bahena MH, Peix A, Rivas R, Camacho M, Rodriguez-Navarro DN, Mateos PF, Martinez-Molina E, Willems A, Velazquez E (2009) Bradyrhizobium pachyrhizi sp. nov. and Bradyrhizobium jicamae sp. nov., isolated from effective nodules of Pachyrhizus erosus. Int J Syst Evol Microbiol 59:1929–1934

    Article  PubMed  Google Scholar 

  • Ramirez-Bahena MH, Hernandez M, Peix A, Velazques E, Leon-Barrios M (2012) Mesorhizobial strains nodulating Anagyris latifolia and Lotus berthelotii inTamadaya ravine (Tenerife, Canary Islands) are two symbiovars of the same species, Mesorhizobium tamadayense sp. nov. Syst Appl Microbiol 35:334–341

    Article  PubMed  Google Scholar 

  • Ramirez-Bahena MH, Chahboune R, Peix A, Velazquez E (2013) Reclassification of Agromonas oligotrophica into the genus Bradyrhizobium as Bradyrhizobium oligotrophicum comb. nov. Int J Syst Evol Microbiol 63:1013–1016

    Article  PubMed  Google Scholar 

  • Rashid MH, Young JP, Everall I, Clercx P, Willems A, Braun MS, Wink M (2015) Average nucleotide identity of genome sequences supports the description of Rhizobium lentis sp. nov., Rhizobium bangladeshense sp. nov. and Rhizobium binae sp. nov. from lentil (Lens culinaris) nodules. Int J Syst Evol Microbiol 65:3037–3045

    Article  PubMed  CAS  Google Scholar 

  • Rasolomampianina R, Bailly X, Fetiarison R, Rabevohitra R, Béna G, Ramaroson I, Raherimandimby M, Moulin I, de lajudie P, Dreyfus B, Avarre JC (2005) Nitrogen-fixing nodules from rose wood legume trees (Dalbergia spp.) endemic to Madagascar host seven different genera belonging to alpha - and beta-Proteobacteria. Mol Ecol 14:4135–4146

    Article  CAS  PubMed  Google Scholar 

  • Ren DW, Chen FW, Sui XH, Wang ET, Chen WX (2011a) Rhizobium vignae sp. nov., a symbiotic bacterium isolated from multiple legume species. Int J Syst Evol Microbiol 61:580–586

    Article  CAS  Google Scholar 

  • Ren DW, Wang ET, Chen WF, Sui XH, Zhang XX, Liu HC, Chen WX (2011b) Rhizobium herbae sp. nov. and Rhizobium giardinii-related bacteria, minor microsymbionts of various wild legumes in China. Int J Syst Evol Microbiol 61:1912–1920

    Article  CAS  Google Scholar 

  • Ribeiro RA, Barcellos FG, Thompson FL, Hungria M (2009) Multilocus sequence analysis of Brazilian Rhizobium microsymbionts of common bean (Phaseolus vulgaris L.) reveals unexpected taxonomic diversity. Res Microbiol 160:297–306

    Article  CAS  PubMed  Google Scholar 

  • Ribeiro RA, Rogel MA, Lopez-Lopez A, Ormeno-Orrillo E, Barcellos FG, Martinez J, Thompson FL, Martinez-Romero E, Hungria M (2012) Reclassification of Rhizobium tropici type A strains as Rhizobium leucaenae sp. nov. Int J Syst Evol Microbiol 62:1179–1184

    Article  PubMed  Google Scholar 

  • Rincón-Rosales R, Villalobos-Escobedo JM, Rogel MA, Martinez J, Ormeño-Orrillo E, Martínez-Romero E (2013) Rhizobium calliandrae sp. nov., Rhizobium mayense sp. nov. and Rhizobium jaguaris sp. nov., rhizobial species nodulating the medicinal legume Calliandra grandiflora. Int J Syst Evol Microbiol 63:3423–3429

    Article  PubMed  CAS  Google Scholar 

  • Rivas R, Willems A, Subba-Rao NS, Mateos PF, Dazzo FB, Kroppenstedt RM, Martínez-Molina E, Gillis M, Velázquez E (2003) Description of Devosia neptuniae sp. nov. that nodulates and fixes nitrogen in symbiosis with Neptunia natans, an aquatic legume from India. Syst Appl Microbiol 26:47–53

    Article  CAS  PubMed  Google Scholar 

  • Rivas R, Willems A, Palomo JL, Garcia-Benavides P, Mateos PF, Martinez-Molina E, Gillis M, Velazquez E (2004) Bradyrhizobium betae sp. nov., isolated from roots of Beta vulgaris affected by tumour-like deformations. Int J Syst Evol Microbiol 54:1271–1275

    Article  CAS  PubMed  Google Scholar 

  • Román-Ponce B, Zhang YJ, Vásquez-Murrieta MS, Sui XH, Chen WF, Padilla JCA, Guo XW, Gao JL, Yan J, WeiGe H, Wang ET (2016) Rhizobium acidisoli sp. nov., isolated from 1 root nodules of Phaseolus vulgaris in acid 2 soils in Mexico. Int J Syst Evol Microbiol 66:398–406

    Article  PubMed  CAS  Google Scholar 

  • Rome S, Fernandez MP, Brunel B, Normannd P, Cleyet-Marel JC (1996) Sinorhizobium medicae sp. nov., isolated from annual Medicago spp. Int J Syst Evol Microbiol 46:972–980

    CAS  Google Scholar 

  • Rozahon M, Ismayil N, Hamood B, Erkin R, Abdurahman M, Mamtimin H, Abdukerim M, La R, Rahman E (2014) Rhizobiun populi sp. nov., an endophytic bacterium isolated from Populus euphratica. Int J Syst Evol Microbiol 64:3215–3221

    Article  CAS  PubMed  Google Scholar 

  • Saidi S, Ramirez-Bahena MH, Santillana N, Sungia D, Alvarez-Martinez E, Peix A, Mhamdi R, Velazquez E (2014) Rhizobium laguerreae sp. nov., nodulates Vicia faba on several Continents. Int J Syst Evol Microbiol 64:242–247

    Article  CAS  PubMed  Google Scholar 

  • Sánchez M, Ramírez-Bahena MH, Peix A, Lorite MJ, Sanjuán J, Velázquez E, Monza J (2014) Phyllobacterium loti sp. nov. isolated from nodules of Lotus corniculatus. Int J Syst Evol Microbiol 64:781–786

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sawada H, Kuykendal LD, Young JM (2003) Changing concepts in the systematics of bacterial nitrogen-fixing legume symbionts. J Gen Appl Microbiol 49:155–179

    Article  CAS  PubMed  Google Scholar 

  • Scholla MH, Elkan GH (1984) Rhizobium fredii sp. nov. a fast-growing species that effectively nodulates soybeans. Int J Syst Bacteriol 34:484–486

    Article  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Segovia L, Young JP, Martinez-Romero E (1993) Reclassification of American Rhizobium leguminosarum biovar phaseoli type I strains as Rhizobium etli sp. nov. Int J Syst Bacteriol 43:374–377

    Article  CAS  PubMed  Google Scholar 

  • Shamseldin A, Carro L, Peix A, Velázquez E, Moawad H, Sadowsky MJ (2016) The symbiovar trifolii of Rhizobium bangladeshense and Rhizobium aegyptiacum sp. nov. nodulate Trifolium alexandrinum in Egypt. Syst Appl Microbiol 39:275–279

    Article  PubMed  Google Scholar 

  • Shen L, Zhang LP, Liu H, Liu R, Zhang KY, Lai R (2010) Rhizobium kunmingense sp. nov. isolated from rhizosphere soil of Camptotheca acuminta Decne. J Gen Appl Microbiol 56:143–149

    Article  CAS  PubMed  Google Scholar 

  • Sheu SY, Chou JH, Bontemps C, Elliott GN, Gross E, James EK, Sprent JI, Young JP, Chen WM (2012) Burkholderia symbiotica sp. nov., isolated from root nodules of Mimosa spp. native to north-east Brazil. Int J Syst Evol Microbiol 62:2272–2278

    Article  CAS  PubMed  Google Scholar 

  • Sheu SY, Chou JH, Bontemps C, Elliott GN, Gross E, dos Reis Junior FB, Melkonian R, Moulin L, James EK, Sprent JI, Young JPW, Chen WM (2013) Burkholderia diazotrophica sp. nov., isolated from root nodules of Mimosa spp. Int J Syst Evol Microbiol 63:435–441

    Article  CAS  PubMed  Google Scholar 

  • Sheu SH, Huang HW, Young CC, Chen WM (2015) Rhizobium alvei sp. nov., isolated from a freshwater river. Int J Syst Evol Microbiol 65:472–478

    Article  CAS  PubMed  Google Scholar 

  • Sheu SY, Chen ZH, Young CC, Chen WM (2016) Rhizobium ipomoeae 1 sp. nov., isolated from a water convoevueus field. Int J Syst Evol Microbiol 66:1633–1640

    Article  PubMed  Google Scholar 

  • Shiraishi A, Matsushita N, Hougetsu T (2010) Nodulation in black locust by the Gamma-Proteobacteria Pseudomonas sp. and the Beta-Proteobacteria Burkholderia sp. Syst Appl Microbiol 33:269–274

    Article  CAS  PubMed  Google Scholar 

  • Silva FV, De Meyer SE, Simoes-Araujo JL, da Costa Barbe T, Xavier GR, O’Hara G, Ardley JK, Rumjanek NG, Willems A, Zilli JE (2014) Bradyrhizobium manausense sp. nov., isolated from effective nodules of Vigna unguiculata grown in Brazilian Amazonian rainforest soils. Int J Syst Evol Microbiol 64:2358–2363

    Article  CAS  PubMed  Google Scholar 

  • Somasegaran P, Hoben HJ (1985) Methods in legume Rhizobium technology. Niftal Project; Mircen, Hawai

    Google Scholar 

  • Sprent JI (2001) Nodulation in legumes. Royal Botanic Gardens, Kew

    Google Scholar 

  • Squartini A, Struffi P, Doring H, Selenska-Pobell S, Tola E, Giacomini A, Vendramin E, Velazquez E, Mateos PF, Martinez-Molina E, Dazzo FB, Casella S, Nuti MP (2002) Rhizobium sullae sp. nov. (formerly Rhizobium hedysari), the root-nodule microsymbiont of Hedysarum coronarium L. Int J Syst Evol Microbiol 52:1267–1276

    CAS  PubMed  Google Scholar 

  • Stackebrandt E, Gobel BM (1994) Taxonomic note: a place for DNA-DNA re-association and 16S rRNA sequence analysis in the present species definition in bacteriology. Int J Syst Bacteriol 44:846–849

    Article  CAS  Google Scholar 

  • Steenkampa ET, van Zyla E, Beukesa CW, Avontuura JR, Chana WY, Palmera M, Mthombenia LS, Phalaneb FL, Seremea TK, Ventera SN (2015) Burkholderia kirstenboschensis sp. nov. nodulates papilionoid legumes indigenous to South Africa Emma. Syst Appl Microbiol 38:545–554

    Article  CAS  Google Scholar 

  • Tan ZY, Kan LF, Peng XG, Wang ET, Reinhold-Hurek B, Chen WX (2001) Rhizobium yanglingense sp. nov., isolated from arid and semi-arid regions in China. Int J Syst Evol Microbiol 51:909–914

    Article  CAS  PubMed  Google Scholar 

  • Teamtisong K, Songwattana P, Noisangiam R, Piromyou P, Boonker N, Tittabutr P, Minamisawa K, Nantagij A, Okazaki S, Abe M, Uchiumi T, Teaumroong N (2013) Divergent Nod-Containing Bradyrhizobium sp. DOA9 with a megaplasmid and its host range. Microbes Environ 29:370–376

    Article  Google Scholar 

  • Tian CF, Wang ET, Wu LJ, Han TX, Chen WF, Gu CT, Gu JG, Chen WX (2008) Rhizobium fabae sp. nov., a bacterium that nodulates Vicia faba. Int J Syst Evol Microbiol 58:2871–2875

    Article  CAS  PubMed  Google Scholar 

  • Tighe SW, de Lajudie P, Dipietro K, Lindstrom K, Nick G, Jarvis BDW (2000) Analysis of cellular fatty acids and phenotypic relationships of Agrobacterium, Bradyrhizobium, Mesorhizobium, Rhizobium and Sinorhizobium species using the sherlock microbial identification system. Int J Syst Evol Microbiol 50:787–801

    Article  CAS  PubMed  Google Scholar 

  • Toledo I, Lloret L, Martínez-Romero E (2003) Sinorhizobium americanus sp. nov., a new Sinorhizobium species nodulating native Acacia spp. in Mexico. Syst Appl Microbiol 26:54–64

    Article  CAS  PubMed  Google Scholar 

  • Trujillo ME, Willems A, Abril A, Planchuelo AM, Rivas R, Ludena D, Mateos PF, Martinez-Molina E, Velazquez E (2005) Nodulation of Lupinus albus by strains of Ochrobactrum lupini sp. nov. Appl Environ Microbiol 71:1318–1327

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Turdahon M, Osman C, Hamdun M, Yusuf K, Abdurehim Z, Abaydulla G, Abdulkarim M, Fang C, Rahman E (2013) Rhizobium tarimense sp. nov., isolated from soil in the ancient Khiyik river. Int J Syst Evol Microbiol 63:2424–2429

    Article  CAS  PubMed  Google Scholar 

  • Valverde A, Velazquez E, Santos FF, Vizcaıno N, Rivas R, Mateos PF, Martinez-Molina E, Igual JM, Willems A (2005) Phyllobacterium trifolii sp. nov., nodulating Trifolium and Lupinus in Spanish soils. Int J Syst Evol Microbiol 55:1985–1989

    Article  CAS  PubMed  Google Scholar 

  • Valverde A, Igual JM, Peix A, Cervantes E, Velazquez E (2006) Rhizobium lusitanum sp. nov. a bacterium that nodulates Phaseolus vulgaris. Int J Syst Evol Microbiol 56:2631–2637

    Article  CAS  PubMed  Google Scholar 

  • Van Berkum P, Eardly BD (2002) The aquatic budding bacterium Blastobacter denitrificans is a nitrogen-fixing symbiont of Aeschynomene indica. Appl Environ Microbiol 68:1132–1136

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Van Berkum P, Beyene D, Bao G, Campbell TA, Eardly BD (1998) Rhizobium mongolense sp. nov. is one of three rhizobial genotypes identified which nodulate and form nitrogen-fixing symbioses with Medicago ruthenica [(L.) Ledebour]. Int J Syst Evol Microbiol 48:13–22

    Google Scholar 

  • Van Berkum P, Leiboldb JM, Eardly BD (2006) Proposal for combining Bradyrhizobium spp. (Aeschynomene indica) with Blastobacter denitrificans and to transfer Blastobacter denitrificans (Hirsch and Muller, 1985) to the genus Bradyrhizobium as Bradyrhizobium denitrificans (comb. nov.). Syst Appl Microbiol 29:207–215

    Article  PubMed  CAS  Google Scholar 

  • Vandamme P, Goris J, Chen WM, 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

    Article  PubMed  Google Scholar 

  • Vanlaere E, Baldwin A, Gevers D, Henry D, De Brandt E, LiPuma JJ, Mahenthiralingam E, Speert DP, Dowson C, Vandamme P (2009) Taxon K, a complex within the Burkholderia cepacia complex, comprises at least two novel species. Burkholderia contaminans sp. nov. and Burkholderia lata sp. nov. Int J Syst Evol Microbiol 59:102–111

    Article  CAS  PubMed  Google Scholar 

  • Velazquez E, Igual JM, Willems A, Fernandez MP, Munoz E, Mateos PF, Abril A, Toro N, Normand P, Cervantes E, Gillis M, Martinez-Molina E (2001) Mesorhizobium chacoense sp. nov., a novel species that nodulates Prosopis alba in the Chaco Arido region (Argentina). Int J Syst Evol Microbiol 51:1011–1021

    Article  CAS  PubMed  Google Scholar 

  • Vidal C, Chantreuil C, Berge O, Maure L, Escarre J, Bena G, Brunel B, Cleyet-Mare JC (2009) Mesorhizobium metallidurans sp. nov., a metal resistant symbiont of Anthyllis vulneraria growing on metallicolous soil in Languedoc, France. Int J Syst Evol Microbiol 59:850–855

    Article  CAS  PubMed  Google Scholar 

  • Vincent JM (1970) The cultivation, isolation and maintenance of rhizobia. In: Vincent JM (ed) A manual for the practical study of root-nodule. Blackwell Scientific Publications, Oxford, pp 1–13

    Google Scholar 

  • Vinuesa P, Leon-Barrios M, Silva C, Willems A, Jarabo-Lorenzo A, Perez-Galdona R, Werner D, Martinez-Romero E (2005) Bradyrhizobium canariense sp. nov., an acid tolerant endosymbiont that nodulates endemic genistoid legumes (Papilionoideae: Genisteae) from the Canary Islands, along with Bradyrhizobium japonicum bv. genistearum, Bradyrhizobium genospecies alpha and Bradyrhizobium genospecies beta. Int J Syst Evol Microbiol 55:569–575

    Article  CAS  PubMed  Google Scholar 

  • Wang ET, van Berkum P, Beyene D, Sui XH, Dorado O, Chen WX, Martinez-Romero E (1998) Rhizobium huautlense sp. nov., a symbiont of Sesbania herbacea that has a close phylogenetic relationship with Rhizobium galegae. Int J Syst Bacteriol 48:687–699

    Article  CAS  PubMed  Google Scholar 

  • Wang ET, Rogel MA, Los Santos AG, Martinez-Romero J, Cevallos MA, Martinez-Romero E (1999a) Rhizobium etli bv. mimosae, a novel biovar isolated from Mimosa affinis. Int J Syst Bacteriol 49:1479–1491

    Article  CAS  PubMed  Google Scholar 

  • Wang ET, van Berkum P, Sui XH, Beyene D, Chen WX, Martinez-Romero E (1999b) Diversity of rhizobia associated with Amorpha fruticosa isolated from Chinese soils and description of Mesorhizobium amorphae sp. nov. Int J Syst Bacteriol 49:51–65

    Article  PubMed  Google Scholar 

  • Wang ET, Tan ZY, Willems A, Fernandez-Lopez M, Reinhold-Hurek B, Martinez-Romero E (2002) Sinorhizobium morelense sp. nov., a Leucaena leucocephala-associated bacterium that is highly resistant to multiple antibiotics. Int J Syst Evol Microbiol 52:1687–1693

    CAS  PubMed  Google Scholar 

  • Wang FQ, Wang ET, Liu J, Chen Q, Sui XH, Chen WF, Chen WX (2007) Mesorhizobium albiziae sp. nov., a novel bacterium that nodulates Albizia kalkora in a subtropical region of China. Int J Syst Evol Microbiol 57:1192–1199

    Article  CAS  PubMed  Google Scholar 

  • Wang F, Wang TE, Wu LJ, Sui XHYL Jr, Chen WX (2011) Rhizobium vallis sp. nov., isolated from nodules of three leguminous species. Int J Syst Evol Microbiol 61:2582–2588

    Article  PubMed  Google Scholar 

  • Wang JY, Wang R, Zhang YM, Liu HC, Chen WF, Wang ET, Sui XH, Chen WX (2013a) Bradyrhizobium daqingense sp. nov., isolated from soybean nodules. Int J Syst Evol Microbiol 63:616–624

    Article  CAS  PubMed  Google Scholar 

  • Wang R, Chang YL, Zheng WT, Zhang D, Zhang XX, Suia XH, Wang ET, Hu JQ, Zhang LY, Chen WX (2013b) Bradyrhizobium arachidis sp. nov., isolated from effective nodules of Arachis hypogaea grown in China. Syst Appl Microbiol 36:101–105

    Article  PubMed  CAS  Google Scholar 

  • Wang YC, Wang F, Hou BC, Wang ET, Chen WF, Sui XH, Chen WX, Li Y, Zhang YB (2013c) Proposal of Ensifer psoraleae sp. nov., Ensifer sesbaniae sp. nov., Ensifer morelense comb. nov. and Ensifer americanum comb. nov. Syst Appl Microbiol 36:467–473

    Article  PubMed  CAS  Google Scholar 

  • Wei GH, Wang ET, Tan ZY, Zhu ME, Chen WX (2002) Rhizobium indigoferae sp. nov. and Sinorhizobium kummerowiae sp. nov., respectively isolated from Indigofera spp. and Kummerowia stipulacea. Int J Syst Evol Microbiol 52:2231–2239

    CAS  PubMed  Google Scholar 

  • Wei GH, Tan ZY, Zhu ME, Wang ET, Han SZ, Chen WX (2003) Characterization of rhizobia isolated from legume species within the genera Astragalus and Lespedeza grown in the Loess Plateau of China and description of Rhizobium loessense sp. nov. Int J Syst Evol Microbiol 53:1575–1583

    Article  CAS  PubMed  Google Scholar 

  • Wellner S, Lodders N, Glaeser SP, Kämpfer P (2013) Methylobacterium trifolii sp. nov. and Methylobacterium thuringiense sp. nov., methanol-utilizing, pink-pigmented bacteria isolated from leaf surfaces. Int J Syst Evol Microbiol 63:2690–2699

    Article  CAS  PubMed  Google Scholar 

  • Wen Y, Zhang J, Yan Q, Li S, Hong Q (2011) Rhizobium phenanthrenilyticum sp. nov., a novel phenanthrene-degrading bacterium isolated from a petroleum residue treatment system. J Gen Appl Microbiol 57:319–329

    Article  CAS  PubMed  Google Scholar 

  • Willems A (2006) The taxonomy of rhizobia: an overview. Plant Soil 287:3–14

    Article  CAS  Google Scholar 

  • Willems A, Collins MD (1993) Phylogenetic analysis of rhizobia and agrobacteria based on 16S rRNA gene sequences. Int J Syst Bacteriol 43:305–313

    Article  CAS  PubMed  Google Scholar 

  • Xu LM, Ge C, Cui Z, Li J, Fan H (1995) Bradyhizobium liaoningense sp. nov., isolated from the root nodules of soybeans. Int J Syst Bacteriol 45:706–711

    Article  CAS  PubMed  Google Scholar 

  • Xu L, Shi JF, Zhao P, Chen WM, Qin W, Tang M, Wei GH (2011) Rhizobium sphaerophysae sp. nov., a novel species isolated from root nodules of Sphaerophysa salsula in China. Antonie Van Leeuwenhoek 99:845–854

    Article  PubMed  Google Scholar 

  • Xu L, Zhang Y, Deng ZS, Zhao L, Wei XL, Wei GH (2013) Rhizobium qilianshanense sp. nov., a novel species isolated from root nodule of Oxytropis ochrocephala Bunge in China. Antonie Van Leeuwenhoek 103:559–565

    Article  PubMed  Google Scholar 

  • Yanagi M, Yamasato K (1993) Phylogenetic analysis of the family Rhizobiaceae and related bacteria by sequencing of 16S rRNA gene using PCR and DNA sequencer. FEMS Microbiol Lett 107:115–120

    Article  CAS  PubMed  Google Scholar 

  • Yao ZY, Kan FL, Wang ET, Wei GH, Chen WX (2002) Characterization of rhizobia that nodulate legume species of the genus Lespedeza and description of Bradyrhizobium yuanmingense sp. nov. Int J Syst Evol Microbiol 52:2219–2230

    CAS  PubMed  Google Scholar 

  • Yao LJ, Shen YY, Zhan JP, Xu W, Cui GL, Wei GH (2012) Rhizobium taibaishanense sp. nov., isolated from a root nodule of Kummerowia striata. Int J Syst Evol Microbiol 62:335–341

    Article  CAS  PubMed  Google Scholar 

  • Yao Y, Sui XH, Zhang XX, Wang ET, Chen WX (2015) Bradyrhizobium erythrophlei sp. nov. and Bradyrhizobium ferriligni sp. nov., isolated from effective nodules of Erythrophleum fordii. Int J Syst Evol Microbiol 65:1831–1837

    Article  CAS  PubMed  Google Scholar 

  • Yoon JH, Kang SJ, Yi HS, Oh TK, Ryu CM (2010) Rhizobium soli sp. nov., isolated from soil. Int J Syst Evol Microbiol 60:1387–1393

    Article  CAS  PubMed  Google Scholar 

  • Young JM (2003) The genus name Ensifer Casida 1982 takes priority over Sinorhizobium Chen et al. 1988, and Sinorhizobium morelense Wang et al. 2002 is a later synonym of Ensifer adhaerens Casida 1982. Is the combination ‘Sinorhizobium adhaerens’ (Casida 1982) Willems et al. 2003 legitimate? Request for an Opinion. Int J Syst Evol Microbiol 53:2107–2110

    Article  CAS  PubMed  Google Scholar 

  • Young JM (2004) Renaming of Agrobacterium larrymoorei Bouzar and Jones 2001 as Rhizobium larrymoorei (Bouzar and Jones 2001) comb. nov. Int J Syst Evol Microbiol 54:149–149

    Article  CAS  PubMed  Google Scholar 

  • Young JM, Kuykendall LD, 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

    Article  CAS  PubMed  Google Scholar 

  • Yu X, Cloutier S, Tambong JT, Bromfield ESP (2014) Bradyrhizobium ottawaense sp. nov., a symbiotic nitrogen fixing bacterium from root nodules of soybeans in Canada. Int J Syst Evol Microbiol 64:3202–3207

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  Google Scholar 

  • Zhang GX, Ren SZ, Xu MY, Zen GQ, Luo HD, Chen JL, Tan ZY, Sun GP (2011a) Rhizobium borbori sp. nov., aniline-degrading bacteria isolated from activated sludge. Int J Syst Evol Microbiol 61:816–822

    Article  CAS  PubMed  Google Scholar 

  • Zhang RJ, Hou BC, Wang ET, Li Y Jr, Zhan XX, Chen WX (2011b) Rhizobium tubonense sp. nov., isolated from root nodules of Oxytropis glabra. Int J Syst Evol Microbiol 61:512–5177

    Article  CAS  PubMed  Google Scholar 

  • Zhang X, Sun L, Ma X, Sui XH, Jiang R (2011c) Rhizobium pseudoryzae sp. nov., isolated from the rhizosphere of rice. Int J Syst Evol Microbiol 61:2425–2429

    Article  CAS  PubMed  Google Scholar 

  • Zhang JJ, Liu TY, Chen WF, Wang ET, Sui XH, Zhang XX, Li Y, Li Y, Chen WX (2012a) Mesorhizobium muleiense sp. nov., nodulating with Cicer arietinum L. Int J Syst Evol Microbiol 62:2737–2742

    Article  CAS  PubMed  Google Scholar 

  • Zhang X, Li B, Wang H, Sui X, Max X, Hong Q, Jiang R (2012b) Rhizobium petrolearium sp. nov., isolated from oil contaminated soil. Int J Syst Evol Microbiol 62:1871–1876

    Article  CAS  PubMed  Google Scholar 

  • Zhang YM, Li Y Jr, Chen WF, Wang ET, Sui XH, Li QQ, Zhan YZ, Zhou YG, Chen WX (2012c) Bradyrhizobium huanghuaihaiense sp. nov., an effective symbiotic bacterium isolated from soybean (Glycine max L.) nodules. Int J Syst Evol Microbiol 62:1951–1957

    Article  CAS  PubMed  Google Scholar 

  • Zhang L, Shi X, Si M, Li C, Zhu L, Zhao L, Shen X, Wang Y (2014a) Rhizobium smilacinae sp. nov., an endophytic bacterium isolated from the leaf of Smilacina japonica. Antonie Van Leeuwenhoek 106:715–723

    Article  PubMed  Google Scholar 

  • Zhang XX, Tang X, Sheirdil AR, Sun L, Tong MX (2014b) Rhizobium rhizoryzae sp. nov., isolated from rice roots. Int J Syst Evol Microbiol 64:1373–1377

    Article  CAS  PubMed  Google Scholar 

  • Zhang XX, Gao JS, Cao YH, Sheirdil RA, Wang XC, Zhang L (2015) Rhizobium oryzicola sp. nov., potential plant growth-promoting endophytic bacteria isolated from rice roots. Int J Syst Evol Microbiol 65:2931–2936

    Article  CAS  PubMed  Google Scholar 

  • Zhao CT, Wang ET, Zhang YM, Chen WF, Sui XH, Chen WX, Liu HC, Zhang XX (2012) Mesorhizobium silamurunense sp. nov., isolated from root nodules of Astragalus species. Int J Syst Evol Microbiol 62:2180–2186

    Article  CAS  PubMed  Google Scholar 

  • Zheng WTLY Jr, Wang R, Sui XH, Zhang XX, Zhang JJ, Wang ET, Chen WX (2013) Mesorhizobium qingshengii sp. nov., isolated from effective nodules of Astragalus sinicus. Int J Syst Evol Microbiol 63:2002–2007

    Article  CAS  PubMed  Google Scholar 

  • Zhou PF, Chen WM, Wei GH (2010) Mesorhizobium robiniae sp. nov., isolated from root nodules of Robinia pseudoacacia. Int J Syst Evol Microbiol 60:2552–2556

    Article  CAS  PubMed  Google Scholar 

  • Zhou S, Li Q, Jiang H, Lindström K, Zhang X (2013) Mesorhizobium sangaii sp. nov., isolated from the root nodules of Astragalus luteolus and Astragalus ernestii. Int J Syst Evol Microbiol 63:2794–2799

    Article  CAS  PubMed  Google Scholar 

  • Zhu YJ, Lu JK, Chen YL, Wang SK, Sui XH, Kang LH (2015) Mesorhizobium acaciae sp. nov., isolated from root nodules of Acacia melanoxylon R. Br. Int J Syst Evol Microbiol 65:3558–3563

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zilli JE, Barauna AC, da Silva K, De Meyer SE, Farias Eliane NC, Kaminski PE, da Costa IB, Ardley JK, Willems A, Camacho NN, Dourado FS, O’Hara G (2014) Bradyrhizobium neotropicale sp. nov., isolated from effective nodules of Centrolobium paraense. Int J Syst Evol Microbiol 64:3950–3957

    Article  PubMed  CAS  Google Scholar 

  • Zurdo-Pineiro JL, Rivas R, Trujillo ME, Vizcaino N, Carrasco JA, Chamber M, Palomares A, Mateos PF, Martinez-Molina E, Velazquez E (2007) Ochrobactrum cytisi sp. nov., isolated from nodules of Cytisus scoparius in Spain. Int J Syst Evol Microbiol 57:784–788

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

The authors thank the STDF of Egypt for funding this work through project no. 1268. This projected was also funded, in part, by the Minnesota Agricultural Experiment Station (to MJS).

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Shamseldin, A., Abdelkhalek, A. & Sadowsky, M.J. Recent changes to the classification of symbiotic, nitrogen-fixing, legume-associating bacteria: a review. Symbiosis 71, 91–109 (2017). https://doi.org/10.1007/s13199-016-0462-3

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