1887

Abstract

The genus is considered as the probable ancestor lineage of all rhizobia, broadly spread in a variety of ecosystems and with remarkable diversity. A polyphasic study was performed to characterize and clarify the taxonomic position of eight bradyrhizobial strains isolated from indigenous legumes to Western Australia. As expected for the genus, the 16S rRNA gene sequences were highly conserved, but the results of multilocus sequence analysis with four housekeeping genes (, and ) confirmed three new distinct clades including the following strains: (1) WSM 1744, WSM 1736 and WSM 1737; (2) WSM 1791 and WSM 1742; and (3) WSM 1741, WSM 1735 and WSM 1790. The highest ANI values of the three groups in relation to the closest type strains were 92.4, 92.3 and 93.3 %, respectively, below the threshold of species circumscription. The digital DNA–DNA hybridization analysis also confirmed new species descriptions, with less than 52 % relatedness with the closest type strains. The phylogeny of the symbiotic gene clustered the eight strains into the symbiovar retamae, together with seven type strains, sharing from 94.2–98.1 % nucleotide identity (NI), and less than 88.7 % NI with other related strains and symbiovars. Morpho-physiological, phylogenetics, genomic and symbiotic traits were determined for the new groups and our data support the description of three new species, sp. nov., sp. nov. and , with WSM 1744 (=CNPSo 4013=LMG 31646), WSM 1791 (=CNPSo 4014=LMG 31647) and WSM 1741 (=CNPSo 4020=LMG 31651) designated as type strains, respectively.

Funding
This study was supported by the:
  • INCT - Plant-Growth Promoting Microorganisms for Agricultural Sustainability and Environmental Responsibility (Award CNPq 465133/2014-4, Fundação Araucária-STI 043/2019, CAPES)
    • Principle Award Recipient: Mariangela Hungria
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2020-07-15
2024-04-19
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References

  1. Parker MA. The spread of Bradyrhizobium lineages across host legume clades: from Abarema to Zygia . Microb Ecol 2015; 69:630–640 [View Article][PubMed]
    [Google Scholar]
  2. Ferraz Helene LC, Marçon Delamuta JR, Augusto Ribeiro R, Ormeño-Orrillo E, Antonio Rogel M et al. Bradyrhizobium viridifuturi sp. nov., encompassing nitrogen-fixing symbionts of legumes used for green manure and environmental services. Int J Syst Evol Microbiol 2015; 65:4441–4448 [View Article][PubMed]
    [Google Scholar]
  3. Hungria M, Loureiro MF, Mendes IC, Campo RJ, Graham PH. Inoculant preparation, production and application. In Werner W, Newton WE. (editors) Nitrogen Fixation in Agriculture, Forestry, Ecology and the Environment Dordrecht, Amsterdam: Springer; 2005 pp 223–254
    [Google Scholar]
  4. Ormeño-Orrillo E, Hungria M, Martínez-Romero E et al. Dinitrogen-fixing prokaryotes. In Rosenberg E. editor The Prokaryotes – Prokaryotic Physiology and Biochemistry Berlin Heidelberg: Springer-Verlag; 2013 pp 427–451
    [Google Scholar]
  5. Jordan DC. Notes: 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 1982; 32:136–139 [View Article]
    [Google Scholar]
  6. Hungria M, Menna P, Delamuta JRM. Bradyrhizobium, the ancestor of all rhizobia: phylogeny of housekeeping and nitrogen-fixation genes. In de Bruijn F. editor Biological Nitrogen Fixation Hoboken: John Wiley & Sons; 2015 pp 191–202
    [Google Scholar]
  7. Menna P, Barcellos FG, Hungria M. Phylogeny and taxonomy of a diverse collection of Bradyrhizobium strains based on multilocus sequence analysis of the 16S rRNA gene, ITS region and glnII, recA, atpD and dnaK genes. Int J Syst Evol Microbiol 2009; 59:2934–2950 [View Article][PubMed]
    [Google Scholar]
  8. Delamuta JRM, Ribeiro RA, Ormeño-Orrillo E, Parma MM, Melo IS et al. Bradyrhizobium tropiciagri sp. nov. and Bradyrhizobium embrapense sp. nov., nitrogen-fixing symbionts of tropical forage legumes. Int J Syst Evol Microbiol 2015; 65:4424–4433 [View Article][PubMed]
    [Google Scholar]
  9. Delamuta JRM, Ribeiro RA, Araújo JLS, Rouws LFM, Zilli Jerri Édson, Zilli JE et al. Bradyrhizobium stylosanthis sp. nov., comprising nitrogen-fixing symbionts isolated from nodules of the tropical forage legume Stylosanthes spp. Int J Syst Evol Microbiol 2016; 66:3078–3087 [View Article][PubMed]
    [Google Scholar]
  10. Delamuta JRM, Menna P, Ribeiro RA, Hungria M. Phylogenies of symbiotic genes of Bradyrhizobium symbionts of legumes of economic and environmental importance in Brazil support the definition of the new symbiovars pachyrhizi and sojae. Syst Appl Microbiol 2017; 40:254–265 [View Article][PubMed]
    [Google Scholar]
  11. Azarias Guimarães A, Florentino LA, Alves Almeida K, Lebbe L, Barroso Silva K, Guimarães AA, Almeida KA, Silva KB et al. High diversity of Bradyrhizobium strains isolated from several legume species and land uses in Brazilian tropical ecosystems. Syst Appl Microbiol 2015; 38:433–441 [View Article][PubMed]
    [Google Scholar]
  12. Ferraz Helene LC, O'Hara G, Hungria M, Helene LCF, Hara GW. Characterization of Bradyrhizobium strains indigenous to Western Australia and South Africa indicates remarkable genetic diversity and reveals putative new species. Syst Appl Microbiol 2020; 43:126053 [View Article][PubMed]
    [Google Scholar]
  13. Klepa MS, Urquiaga MCdeO, Somasegaran P, Delamuta JRM, Ribeiro RA et al. Bradyrhizobium niftali sp. nov., an effective nitrogen-fixing symbiont of partridge pea [Chamaecrista fasciculata (Michx.) Greene], a native caesalpinioid legume broadly distributed in the USA. Int J Syst Evol Microbiol 2019; 69:3448–3459 [View Article]
    [Google Scholar]
  14. Weisburg WG, Barns SM, Pelletier DA, Lane DJ. 16S ribosomal DNA amplification for phylogenetic study. J Bacteriol 1991; 173:697–703 [View Article][PubMed]
    [Google Scholar]
  15. van Berkum P, Fuhrmann JJ. Evolutionary relationships among the soybean bradyrhizobia reconstructed from 16S rRNA gene and internally transcribed spacer region sequence divergence. Int J Syst Evol Microbiol 2000; 50 Pt 6:2165–2172 [View Article][PubMed]
    [Google Scholar]
  16. Stackebrandt E, Ebers J. Taxonomic parameters revisited: tarnished gold standards. Microbiol Today 2006; 8:6–9
    [Google Scholar]
  17. Kim M, Oh H-S, Park S-C, Chun J. Towards a taxonomic coherence between average nucleotide identity and 16S rRNA gene sequence similarity for species demarcation of prokaryotes. Int J Syst Evol Microbiol 2014; 64:346–351 [View Article][PubMed]
    [Google Scholar]
  18. Chun J, Oren A, Ventosa A, Christensen H, Arahal DR et al. Proposed minimal standards for the use of genome data for the taxonomy of prokaryotes. Int J Syst Evol Microbiol 2018; 68:461–466 [View Article][PubMed]
    [Google Scholar]
  19. Schleifer KH. Classification of bacteria and archaea: past, present and future. Syst Appl Microbiol 2009; 32:533–542 [View Article][PubMed]
    [Google Scholar]
  20. Oren A, Garrity GM. Then and now: a systematic review of the systematics of prokaryotes in the last 80 years. Antonie Van Leeuwenhoek 2014; 106:43–56 [View Article][PubMed]
    [Google Scholar]
  21. Konstantinidis KT, Ramette A, Tiedje JM. Toward a more robust assessment of intraspecies diversity, using fewer genetic markers. Appl Environ Microbiol 2006; 72:7286–7293 [View Article][PubMed]
    [Google Scholar]
  22. Durán D, Rey L, Mayo J, Zúñiga-Dávila D, Imperial J et al. 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 2014; 64:2072–2078 [View Article][PubMed]
    [Google Scholar]
  23. Meier-Kolthoff JP, Auch AF, Klenk H-P, Göker M. Genome sequence-based species delimitation with confidence intervals and improved distance functions. BMC Bioinformatics 2013; 14:60–14 [View Article]
    [Google Scholar]
  24. Yates R, Howieson JG, Nandasena KG, O'Hara GW. Root-Nodule bacteria from Indigenous legumes in the north-west of Western Australia and their interaction with exotic legumes. Soil Biol Biochem 2004; 36:1319–1329 [View Article]
    [Google Scholar]
  25. Hungria M, O’Hara GW, Zilli JE, Araujo RS, Deaker R et al. Isolation and growth of rhizobia. In Howieson JG, Dilworth MJ. (editors) Working with Rhizobia Canberra: Australian Centre for International Agriculture Research (ACIAR); 2016 pp 39–60
    [Google Scholar]
  26. Stepkowski T, Moulin L, Krzyzańska A, McInnes A, Law IJ et al. European origin of Bradyrhizobium populations infecting lupins and serradella in soils of Western Australia and South Africa. Appl Environ Microbiol 2005; 71:7041–7052 [View Article][PubMed]
    [Google Scholar]
  27. Felsenstein J. Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol 1981; 17:368–376 [View Article][PubMed]
    [Google Scholar]
  28. Kumar S, Stecher G, Tamura K. MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 2016; 33:1870–1874 [View Article][PubMed]
    [Google Scholar]
  29. Edgar RC. Muscle: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 2004; 32:1792–1797 [View Article][PubMed]
    [Google Scholar]
  30. Felsenstein J. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 1985; 39:783–791 [View Article][PubMed]
    [Google Scholar]
  31. Schwarz G. Estimating the dimension of a model. Ann Statist. 1978; 6:461–464 [View Article]
    [Google Scholar]
  32. Hall T. BioEdit: a user-friendly biological sequence alignment editor and analysis program for windows 95/98/NT. Nucleic Acids Symp Ser 1999; 41:95–98
    [Google Scholar]
  33. Helene LCF, Delamuta JRM, Ribeiro RA, Hungria M. Bradyrhizobium mercantei sp. nov., a nitrogen-fixing symbiont isolated from nodules of Deguelia costata (syn. Lonchocarpus costatus). Int J Syst Evol Microbiol 2017; 67:1827–1834 [View Article][PubMed]
    [Google Scholar]
  34. Ahnia H, Boulila F, Boulila A, Boucheffa K, Durán D et al. Cytisus villosus from Northeastern Algeria is nodulated by genetically diverse Bradyrhizobium strains. Antonie van Leeuwenhoek 2014; 105:1121–1129 [View Article][PubMed]
    [Google Scholar]
  35. Lasse Grönemeyer J, Hurek T, Reinhold-Hurek B, Grönemeyer JL, Bünger W. Bradyrhizobium kavangense sp. nov., a symbiotic nitrogen-fixing bacterium from root nodules of traditional Namibian pulses. Int J Syst Evol Microbiol 2015; 65:4886–4894 [View Article][PubMed]
    [Google Scholar]
  36. Grönemeyer JL, Hurek T, Bünger W, Reinhold-Hurek B. Bradyrhizobium vignae sp. nov., a nitrogen-fixing symbiont isolated from effective nodules of Vigna and Arachis . Int J Syst Evol Microbiol 2016; 66:62–69 [View Article][PubMed]
    [Google Scholar]
  37. Rogel MA, Ormeño-Orrillo E, Martinez Romero E, Romero EM. Symbiovars in rhizobia reflect bacterial adaptation to legumes. Syst Appl Microbiol 2011; 34:96–104 [View Article][PubMed]
    [Google Scholar]
  38. Peix A, Ramírez-Bahena MH, Velázquez E, Bedmar EJ. Bacterial associations with legumes. CRC Crit Rev Plant Sci 2015; 34:17–42 [View Article]
    [Google Scholar]
  39. Vinuesa P, León-Barrios M, Silva C, Willems A, Jarabo-Lorenzo A et al. 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 2005; 55:569–575 [View Article][PubMed]
    [Google Scholar]
  40. Bejarano A, Ramírez-Bahena M-H, Velázquez E, Peix A. Vigna unguiculata is nodulated in Spain by endosymbionts of Genisteae legumes and by a new symbiovar (vignae) of the genus Bradyrhizobium . Syst Appl Microbiol 2014; 37:533–540 [View Article][PubMed]
    [Google Scholar]
  41. Cobo-Díaz JF, Martínez-Hidalgo P, Fernández-González AJ, Martínez-Molina E, Toro N et al. The endemic Genista versicolor from Sierra Nevada National Park in Spain is nodulated by putative new Bradyrhizobium species and a novel symbiovar (sierranevadense). Syst Appl Microbiol 2014; 37:177–185 [View Article][PubMed]
    [Google Scholar]
  42. Guerrouj K, Ruíz-Díez B, Chahboune R, Ramírez-Bahena M-H, Abdelmoumen H et al. Definition of a novel symbiovar (sv. retamae) within Bradyrhizobium retamae sp. nov., nodulating Retama sphaerocarpa and Retama monosperma . Syst Appl Microbiol 2013; 36:218–223 [View Article][PubMed]
    [Google Scholar]
  43. Ramírez-Bahena MH, Flores-Félix JD, Chahboune R, Toro M, Velázquez E et al. Bradyrhizobium centrosemae (symbiovar centrosemae) sp. nov., Bradyrhizobium americanum (symbiovar phaseolarum) sp. nov. and a new symbiovar (tropici) of Bradyrhizobium viridifuturi establish symbiosis with Centrosema species native to America. Syst Appl Microbiol 2016; 39:378–383 [View Article][PubMed]
    [Google Scholar]
  44. Msaddak A, Durán D, Rejili M, Mars M, Ruiz-Argüeso T et al. Diverse bacteria affiliated with the genera Microvirga, Phyllobacterium, and Bradyrhizobium nodulate Lupinus micranthus growing in soils of northern Tunisia. Appl Environ Microbiol 2017; 83:02820–16 [View Article][PubMed]
    [Google Scholar]
  45. Chun J, Rainey FA. Integrating genomics into the taxonomy and systematics of the bacteria and archaea. Int J Syst Evol Microbiol 2014; 64:316–324 [View Article][PubMed]
    [Google Scholar]
  46. Aziz RK, Bartels D, Best AA, DeJongh M, Disz T et al. The RAST server: rapid annotations using subsystems technology. BMC Genomics 2008; 9:75 [View Article][PubMed]
    [Google Scholar]
  47. Rodriguez-R LM, Konstantinidis KT. The enveomics collection: a toolbox for specialized analyses of microbial genomes and metagenomes. Peer J Prepr 2016; 4:e1900v1
    [Google Scholar]
  48. Overbeek R, Olson R, Pusch GD, Olsen GJ, Davis JJ et al. The seed and the rapid annotation of microbial genomes using subsystems technology (RAST). Nucleic Acids Res 2014; 42:D206–D214 [View Article]
    [Google Scholar]
  49. Xu LM, Ge C, Cui Z, Li J, Fan H. Bradyrhizobium liaoningense sp. nov., isolated from the root nodules of soybeans. Int J Syst Bacteriol 1995; 45:706–711 [View Article][PubMed]
    [Google Scholar]
  50. Chibeba AM, Kyei-Boahen S, Guimarães MdeF, Nogueira MA, Hungria M. Isolation, characterization and selection of indigenous Bradyrhizobium strains with outstanding symbiotic performance to increase soybean yields in Mozambique. Agric Ecosyst Environ 2017; 246:291–305 [View Article][PubMed]
    [Google Scholar]
  51. Sneath PHA, Sokal RR. Numerical Taxonomy: the Principles and Practice of Numerical Classification San Francisco, USA: W. H. Freeman and Company; 1973 p 573
    [Google Scholar]
  52. Jaccard P. The distribution of the flora in the alpine ZONE.1. New Phytol 1912; 11:37–50 [View Article]
    [Google Scholar]
  53. Hungria M, Chueire Lı́gia Maria de O, Coca RG, Megı́as M. Preliminary characterization of fast growing rhizobial strains isolated from soyabean nodules in Brazil. Soil Biol Biochem 2001; 33:1349–1361 [View Article]
    [Google Scholar]
  54. Yates RJ, Howieson JG, Hungria M, Bala A, O’Hara GW et al. Authentication of rhizobia and assessment of the legume symbiosis in controlled plant growth systems. In Howieson JG, Dilworth MJ. (editors) Working with Rhizobia. Chapter 5 Canberra: Australian Center for International Agricultural Research (ACIAR);; 2016 pp 73–108
    [Google Scholar]
  55. Ramírez-Bahena MH, Peix A, Rivas R, Camacho M, Rodríguez-Navarro DN et al. Bradyrhizobium pachyrhizi sp. nov. and Bradyrhizobium jicamae sp. nov., isolated from effective nodules of Pachyrhizus erosus . Int J Syst Evol Microbiol 2009; 59:1929–1934 [View Article][PubMed]
    [Google Scholar]
  56. Chang YL, Wang JY, Wang ET, Liu HC, Sui XH et al. Bradyrhizobium lablabi sp. nov., isolated from effective nodules of Lablab purpureus and Arachis hypogaea . Int J Syst Evol Microbiol 2011; 61:2496–2502 [View Article][PubMed]
    [Google Scholar]
  57. Grönemeyer JL, Bünger W, Reinhold-Hurek B. Bradyrhizobium namibiense sp. nov., a symbiotic nitrogen-fixing bacterium from root nodules of Lablab purpureus, hyacinth bean, in Namibia. Int J Syst Evol Microbiol 2017; 67:4884–4891 [View Article][PubMed]
    [Google Scholar]
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