Abstract
Thirteen Gram-negative, aerobic, motile with polar flagella, rod-shaped bacteria were isolated from root nodules of Centrolobium paraense Tul. grown in soils from the Amazon region of Brazil. Growth of strains was observed at temperature range 20–36 °C (optimal 28 °C), pH ranges 5–11 (optimal 6.0–7.0), and 0.1–0.5%NaCl (optimal 0.1–0.3%). Analysis of 16S rRNA gene placed the strains into two groups within Bradyrhizobium. Closest neighbouring species (98.8%) for group I was B. neotropicale while for group II were 12 species with more than 99% of similarity. Multi-locus sequence analysis (MLSA) with dnaK, glnII, recA, and rpoB confirmed B. neotropicale BR 10247T as the closest type strain for the group I and B. elkanii USDA 76T and B. pachyrhizi PAC 48T for group II. Average Nucleotide Identity (ANI) differentiated group I from the B. neotropicale BR 10247T (79.6%) and group II from B. elkanii USDA 76T and B. pachyrhizi PAC 48T (88.1% and 87.9%, respectively). Fatty acid profiles [majority C16:0 and Summed feature 8 (18:1ω6c/18:1ω7c) for both groups], DNA G + C content, and carbon compound utilization supported the placement of the novel strains in the genus Bradyrhizobium. Gene nodC and nifH of the new strains have in general low similarity with other Bradyrhizobium species. Both groups nodulated plants from the tribes Crotalarieae, Dalbergiae, Genisteae, and Phaseoleae. Based on the presented data, two novel species which the names Bradyrhizobium centrolobii and Bradyrhizobium macuxiense are proposed, with BR 10245T (=HAMBI 3597T) and BR 10303T (=HAMBI 3602T) as the respective-type strains.
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References
Baraúna AC, da Silva K, Pereira GMD, Kaminski PE, Perin L, Zilli JE (2014) Diversity and nitrogen fixation efficiency or rhizobia isolated from nodules of Centrolobium paraense. Pesq. agropec. bras. 49: 296–305
Baraúna AC, Rouws LFM, Simoes-Araújo JL, Junior FBR, Iannetta PPM, Maluk MM, Goi SR, Reis VM, James EK & Zilli JE (2016) Rhizobium altiplani sp. nov. isolated from effective nodules on Mimosa pudica growing in untypically alkaline soil in Central Brazil. Int J Syst Evol Microbiol doi:10.1099/ijsem.0.001322
Dahmer N, Wittman MTS, Kaminski PE (2009) Chromosome number and karyotype of the endangered Amazonian woody Centrolobium paraense Tul. species. Crop Breeding and Applied. Biotechnology 9:382–385
Delamuta JRM, Ribeiro RA, Simoes-Araújo JL, Rouws LFM, Zilli JE, Parma MM, Melo IS, Hungria M (2016) Bradyrhizobium stylosanthis sp. nov., comprising nitrogen-fixing symbionts isolated from nodules of the tropical forage legume Stylosanthes spp. Int J Syst Evol Microbiol 66:3078–3087
Felsenstein J (1981) Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol 17:368–376
Gouy M, Guindon S, Gascuel O (2010) SeaView version 4: a multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Mol Biol Evol 27:221–224
Helene LCF (2015) Diversidade entre estirpes do gênero Bradyrhizobium avaliada por Multilocus Sequence Analysis (MLSA) e Análise Polifásica. Dissertation, Universidade Estadual de Londrina
Jukes TH, Cantor CR (1969) Evolution of protein molecules. In: Munro HN (ed) Mammalian protein metabolism. Academic, New York, 21–123
Kumar S, Stecher G, Tamura K (2016) Mega 7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874
Kuykendall LD, Saxena B, Devine TE, Udell SE (1992) Genetic diversity in Bradyrhizobium japonicum Jordan 1982 and a proposal for Bradyrhizobium elkanii sp. nov. Can J Microbiol 38:501–505
Martens M, Dawyndt P, Coopman R, Gillis M, De Vos P, Willems A (2008) Advantages of multilocus sequence analysis fortaxonomic studies: a case study using 10 housekeeping genes in the genus Ensifer (including former Sinorhizobium). Int J Syst Evol Microbiol 58:200–214
Menna P, Barcellos FG, Hungria M (2009) 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 59:2934–2950
Pedreira JL (2010) Uso e manejo indígena de pau-rainha (Centrolobium paraense Tul. – Fabaceae) na terra indıgena Araça, RR. Dissertation, Instituto Nacional de Pesquisas da Amazônia
Peix A, Ramírez-Bahena MH, Velázquez E, Bedmar EJ (2015) Bacterial association with legumes. Crit Rev Plant Sci 34:17–42
Pirie MD, Klitgaard BB, Pennington RT (2009) Revision and biogeography of Centrolobium (Leguminosae–Papilionoideae). Syst Bot 34:345–359
Poly F, Monrozier LJ, Bally R (2001) Improvement in the RFLP procedure for studying the diversity of nifH genes in communities of nitrogen fixers in soil. Res Microbiol 152:95–103
Radl V, Simoes-Araujo JL, Leite J, Passos SR, Martins LMV, 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 64:725–730
Ramírez-Bahena, MH, Peix A, Rivas R, Camacho M, Rodrígues-Navarro DN, Mateos PF, Martínez-Molina E, Willems A, Velázques 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
Richter M, Rossello-Mora R (2009) Shifting the genomic gold standard for the prokaryotic species definition. Proc Natl Acad Sci USA 106:19126–19131
Rivas R, Martens M, de Lajudie P, Willems A (2009) Multilocus sequence analysis of the genus Bradyrhizobium. Syst Appl Microbiol 32:101–110
Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425
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 54:1–11
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
Versalovic J, Schneider M, de Bruijn FJ, Lupski JR (1994) Genomic fingerprinting of bacteria using repetitive sequence-based polymerase chain reaction. Methods. Mol Cell Biol 5:25–40
Vinuesa P, Silva C, Werner D, Martínez-Romero E (2005) Population genetics and phylogenetic inference in bacterial molecular systematics: the roles of migration and recombination in Bradyrhizobium species cohesion and delineation. Mol Phylogenet Evol 34:29–54
Zilli JE, Baraúna AC, da Silva K, de Meyer SE, Farias ENC, Kaminsky PE, da Costa IB, Ardley JK, Willens A, Camacho NN, Dourado FS, O´Hara G (2014) Bradyrhizobium neotropicale sp. nov., isolated from effective nodules of Centrolobium paraense. Int J Syst Evol Mictobiol 64:3950–3957
Acknowledgements
The authors would like to thank Rosa Pitard, Fernanda Dourado, Natalia Camacho, and Karine Freitas (Embrapa Agrobiologia) for technical assistance. Embrapa, CNPq, and FAPERJ financially supported this study.
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Communicated by Erko Stackebrandt.
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Michel, D.C., Passos, S.R., Simões-Araujo, J.L. et al. Bradyrhizobium centrolobii and Bradyrhizobium macuxiense sp. nov. isolated from Centrolobium paraense grown in soil of Amazonia, Brazil. Arch Microbiol 199, 657–664 (2017). https://doi.org/10.1007/s00203-017-1340-y
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DOI: https://doi.org/10.1007/s00203-017-1340-y