1887

Abstract

Root nodule bacteria were isolated from Tul. grown in soils from the Amazon region, State of Roraima (Brazil). 16S rRNA gene sequence analysis of seven strains (BR 10247, BR 10296, BR 10297, BR 10298, BR 10299, BR 10300 and BR 10301) placed them in the genus with the closest neighbours being the type strains of (98.8 % similarity), (98.8 %), (98.7 %), (98.6 %), (98.6 %), (98.6 %) and (98.3 %). This high similarity, however, was not confirmed by the intergenic transcribed spacer (ITS) 16S–23S rRNA region sequence analysis nor by multi-locus sequence analysis. Phylogenetic analyses of five housekeeping genes (, , , and ) revealed EK05 ( = LMG 24129) to be the most closely related type strain (95.7 % sequence similarity or less). Chemotaxonomic data, including fatty acid profiles [major components being C and summed feature 8 (18 : 1ω6/18 : 1ω7)], DNA G+C content, slow growth rate and carbon compound utilization patterns, supported the placement of the novel strains in the genus . Results of DNA–DNA relatedness studies and physiological data (especially carbon source utilization) differentiated the strains from the closest recognized species of the genus . Symbiosis-related genes for nodulation () and nitrogen fixation () placed the novel species in a new branch within the genus . Based on the current data, these seven strains represent a novel species for which the name sp. nov. is proposed. The type strain is BR 10247 ( = HAMBI 3599).

Funding
This study was supported by the:
  • CNPq
  • Embrapa
  • Murdoch University
Loading

Article metrics loading...

/content/journal/ijsem/10.1099/ijs.0.065458-0
2014-12-01
2021-08-04
Loading full text...

Full text loading...

/deliver/fulltext/ijsem/64/12/3950.html?itemId=/content/journal/ijsem/10.1099/ijs.0.065458-0&mimeType=html&fmt=ahah

References

  1. Altschul S. F., Gish W., Miller W., Myers E. W., Lipman D. J. ( 1990 ). Basic local alignment search tool. . J Mol Biol 215, 403410. [View Article] [PubMed]
    [Google Scholar]
  2. Araújo W. F., Andrade Júnior A. S., Medeiros R. D., Sampaio R. A. ( 2001 ). Precipitação pluviométrica mensal provável em Boa Vista, Estado de Roraima, Brasil. . Rev Bras Eng Agric Ambient 5, 563567. [View Article]
    [Google Scholar]
  3. Baraúna A. C., da Silva K., Pereira G. M. D., Kaminski P. E., Perin L., Zilli J. E. ( 2014 ). Diversity and nitrogen fixation efficiency of rhizobia isolated from nodules of Centrolobium paraense . . Pesquisa Agropecu Bras 49, 296305. [View Article]
    [Google Scholar]
  4. Cobo-Díaz J. F., Martínez-Hidalgo P., Fernández-González A. J., Martínez-Molina E., Toro N., Velázquez E., Fernández-López M. ( 2014 ). 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 37, 177185. [View Article] [PubMed]
    [Google Scholar]
  5. Dahmer N., Wittman M. T. S., Kaminski P. E. ( 2009 ). Chromosome number and karyotype of the endangered Amazonian woody Centrolobium paraense Tul. species. . Crop Breeding App Biotech 9, 382385. [View Article]
    [Google Scholar]
  6. Delamuta J. R. M., Ribeiro R. A., Ormeño-Orrillo E., Melo I. S., Martínez-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, 33423351. [View Article] [PubMed]
    [Google Scholar]
  7. Ezaki T., Hashimoto Y., Yabuuchi E. ( 1989 ). Fluorometric deoxyribonucleic acid-deoxyribonucleic acid hybridization in microdilution wells as an alternative to membrane filter hybridization in which radioisotopes are used to determine genetic relatedness among bacterial strains. . Int J Syst Bacteriol 39, 224229. [View Article]
    [Google Scholar]
  8. Farris J. S., Källersjö M., Kluge A. G., Bult C. ( 1994 ). Testing significance of incongruence. . Cladistics 10, 315319. [View Article]
    [Google Scholar]
  9. Felsenstein J. ( 1981 ). Evolutionary trees from DNA sequences: a maximum likelihood approach. . J Mol Evol 17, 368376. [View Article] [PubMed]
    [Google Scholar]
  10. Fred E. B., Waksman S. ( 2003 ). Yeast extract-mannitol agar for laboratory: manual of general microbiology. . New York:: McGraw Hill;, 1928. 145p.
    [Google Scholar]
  11. Goris J., Suzuki K., De Vos P., Nakase T., Kersters K. ( 1998 ). Evaluation of a microplate DNA - DNA hybridization method compared with the initial renaturation method. . Can J Microbiol 44, 11481153. [View Article]
    [Google Scholar]
  12. 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, 221224. [View Article] [PubMed]
    [Google Scholar]
  13. Hollis A. B., Kloos W. E., Elkan G. E. ( 1981 ). DNA:DNA hybridization studies of Rhizobium japonicum and related Rhizobiaceae . . J Gen Microbiol 123, 215222.
    [Google Scholar]
  14. Howieson J. G., De Meyer S. E., Vivas-Marfisi A., Ratnayake S., Ardley J. K., Yates R. J. ( 2013 ). Novel Burkholderia bacteria isolated from Lebeckia ambigua – a perennial suffrutescent legume of the fynbos. . Soil Biol Biochem 60, 5564. [View Article]
    [Google Scholar]
  15. Islam M. S., 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. . Biosci Biotechnol Biochem 72, 14161429. [View Article] [PubMed]
    [Google Scholar]
  16. Lindström, K. & Gyllenberg, H. (2007). The species paradigm: proposal for a cross-disciplinary species concept. 11th International Congress on Culture Collections. I. Kurtböke. Goslar, Germany. World Federation of Culture Collections.
  17. Marques M. S., Pagano M., Scotti M. R. M. M. L. ( 2001 ). Dual inoculation of a woody legume (Centrolobium tomentosum) with rhizobia and mycorrhizal fungi in south-eastern Brazil. . Agrofor Syst 52, 107117. [View Article]
    [Google Scholar]
  18. 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, 200214. [View Article] [PubMed]
    [Google Scholar]
  19. Menna P., Barcellos F. G., 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, 29342950. [View Article] [PubMed]
    [Google Scholar]
  20. Mesbah M., Premachandran U., Whitman W. B. ( 1989 ). Precise measurement of the G+C content of deoxyribonucleic-acid by highperformance liquid-chromatography. . Int J Syst Bacteriol 39, 159167. [View Article]
    [Google Scholar]
  21. Moreira F. M. S., Haukka K., Young J. P. W. ( 1998 ). Biodiversity of rhizobia isolated from a wide range of forest legumes in Brazil. . Mol Ecol 7, 889895. [View Article] [PubMed]
    [Google Scholar]
  22. Ormeño-Orrillo E., Rogel-Hernández M. A., Lloret L., López-López A., Martínez J., Barois I., Martínez-Romero E. ( 2012 ). Change in land use alters the diversity and composition of Bradyrhizobium communities and led to the introduction of Rhizobium etli into the tropical rain forest of Los Tuxtlas (Mexico). . Microb Ecol 63, 822834. [View Article] [PubMed]
    [Google Scholar]
  23. Pagano M. C. ( 2008 ). Rhizobia associated with neotropical tree Centrolobium tomentonsum used in riparian restoration. . Plant Soil Environ 54, 498508.
    [Google Scholar]
  24. Parker M. ( 2008 ). Symbiotic Relationships of Legumes and Nodule Bacteria on Barro Colorado Island, Panama: A Review. . Microbial Ecology 55, 662672. [CrossRef]
    [Google Scholar]
  25. Parker M. A. ( 2003 ). Genetic markers for analysing symbiotic relationships and lateral gene transfer in Neotropical bradyrhizobia. . Mol Ecol 12, 24472455. [View Article] [PubMed]
    [Google Scholar]
  26. Pedreira, J. L. (2010). Uso e manejo indígena de pau-rainha (Centrolobium paraense Tul. – Fabaceae) na terra indígena Araçá, RR. Master’s thesis, Instituto Nacional de Pesquisa Amazônicas, Manaus, Brazil.
  27. Pirie M. D., Klitgaard B. B., Pennington R. T. ( 2009 ). Revision and biogeography of Centrolobium (Leguminosae - Papilionoideae). . Syst Bot 34, 345359. [View Article]
    [Google Scholar]
  28. Pitcher D. G., Saunders N. A., Owen R. J. ( 1989 ). Rapid extraction of bacterial genomic DNA with guanidium thiocyanate. . Lett Appl Microbiol 8, 151156. [View Article]
    [Google Scholar]
  29. Radl V., Simões-Araújo J. L., Leite J., Passos S. R., Martins L. M. V., Xavier G. R., Rumjanek N. G., Baldani J. I., Zilli J. E. ( 2014 ). Microvirga vignae sp. nov., a root nodule symbiotic bacterium isolated from cowpea grown in semi-arid Brazil. . Int J Syst Evol Microbiol 64, 725730. [View Article] [PubMed]
    [Google Scholar]
  30. Rivas R., Martens M., de Lajudie P., Willems A. ( 2009 ). Multilocus sequence analysis of the genus Bradyrhizobium . . Syst Appl Microbiol 32, 101110. [View Article] [PubMed]
    [Google Scholar]
  31. Sarita S., Sharma P. K., Priefer U. B., 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, 111. [View Article] [PubMed]
    [Google Scholar]
  32. Souza L. A. G., da Silva M. F., Moreira F. W. ( 1994 ). Capacidade de nodulação de cem Leguminosas da Amazônia. . Acta Amazon 24, 919.
    [Google Scholar]
  33. Swofford D. L. ( 2002 ). paup*: Phylogenetic analysis using parsimony (and other methods), version 4. . Sunderland, MA:: Sinauer Associates;.
    [Google Scholar]
  34. Tamura K., Peterson D., Peterson N., Stecher G., Nei M., Kumar S. ( 2011 ). mega5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. . Mol Biol Evol 28, 27312739. [View Article] [PubMed]
    [Google Scholar]
  35. Tighe S. W., de Lajudie P., Dipietro K., Lindström K., Nick G., Jarvis B. D. W. ( 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, 787801. [View Article] [PubMed]
    [Google Scholar]
  36. Tindall B. J., Rosselló-Móra R., Busse H.-J., Ludwig W., Kämpfer P. ( 2010 ). Notes on the characterization of prokaryote strains for taxonomic purposes. . Int J Syst Evol Microbiol 60, 249266. [View Article] [PubMed]
    [Google Scholar]
  37. Ueda T., Suga Y., Yahiro N., Matsuguchi T. ( 1995 ). Remarkable N2-fixing bacterial diversity detected in rice roots by molecular evolutionary analysis of nifH gene sequences. . J Bacteriol 177, 14141417.[PubMed]
    [Google Scholar]
  38. van Berkum P., Fuhrmann J. J. ( 2009 ). Evidence from Internally Transcribed Spacer Sequence Analysis of Soybean Strains that Extant Bradyrhizobium spp. Are Likely the Products of Reticulate Evolutionary Events. . Applied Environ Microbio 75, 7882. [CrossRef]
    [Google Scholar]
  39. van Berkum P., Terefework Z., Paulin L., Suomalainen S., Lindström K., Eardly B. D. ( 2003 ). Discordant Phylogenies within the rrn Loci of Rhizobia. . J Bacteriol 185, 29882998. [CrossRef]
    [Google Scholar]
  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, 2954. [View Article] [PubMed]
    [Google Scholar]
  41. Willems A., Coopman R., Gillis M. ( 2001a ). Phylogenetic and DNA–DNA hybridization analyses of Bradyrhizobium species. . Int J Syst Evol Microbiol 51, 111117.[PubMed]
    [Google Scholar]
  42. Willems A., Doignon-Bourcier F., Goris J., Coopman R., de Lajudie P., De Vos P., Gillis M. ( 2001b ). DNA–DNA hybridization study of Bradyrhizobium strains. . Int J Syst Evol Microbiol 51, 13151322.[PubMed]
    [Google Scholar]
  43. Willems A., Munive A., de Lajudie P., Gillis M. ( 2003 ). In most Bradyrhizobium groups sequence comparison of 16S–23S rDNA internal transcribed spacer regions corroborates DNA–DNA hybridizations. . Syst Appl Microbiol 26, 203210. [View Article] [PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/ijsem/10.1099/ijs.0.065458-0
Loading
/content/journal/ijsem/10.1099/ijs.0.065458-0
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF

Most cited this month Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error