1887

Abstract

Rhizobial strains isolated from effective root nodules of field-grown lentil () from different parts of Bangladesh were previously analysed using sequences of the 16S rRNA gene, three housekeeping genes (, and ) and three nodulation genes (, and ), DNA fingerprinting and phenotypic characterization. Analysis of housekeeping gene sequences and DNA fingerprints indicated that the strains belonged to three novel clades in the genus . In present study, a representative strain from each clade was further characterized by determination of cellular fatty acid compositions, carbon substrate utilization patterns and DNA–DNA hybridization and average nucleotide identity (ANI) analyses from whole-genome sequences. DNA–DNA hybridization showed 50–62 % relatedness to their closest relatives (the type strains of and ) and 50–60 % relatedness to each other. These results were further supported by ANI values, based on genome sequencing, which were 87–92 % with their close relatives and 88–89 % with each other. On the basis of these results, three novel species, sp. nov. (type strain BLR27 = LMG 28441 = DSM 29286), sp. nov. (type strain BLR175 = LMG 28442 = DSM 29287) and sp. nov. (type strain BLR195 = LMG 28443 = DSM 29288), are proposed. These species share common nodulation genes (, and ) that are similar to those of the symbiovar .

Loading

Article metrics loading...

/content/journal/ijsem/10.1099/ijs.0.000373
2015-09-01
2019-09-22
Loading full text...

Full text loading...

/deliver/fulltext/ijsem/65/9/3037.html?itemId=/content/journal/ijsem/10.1099/ijs.0.000373&mimeType=html&fmt=ahah

References

  1. Beringer J.E.. ( 1974;). R factor transfer in Rhizobium leguminosarum. J Gen Microbiol 84: 188–198 [CrossRef] [PubMed].
    [Google Scholar]
  2. Chan J.Z.-M., Halachev M.R., Loman N.J., Constantinidou C., Pallen M.J.. ( 2012;). Defining bacterial species in the genomic era: insights from the genus Acinetobacter. BMC Microbiol 12: 302 [CrossRef] [PubMed].
    [Google Scholar]
  3. Cleenwerck I., Vandemeulebroecke K., Janssens D., Swings J.. ( 2002;). Re-examination of the genus Acetobacter, with descriptions of Acetobacter cerevisiae sp. nov. and Acetobacter malorum sp. nov. Int J Syst Evol Microbiol 52: 1551–1558 [CrossRef] [PubMed].
    [Google Scholar]
  4. Díaz-Alcántara C.-A., Ramírez-Bahena M.-H., Mulas D., García-Fraile P., Gómez-Moriano A., Peix A., Velázquez E., González-Andrés F.. ( 2014;). Analysis of rhizobial strains nodulating Phaseolus vulgaris from Hispaniola Island, a geographic bridge between Meso and South America and the first historical link with Europe. Syst Appl Microbiol 37: 149–156 [CrossRef] [PubMed].
    [Google Scholar]
  5. Gaunt M.W., Turner S.L., Rigottier-Gois L., Lloyd-Macgilp S.A., Young J.P.W.. ( 2001;). Phylogenies of atpD and recA support the small subunit rRNA-based classification of rhizobia. Int J Syst Evol Microbiol 51: 2037–2048 [CrossRef] [PubMed].
    [Google Scholar]
  6. Geniaux E., Amarger N.. ( 1993;). Diversity and stability of plasmid transfer in isolates from a single field population of Rhizobium leguminosarum bv. viciae. FEMS Microbiol Ecol 102: 251–260 [CrossRef].
    [Google Scholar]
  7. Goris J., Konstantinidis K.T., Klappenbach J.A., Coenye T., Vandamme P., Tiedje J.M.. ( 2007;). DNA-DNA hybridization values and their relationship to whole-genome sequence similarities. Int J Syst Evol Microbiol 57: 81–91 [CrossRef] [PubMed].
    [Google Scholar]
  8. Hall T.A.. ( 1999;). BioEdit: a user friendly biological sequence align ment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41: 95–98.
    [Google Scholar]
  9. Hou B.C., Wang E.T., Li Y., Jia R.Z., Chen W.F., Man C.X., Sui X.H., Chen W.X.. ( 2009;). Rhizobial resource associated with epidemic legumes in Tibet. Microb Ecol 57: 69–81 [CrossRef] [PubMed].
    [Google Scholar]
  10. Hynes M.F., O'Connell M.P.. ( 1990;). Host plant effect on competition among strains of Rhizobium leguminosarum. Can J Microbiol 36: 864–869 [CrossRef].
    [Google Scholar]
  11. Jordan D.C.. ( 1984;). Family III. Rhizobiaceae. . In Bergey's Manual of Systematic Bacteriology, pp. 234–242. Edited by Krieg N. R., Holt J. G..vol. 1 Baltimore: Williams & Wilkins;.
    [Google Scholar]
  12. Konstantinidis K.T., Tiedje J.M.. ( 2005;). Genomic insights that advance the species definition for prokaryotes. Proc Natl Acad Sci U S A 102: 2567–2572 [CrossRef] [PubMed].
    [Google Scholar]
  13. Kurtz S., Phillippy A., Delcher A.L., Smoot M., Shumway M., Antonescu C., Salzberg S.L.. ( 2004;). Versatile and open software for comparing large genomes. Genome Biol 5: R12 [CrossRef] [PubMed].
    [Google Scholar]
  14. Kuykendall L.D., Roy M.A., O'Neill J.J., Devine T.E.. ( 1988;). Fatty acids, antibiotic resistance and deoxyribonucleic acid homology groups of Bradyrhizobium japonicum. Int J Syst Bacteriol 38: 358–361 [CrossRef].
    [Google Scholar]
  15. Laguerre G., Geniaux E., Mazurier S.I., Casartelli R.R., Amarger N.. ( 1993;). Conformity and diversity among field isolates of Rhizobium leguminosarum bv. viciae, bv. trifolii, and bv. phaseoli revealed by DNA hybridization using chromosome and plasmid probes. Can J Microbiol 39: 412–419 [CrossRef].
    [Google Scholar]
  16. Laguerre G., Louvrier P., Allard M.-R., Amarger N.. ( 2003;). Compatibility of rhizobial genotypes within natural populations of Rhizobium leguminosarum biovar viciae for nodulation of host legumes. Appl Environ Microbiol 69: 2276–2283 [CrossRef] [PubMed].
    [Google Scholar]
  17. Martens M., Delaere M., Coopman R., De Vos P., Gillis M., Willems A.. ( 2007;). Multilocus sequence analysis of Ensifer and related taxa. Int J Syst Evol Microbiol 57: 489–503 [CrossRef] [PubMed].
    [Google Scholar]
  18. Materon L.A., Keatinge J.D.H., Beck D.P., Yurtsever N., Karuc K., Altuntas S.. ( 1995;). The role of rhizobial biodiversity in legume crop productivity in the West Asian highlands. Exp Agric 31: 485–491 [CrossRef].
    [Google Scholar]
  19. McCarthy B.J., Bolton E.T.. ( 1963;). An approach to the measurement of genetic relatedness among organisms. Proc Natl Acad Sci U S A 50: 156–164 [CrossRef] [PubMed].
    [Google Scholar]
  20. Mesbah M., Premachandran U., Whitman W.B.. ( 1989;). Precise measurement of the G+C content of deoxyribonucleic acid by high-performance liquid chromatography. Int J Syst Bacteriol 39: 159–167 [CrossRef].
    [Google Scholar]
  21. Moawad H., Beck D.P.. ( 1991;). Some characteristics of Rhizobium leguminosarum isolates from uninoculated field-grown lentil. Soil Biol Biochem 23: 933–937 [CrossRef].
    [Google Scholar]
  22. Mutch L.A., Young J.P.W.. ( 2004;). Diversity and specificity of Rhizobium leguminosarum biovar viciae on wild and cultivated legumes. Mol Ecol 13: 2435–2444 [CrossRef] [PubMed].
    [Google Scholar]
  23. Ramírez-Bahena M.H., García-Fraile P., Peix A., Valverde A., Rivas R., Igual J.M., Mateos P.F., Martínez-Molina E., Velázquez E.. ( 2008;). Revision of the taxonomic status of the species Rhizobium leguminosarum (Frank 1879) Frank 1889AL Rhizobium phaseoli Dangeard 1926AL Rhizobium trifolii Dangeard 1926AL R. trifolii is a later synonym of R. leguminosarum. Reclassification of the strain R. leguminosarum DSM 30132 ( = NCIMB 11478) as Rhizobium pisi sp. nov. Int J Syst Evol Microbiol 58: 2484–2490 [CrossRef] [PubMed].
    [Google Scholar]
  24. Rashid M.H., Schäfer H., Gonzalez J., Wink M.. ( 2012;). Genetic diversity of rhizobia nodulating lentil (Lens culinaris) in Bangladesh. Syst Appl Microbiol 35: 98–109 [CrossRef] [PubMed].
    [Google Scholar]
  25. Rashid M.H., Gonzalez J., Young J.P.W., Wink M.. ( 2014;). Rhizobium leguminosarum is the symbiont of lentils in the Middle East and Europe but not in Bangladesh. FEMS Microbiol Ecol 87: 64–77 [CrossRef] [PubMed].
    [Google Scholar]
  26. Richter M., Rosselló-Móra R.. ( 2009;). Shifting the genomic gold standard for the prokaryotic species definition. Proc Natl Acad Sci U S A 106: 19126–19131 [CrossRef] [PubMed].
    [Google Scholar]
  27. Rogel M.A., Ormeño-Orrillo E., Martínez Romero E.. ( 2011;). Symbiovars in rhizobia reflect bacterial adaptation to legumes. Syst Appl Microbiol 34: 96–104 [CrossRef] [PubMed].
    [Google Scholar]
  28. Rogers J.S., Swofford D.L.. ( 1998;). A fast method for approximating maximum likelihoods of phylogenetic trees from nucleotide sequences. Syst Biol 47: 77–89 [CrossRef] [PubMed].
    [Google Scholar]
  29. Saı¨di S., Ramírez-Bahena M.-H., Santillana N., Zúñiga D., Álvarez-Martínez E., Peix A., Mhamdi R., Velázquez E.. ( 2014;). Rhizobium laguerreae sp. nov. nodulates Vicia faba on several continents. Int J Syst Evol Microbiol 64: 242–247 [CrossRef] [PubMed].
    [Google Scholar]
  30. Saitou N., Nei M.. ( 1987;). The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4: 406–425 [PubMed].
    [Google Scholar]
  31. Santillana N., Ramírez-Bahena M.H., García-Fraile P., Velázquez E., Zúñiga D.. ( 2008;). Phylogenetic diversity based on rrs, atpD, recA genes and 16S-23S intergenic sequence analyses of rhizobial strains isolated from Vicia faba and Pisum sativum in Peru. Arch Microbiol 189: 239–247 [CrossRef] [PubMed].
    [Google Scholar]
  32. Segovia L., Young J.P.W., Martínez-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 [CrossRef] [PubMed].
    [Google Scholar]
  33. Stepkowski T., Moulin L., Krzyzańska A., McInnes A., Law I.J., Howieson J.. ( 2005;). European origin of Bradyrhizobium populations infecting lupins and serradella in soils of Western Australia and South Africa. Appl Environ Microbiol 71: 7041–7052 [CrossRef] [PubMed].
    [Google Scholar]
  34. Tamura K., Stecher G., Peterson D., Filipski A., Kumar S.. ( 2013;). mega6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30: 2725–2729 [CrossRef] [PubMed].
    [Google Scholar]
  35. Thompson J.D., Gibson T.J., Plewniak F., Jeanmougin F., Higgins D.G.. ( 1997;). The clustal_x windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25: 4876–4882 [CrossRef] [PubMed].
    [Google Scholar]
  36. Tian C.F., Wang E.T., Wu L.J., Han T.X., Chen W.F., Gu C.T., Gu J.G., Chen W.X.. ( 2008;). Rhizobium fabae sp. nov., a bacterium that nodulates Vicia faba. Int J Syst Evol Microbiol 58: 2871–2875 [CrossRef] [PubMed].
    [Google Scholar]
  37. Tian C.F., Young J.P.W., Wang E.T., Tamimi S.M., Chen W.X.. ( 2010;). Population mixing of Rhizobium leguminosarum bv. viciae nodulating Vicia faba: the role of recombination and lateral gene transfer. FEMS Microbiol Ecol 73: 563–576 [PubMed].
    [Google Scholar]
  38. 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: 249–266 [CrossRef] [PubMed].
    [Google Scholar]
  39. Turner S.L., Young J.P.W.. ( 2000;). The glutamine synthetases of rhizobia: phylogenetics and evolutionary implications. Mol Biol Evol 17: 309–319 [CrossRef] [PubMed].
    [Google Scholar]
  40. Vinuesa P.. ( 2010;). Multilocus sequence analysis and species phylogeny. . In Molecular Phylogeny of Microorganisms, pp. 41–64. Edited by Oren A., Papke R. T.. Wymondham, UK: Caister Academic Press;.
    [Google Scholar]
  41. 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 [CrossRef] [PubMed].
    [Google Scholar]
  42. Wayne L.G., Brenner D.G., Colwell R.R., Grimont P.A.D., Kandler O., Krichevsky M.I., Moore L.H., Moore W.E.C., Murray R.G.E., other authors. ( 1987;). Report of the ad hoc committee on reconciliation of approaches to bacterial systematic. Int J Syst Bacteriol 37: 463–464 [CrossRef].
    [Google Scholar]
  43. Wilson K.. ( 1987;). Preparation of genomic DNA from bacteria. . In Current Protocols in Molecular Biology, pp. 2.4.1–2.4.5. Edited by Ausubel F. M., Brent R., Kingston R. E., Moore D. D., Seidman J. G., Smith J. A., Struhl K.. New York: Greene Publishing and Wiley-Inter Science;.
    [Google Scholar]
  44. Young J.P.W., Wexler M.. ( 1988;). Sym plasmid and chromosomal genotypes are correlated in field populations of Rhizobium leguminosarum. J Gen Microbiol 134: 2731–2739.
    [Google Scholar]
  45. Young J.P.W., Crossman L.C., Johnston A.W.B., Thomson N.R., Ghazoui Z.F., Hull K.H., Wexler M., Curson A.R.J., Todd J.D., other authors. ( 2006;). The genome of Rhizobium leguminosarum has recognizable core and accessory components. Genome Biol 7: R34 [CrossRef] [PubMed].
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/ijsem/10.1099/ijs.0.000373
Loading
/content/journal/ijsem/10.1099/ijs.0.000373
Loading

Data & Media loading...

Supplementary Data



PDF

Most Cited This Month

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