1887

Abstract

The diversity of 71 rhizobial strains belonging to the genus , isolated from root nodules of woody legumes growing in southern Ethiopia, was studied using multilocus sequence analysis (MLSA) and phenotypic approaches. Phylogenetic analyses based on core genes revealed that 43 strains were clustered in seven distinct and consistent positions (genospecies I–VII), while another 25 strains were also distinct but were discrepant in their placement on the different gene trees. The remaining three strains occupied the same phylogenetic branches as defined species and thus were not distinct. Irrespective of their chromosomal background, the majority of the test strains were highly related with respect to their and gene sequences, suggesting that these symbionts might have acquired these genes recently from a common origin. On the phylogenetic tree, the branch containing the test strains and reference species isolated from woody legumes in Africa was clearly separate from those isolated outside the continent, suggesting that these symbionts have a long history of separate evolution within for this gene. A cross-inoculation study showed that our strains were capable of eliciting effective nodulation on the homologous host and on other host species. This suggests a potential to improve nitrogen fixation by selecting for broad-host-range inoculants. Our study confirms the presence of a wide diversity of in East Africa and, while contributing to the general knowledge of the biodiversity within the genus, also highlights the need to focus on previously less-well-explored biogeographical regions to unravel as-yet-unidentified rhizobial resources.

Loading

Article metrics loading...

/content/journal/ijsem/10.1099/ijs.0.039230-0
2012-09-01
2019-12-07
Loading full text...

Full text loading...

/deliver/fulltext/ijsem/62/9/2286.html?itemId=/content/journal/ijsem/10.1099/ijs.0.039230-0&mimeType=html&fmt=ahah

References

  1. Bala A. , Murphy P. , Giller K. E. . ( 2002; ). Occurrence and genetic diversity of rhizobia nodulating Sesbania sesban in African soils. . Soil Biol Biochem 34:, 1759–1768. [CrossRef]
    [Google Scholar]
  2. Boom R. , Sol C. J. , Salimans M. M. , Jansen C. L. , Wertheim-van Dillen P. M. , van der Noordaa J. . ( 1990; ). Rapid and simple method for purification of nucleic acids. . J Clin Microbiol 28:, 495–503.
    [Google Scholar]
  3. Charles L. , Carbone I. , Davies K. G. , Bird D. , Burke M. , Kerry B. R. , Opperman C. H. . ( 2005; ). Phylogenetic analysis of Pasteuria penetrans by use of multiple genetic loci. . J Bacteriol 187:, 5700–5708. [CrossRef] [PubMed]
    [Google Scholar]
  4. Chen W. F. , Guan S. H. , Zhao C. T. , Yan X. R. , Man C. X. , Wang E. T. , Chen W. X. . ( 2008; ). Different Mesorhizobium species associated with Caragana carry similar symbiotic genes and have common host ranges. . FEMS Microbiol Lett 283:, 203–209. [CrossRef] [PubMed]
    [Google Scholar]
  5. Degefu T. , Wolde-meskel E. , Frostegård Å. . ( 2011; ). Multilocus sequence analyses reveal several unnamed Mesorhizobium genospecies nodulating Acacia species and Sesbania sesban trees in southern regions of Ethiopia. . Syst Appl Microbiol 34:, 216–226. [CrossRef] [PubMed]
    [Google Scholar]
  6. de Lajudie P. , Willems A. , Pot B. , Dewettinck D. , Maestrojuan G. , Neyra M. , Collins M. D. , 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.[CrossRef]
    [Google Scholar]
  7. Diouf D. , Fall D. , Chaintreuil C. , Ba A. T. , Dreyfus B. , Neyra M. , Ndoye I. , Moulin L. . ( 2010; ). Phylogenetic analyses of symbiotic genes and characterization of functional traits of Mesorhizobium spp. strains associated with the promiscuous species Acacia seyal Del.. J Appl Microbiol 108:, 818–830. [CrossRef] [PubMed]
    [Google Scholar]
  8. Donate-Correa J. , León-Barrios M. , Hernández M. , Pérez-Galdona R. , del Arco-Aguilar M. . ( 2007; ). Different Mesorhizobium species sharing the same symbiotic genes nodulate the shrub legume Anagyris latifolia . . Syst Appl Microbiol 30:, 615–623. [CrossRef] [PubMed]
    [Google Scholar]
  9. 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]
  10. Haukka K. , Lindström K. , Young J. P. W. . ( 1998; ). Three phylogenetic groups of nodA and nifH genes in Sinorhizobium and Mesorhizobium isolates from leguminous trees growing in Africa and Latin America. . Appl Environ Microbiol 64:, 419–426.[PubMed]
    [Google Scholar]
  11. Iglesias O. , Rivas R. , García-Fraile P. , Abril A. , Mateos P. F. , Martinez-Molina E. , Velázquez E. V. . ( 2007; ). Genetic characterization of fast-growing rhizobia able to nodulate Prosopis alba in North Spain. . FEMS Microbiol Lett 277:, 210–216. [CrossRef] [PubMed]
    [Google Scholar]
  12. Konstantinidis K. T. , Ramette A. , Tiedje J. M. . ( 2006; ). Toward a more robust assessment of intraspecies diversity, using fewer genetic markers. . Appl Environ Microbiol 72:, 7286–7293. [CrossRef] [PubMed]
    [Google Scholar]
  13. Laguerre G. , Nour S. M. , Macheret V. , Sanjuan J. , Drouin P. , Amarger N. . ( 2001; ). Classification of rhizobia based on nodC and nifH gene analysis reveals a close phylogenetic relationship among Phaseolus vulgaris symbionts. . Microbiology 147:, 981–993.[PubMed]
    [Google Scholar]
  14. Lloret L. , Ormeño-Orrillo E. , Rincón R. , Martínez-Romero J. , Rogel-Hernández M. A. , Martínez-Romero E. . ( 2007; ). Ensifer mexicanus sp. nov. a new species nodulating Acacia angustissima (Mill.) Kuntze in Mexico. . Syst Appl Microbiol 30:, 280–290. [CrossRef] [PubMed]
    [Google Scholar]
  15. Maâtallah J. , Berrah E. B. , Sanjuan J. , Lunch C. . ( 2002; ). Phenotypic characterization of rhizobia isolated from chickpea (Cicer arietinum) growing in Moroccan soils. . Agronomie 22:, 321–329. [CrossRef]
    [Google Scholar]
  16. 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]
  17. 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:, 200–214. [CrossRef] [PubMed]
    [Google Scholar]
  18. Martin F. W. , Lavin M. , Sanderson M. J. . ( 2004; ). A phylogeny of legumes (Leguminosae) based on analysis of the plastid matK gene resolves many well-supported subclades within the family. . Am J Bot 91:, 1846–1862. [CrossRef] [PubMed]
    [Google Scholar]
  19. Merabet C. , Martens M. , Mahdhi M. , Zakhia F. , Sy A. , Le Roux C. , Domergue O. , Coopman R. , Bekki A. . & other authors ( 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. [CrossRef] [PubMed]
    [Google Scholar]
  20. Nick G. , de Lajudie P. , Eardly B. D. , Suomalainen S. , Paulin L. , Zhang X. , 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. [CrossRef] [PubMed]
    [Google Scholar]
  21. Posada D. , Buckley T. R. . ( 2004; ). Model selection and model averaging in phylogenetics: advantages of Akaike information criterion and Bayesian approaches over likelihood ratio tests. . Syst Biol 53:, 793–808. [CrossRef] [PubMed]
    [Google Scholar]
  22. Posada D. , Crandall K. A. . ( 1998; ). modeltest: testing the model of DNA substitution. . Bioinformatics 14:, 817–818. [CrossRef] [PubMed]
    [Google Scholar]
  23. Rincón-Rosales R. , Lloret L. , Ponce E. , Martínez-Romero E. . ( 2009; ). Rhizobia with different symbiotic efficiencies nodulate Acaciella angustissima in Mexico, including Sinorhizobium chiapanecum sp. nov. which has common symbiotic genes with Sinorhizobium mexicanum . . FEMS Microbiol Ecol 67:, 103–117. [CrossRef] [PubMed]
    [Google Scholar]
  24. Rivas R. , Velázquez E. , Willems A. , Vizcaíno N. , Subba-Rao N. S. , Mateos P. F. , Gillis M. , Dazzo F. B. , Martínez-Molina E. . ( 2002; ). A new species of Devosia that forms a unique nitrogen-fixing root-nodule symbiosis with the aquatic legume Neptunia natans (L.f.) Druce. . Appl Environ Microbiol 68:, 5217–5222. [CrossRef] [PubMed]
    [Google Scholar]
  25. Rosselló-Móra R. . ( 2011; ). Towards a taxonomy of Bacteria and Archaea based on interactive and cumulative data repositories. . Environ Microbiol 14:, 318–334. [CrossRef] [PubMed]
    [Google Scholar]
  26. 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:, 1–11. [CrossRef] [PubMed]
    [Google Scholar]
  27. Sawada H. , Kuykendall L. D. , Young J. M. . ( 2003; ). Changing concepts in the systematics of bacterial nitrogen-fixing legume symbionts. . J Gen Appl Microbiol 49:, 155–179. [CrossRef] [PubMed]
    [Google Scholar]
  28. Sharma P. K. , Kundu B. S. , Dogra R. C. . ( 1993; ). Molecular mechanism of host specificity in legume-rhizobium symbiosis. . Biotechnol Adv 11:, 741–779. [CrossRef] [PubMed]
    [Google Scholar]
  29. Shiraishi A. , Matsushita N. , Hougetsu T. . ( 2010; ). Nodulation in black locust by the Gammaproteobacteria Pseudomonas sp. and the Betaproteobacteria Burkholderia sp.. Syst Appl Microbiol 33:, 269–274. [CrossRef] [PubMed]
    [Google Scholar]
  30. Somasegaran P. , Hoben H. J. . ( 1994; ). Handbook for Rhizobia: Methods in Legume-Rhizobium Technology. New York:: Springer;.[CrossRef]
    [Google Scholar]
  31. Stackebrandt E. , Goebel B. M. . ( 1994; ). Taxonomic note: a place for DNA-DNA reassociation and 16S rRNA sequence analysis in the present species definition in bacteriology. . Int J Syst Bacteriol 44:, 846–849. [CrossRef]
    [Google Scholar]
  32. Tamura K. , Dudley J. , Nei M. , Kumar S. . ( 2007; ). mega4: molecular evolutionary genetics analysis (mega) software version 4.0. . Mol Biol Evol 24:, 1596–1599. [CrossRef] [PubMed]
    [Google Scholar]
  33. Terefework Z. , Lortet G. , Suominen L. , Lindström K. . ( 2000; ). Molecular evolution of interactions between rhizobium and their legume hosts. . In Prokaryotic Nitrogen Fixation: a Model for Analysis of a Biological Process, pp. 187–206. Edited by Triplett E. . . Wymondham, UK:: Horizon Press;.
    [Google Scholar]
  34. Terefework Z. , Kaijalainen S. , Lindström K. . ( 2001; ). AFLP fingerprinting as a tool to study the genetic diversity of Rhizobium galegae isolated from Galega orientalis and Galega officinalis . . J Biotechnol 91:, 169–180. [CrossRef] [PubMed]
    [Google Scholar]
  35. Thompson J. D. , Higgins D. G. , Gibson T. J. . ( 1994; ). clustal w: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. . Nucleic Acids Res 22:, 4673–4680. [CrossRef] [PubMed]
    [Google Scholar]
  36. 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. [CrossRef] [PubMed]
    [Google Scholar]
  37. Vandamme P. , Pot B. , Gillis M. , de Vos P. , Kersters K. , Swings J. . ( 1996; ). Polyphasic taxonomy, a consensus approach to bacterial systematics. . Microbiol Rev 60:, 407–438.[PubMed]
    [Google Scholar]
  38. Vinuesa P. , León-Barrios M. , Silva C. , Willems A. , Jarabo-Lorenzo A. , Pérez-Galdona R. , Werner D. , Martínez-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. [CrossRef] [PubMed]
    [Google Scholar]
  39. Weisburg W. G. , Barns S. M. , Pelletier D. A. , Lane D. J. . ( 1991; ). 16S ribosomal DNA amplification for phylogenetic study. . J Bacteriol 173:, 697–703.[PubMed]
    [Google Scholar]
  40. Willems A. , Fernández-López M. , Muñoz-Adelantado E. M. , Goris J. , De Vos P. , Martínez-Romero E. , Toro N. , Gillis M. . ( 2003; ). Description of new Ensifer strains from nodules and proposal to transfer Ensifer adhaerens Casida 1982 to Sinorhizobium as Sinorhizobium adhaerens comb. nov. Request for an Opinion. . Int J Syst Evol Microbiol 53:, 1207–1217. [CrossRef] [PubMed]
    [Google Scholar]
  41. Wolde-meskel E. , Terefework Z. , Lindström K. , Frostegård Å. . ( 2004; ). Metabolic and genomic diversity of rhizobia isolated from field standing native and exotic woody legumes in southern Ethiopia. . Syst Appl Microbiol 27:, 603–611. [CrossRef] [PubMed]
    [Google Scholar]
  42. Wolde-meskel E. , Terefework Z. , Frostegård Å. , Lindström K. . ( 2005; ). Genetic diversity and phylogeny of rhizobia isolated from agroforestry legume species in southern Ethiopia. . Int J Syst Evol Microbiol 55:, 1439–1452. [CrossRef] [PubMed]
    [Google Scholar]
  43. Young J. M. . ( 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. [CrossRef] [PubMed]
    [Google Scholar]
  44. 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]
  45. Zahran H. H. . ( 1999; ). Rhizobium-legume symbiosis and nitrogen fixation under severe conditions and in an arid climate. . Microbiol Mol Biol Rev 63:, 968–989.[PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/ijsem/10.1099/ijs.0.039230-0
Loading
/content/journal/ijsem/10.1099/ijs.0.039230-0
Loading

Data & Media loading...

Supplements

Supplementary material 

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