1887

Abstract

Nine isolates from , , (Tunisia) and (Senegal) were analysed by multilocus sequence analysis (MLSA) of five housekeeping genes (, , , and ), the 16S rRNA gene and the nodulation gene . Analysis of the individual and concatenated gene sequences demonstrated that the nine new strains constituted three stable, well-supported (bootstrap and gene sequence similarity values) monophyletic clusters, A, B and C, all belonging to the branch of the genus , regardless of the phylogenetic reconstruction method used (maximum likelihood, maximum-parsimony, neighbour-joining). The three groups were further characterized by API 100 auxanographic tests, host specificity and gene sequence analysis. On the basis of these data, clusters A and C are suggested as representing two novel species within the genus , for which the names sp. nov. (type strain ORS 1407=LMG 24690=CIP 109850) and sp. nov. (type strain ORS 1400=LMG 24692=CIP 109916) are proposed. The cluster B strains were assigned to genomovar A.

Loading

Article metrics loading...

/content/journal/ijsem/10.1099/ijs.0.012088-0
2010-03-01
2024-03-28
Loading full text...

Full text loading...

/deliver/fulltext/ijsem/60/3/664.html?itemId=/content/journal/ijsem/10.1099/ijs.0.012088-0&mimeType=html&fmt=ahah

References

  1. Baele M., Baele P., Vaneechoutte M., Storms V., Butaye P., Devriese L. A., Verschraegen G., Gillis M., Haesebrouck F. 2000; Application of tRNA intergenic spacer PCR for identification of Enterococcus species. J Clin Microbiol 38:4201–4207
    [Google Scholar]
  2. Bailly X., Olivieri I., de Mita S., Cleyet-Marel J.-C., Béna G. 2006; Recombination and selection shape the molecular diversity pattern of nitrogen-fixing Sinorhizobium sp. associated to Medicago . Mol Ecol 15:2719–2734 [CrossRef]
    [Google Scholar]
  3. Balkwill D. L. 2005; Genus VI. Ensifer Casida 1982, 343VP. In Bergey'sManual of Systematic Bacteriology . , 2nd edn. vol. 2, part C pp 354–358 Edited by Brenner D. J., Staley N. R. Krieg J. T., Garrity G. M. New York: Springer;
  4. Bertrand H. 1997 Stimulation de l'absorption minérale et de la croissance du Colza inoculé avec des bactéries isolées de son rhizoplan. PhD thesis, Université Claude Bernard-Lyon I (in French)
  5. Casida L. E. Jr 1982; Ensifer adhaerens gen. nov., sp. nov. a bacterial predator of bacteria in soil. Int J Syst Bacteriol 32339–345 [CrossRef]
    [Google Scholar]
  6. Coenye T., Gevers D., Van de Peer Y., Vandamme P., Swings J. 2005; Towards a prokaryotic genomic taxonomy. FEMS Microbiol Rev 29:147–167
    [Google Scholar]
  7. de Lajudie P., Willems A., Pot B., Dewettinck D., Maestrojuan G., Neyra M., Collins M. D., Dreyfus B. L., 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]
  8. Debellé F., Moulin L., Mangin B., Dénarié J., Boivin C. 2001; nod genes and Nod signals and the evolution of the Rhizobium legume symbiosis. Acta Biochim Pol 48:359–365
    [Google Scholar]
  9. Eardly B. D., Nour S. M., van Berkum P., Selander R. K. 2005; Rhizobial 16S rRNA and dnaK genes: mosaicism and the uncertain phylogenetic placement of Rhizobium galegae . Appl Environ Microbiol 71:1328–1335 [CrossRef]
    [Google Scholar]
  10. 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 39:224–229 [CrossRef]
    [Google Scholar]
  11. Farris J. S., Källersjö M., Kluge A. G., Bult C. 1995; Constructing a significance test for incongruence. Syst Biol 44:570–572 [CrossRef]
    [Google Scholar]
  12. Ferchichi A. 1996; La lutte contre l’ensablement et pour la stabilisation des dunes: essai de la fixation biologique des dunes en Tunisie presaharienne. Recherche sur la désertification dans la Jeffara. Rev Tunis Geogr 12:49–102 (in French
    [Google Scholar]
  13. 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]
    [Google Scholar]
  14. Gevers D., Cohan F. M., Lawrence J. G., Spratt B. G., Coenye T., Feil E. J., Stackebrandt E., Van de Peer Y., Vandamme P. & other authors; 2005; Opinion: re-evaluating prokaryotic species. Nat Rev Microbiol 3:733–739 [CrossRef]
    [Google Scholar]
  15. Giraud E., Moulin L., Vallenet D. other authors 2007; Legumes symbioses: absence of Nod genes in photosynthetic bradyrhizobia. Science 316:1307–1312 [CrossRef]
    [Google Scholar]
  16. 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 44:1148–1153 [CrossRef]
    [Google Scholar]
  17. 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
    [Google Scholar]
  18. Hernandez-Lucas I., Rogel-Hernandez M. A., Segovia L., Rojas-Jiménez K., Martinez-Romero E. 2004; Phylogenetic relationships of rhizobia based on citrate synthase gene sequences. Syst Appl Microbiol 27:703–706 [CrossRef]
    [Google Scholar]
  19. Judicial Commission of the International Committee on Systematics of Prokaryotes 2008 The genus name Sinorhizobium Chen et al. 1988 is a later synonym of Ensifer Casida 1982 and is not conserved over the latter genus name, and the species name ‘ Sinorhizobium adhaerens ’ is not validly published. Opinion 84. Int J Syst Evol Microbiol 58, 1973 [CrossRef]
  20. Kersters K., De Ley J. 1984; Genus III. Agrobacterium Conn 1942. In Bergey'sManual of Systematic Bacteriology vol 1 pp 244–254 Edited by Krieg N. R., Holt J. G. Baltimore: The Williams & Wilkins Co;
    [Google Scholar]
  21. Kimura M. 1980; A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120 [CrossRef]
    [Google Scholar]
  22. 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]
    [Google Scholar]
  23. Lortet G., Mear N., Lorquin J., Dreyfus B., de Lajudie P., Rosenberg C., Boivin C. 1996; Nod factor thin-layer chromatography profiling as a tool to characterize symbiotic specificity of rhizobial strains: application to Sinorhizobium saheli, S. teranga and Rhizobium sp. strains isolated from Acacia and Sesbania . Mol Plant Microbe Interact 9:736–747 [CrossRef]
    [Google Scholar]
  24. Mahdhi M., Nzoué A., Gueye F., Merabet C., de Lajudie P., Mars M. 2007; Phenotypic and genotypic diversity of Genista saharae microsymbionts from the infra-arid region of Tunisia. Lett Appl Microbiol 45:604–609 [CrossRef]
    [Google Scholar]
  25. Mahdhi M., de Lajudie P., Mars M. 2008; Phylogenetic and symbiotic characterization of rhizobial bacteria nodulating Argyrolobium uniflorum in Tunisian arid soils. Can J Microbiol 54:209–217 [CrossRef]
    [Google Scholar]
  26. Mantelin S., Fischer-Le Saux M., Zakhia F., Béna G., Bonneau S., Jeder H., de Lajudie P., Cleyet-Marel J. C. 2006; Emended description of the genus Phyllobacterium and description of four novel species associated with plant roots Phyllobacterium bourgognense sp.nov., Phyllobacterium ifriqiyense sp. nov., Phyllobacterium leguminum sp. nov. and Phyllobacterium brassicacearum sp. nov. Int J Syst Evol Microbiol 56:827–839 [CrossRef]
    [Google Scholar]
  27. Marmur J. 1961; A procedure for the isolation of deoxyribonucleic acid from microorganisms. J Mol Biol 3:208–218 [CrossRef]
    [Google Scholar]
  28. 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]
    [Google Scholar]
  29. 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]
    [Google Scholar]
  30. Moulin L., Béna G., Boivin-Masson C., Stepkowski T. 2004; Phylogenetic analyses of symbiotic nodulation genes support vertical and lateral gene co-transfer within the Bradyrhizobium genus. Mol Phylogenet Evol 30:720–732 [CrossRef]
    [Google Scholar]
  31. Naser S. M., Thompson F. L., Hoste B., Gevers D., Dawyndt P., Vancanneyt M., Swings J. 2005; Application of multilocus sequence analysis (MLSA) for rapid identification of Enterococcus species based on rpoA and pheS genes. Microbiology 151:2141–2150 [CrossRef]
    [Google Scholar]
  32. Posada D., Buckley T. R. 2004; Model selection and model averaging in phylogenetics: advantages of the Akaike Information Criterion and Bayesian approaches over likelihood ratio tests. Syst Biol 53:793–808 [CrossRef]
    [Google Scholar]
  33. Posada D., Crandall K. A. 1998; MODELTEST: testing the model of DNA substitution. Bioinformatics 14:817–818 [CrossRef]
    [Google Scholar]
  34. 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]
    [Google Scholar]
  35. Rogel M. A., Hernandez-Lucas I., Kuykendall L. D., Balkwill D. L., Martínez-Romero E. 2001; Nitrogen-fixing nodules with Ensifer adhaerens harbouring Rhizobium tropici symbiotic plasmids. Appl Environ Microbiol 67:3264–3268 [CrossRef]
    [Google Scholar]
  36. Saitou N., Nei M. 1987; The neighbour joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425
    [Google Scholar]
  37. Schouls L. M., Schot C. S., Jacobs J. A. 2003; Horizontal transfer of segments of the 16S rRNA genes between species of the Streptococcus anginosus group. J Bacteriol 185:7241–7246 [CrossRef]
    [Google Scholar]
  38. Soler L., Yáñez M. A., Chacon M. R., Aguilera-Arreola M. G., Catalán V., Figueras M. J., Martínez-Murcia A. J. 2004; Phylogenetic analysis of the genus Aeromonas based on two housekeeping genes. Int J Syst Evol Microbiol 54:1511–1519
    [Google Scholar]
  39. Stackebrandt E. 2003; The richness of prokaryotic diversity: there must be a species somewhere. Food Technol Biotechnol 41:17–22
    [Google Scholar]
  40. Stackebrandt E., Frederiksen W., Garrity G. M., Grimont P. A., Kämpfer P., Maiden M. C., Nesme X., Rosselló-Mora R., Swings J. other authors 2002; Report of the ad hoc committee for the re-evaluation of the species definition in bacteriology. Int J Syst Evol Microbiol 52:1043–1047 [CrossRef]
    [Google Scholar]
  41. Stepkowski T., Czaplinska M., Miedzinska K., Moulin L. 2003; The variable part of the dnaK gene as an alternative marker for phylogenetic studies of rhizobia and related alpha Proteobacteria. Syst Appl Microbiol 26:483–494 [CrossRef]
    [Google Scholar]
  42. Swofford D. L. 2002 paup*: Phylogenetic analysis using parsimony (and other methods), version 4 Sunderland, MA: Sinauer Associates;
    [Google Scholar]
  43. 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]
    [Google Scholar]
  44. Toledo I., Lloret L., Martínez-Romero E. 2003; Sinorhizobium americanum sp. nov., a new Sinorhizobium species nodulating native Acacia spp. in Mexico. Syst Appl Microbiol 26:54–64 [CrossRef]
    [Google Scholar]
  45. Turner S. L., Young J. P. W. 2000; The glutamine synthetases of rhizobia: phylogenetics and evolutionary implications. Mol Biol Evol 17:309–319 [CrossRef]
    [Google Scholar]
  46. Ueda K., Seki T., Kudo T., Yoshida T., Kataoka M. 1999; Two distinct mechanisms cause heterogeneity of 16S rRNA. J Bacteriol 181:78–82
    [Google Scholar]
  47. 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 185:2988–2998 [CrossRef]
    [Google Scholar]
  48. 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
    [Google Scholar]
  49. Vinuesa P., Silva C., Lorite M. J., Izaguirre-Mayoral M. L., Bedmar E., Martinez-Romero E. 2005a; Molecular systematics of rhizobia based on maximum likelihood and Bayesian phylogenies inferred from rrs , atpD , recA and nifH sequences, and their use in the classification of Sesbania microsymbionts from Venezuelan wetlands. Syst Appl Microbiol 28:702–716 [CrossRef]
    [Google Scholar]
  50. Vinuesa P., Silva C., Werner D., Martinez-Romero E. 2005b; 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
    [Google Scholar]
  51. Vinuesa P., León-Barrios M., Silva C., Willems A., Jarabo-Lorenzo A., Pérez-Galdona R., Martínez-Romero E. 2005c; Bradyrhizobium canariense sp. nov., an acid-tolerant endosymbiont that nodulates endemic genistoid legumes (Papilionoideae: Genisteae) growing in the Canary Islands, along with Bradyrhizobium japonicum bv. genistearum , Bradyrhizobium genospecies alpha and Bradyrhizobium genospecies beta. Int J Syst Evol Microbiol 55:569–575
    [Google Scholar]
  52. Wang E. T., Tan Z. Y., Willems A., Fernandez-Lopez M., Reinhold-Hurek B., Martinez-Romero E. 2002; Sinorhizobium morelense sp. nov., a Leucaena leucocephala -associated bacterium that is highly resistant to multiple antibiotics. Int J Syst Evol Microbiol 52:1687–1693
    [Google Scholar]
  53. Wei G. H., Wang E. T., Tan Z. Y., Zhu M. E., Chen W. X. 2002; Rhizobium indigoferae sp. nov. and Sinorhizobium kummerowiae sp. nov., respectively isolated from Indigofera spp; and Kummerowia stipulacea . Int J Syst Evol Microbiol 52:2231–2239
    [Google Scholar]
  54. Wertz J. E., Goldstone C., Gordon D. M., Riley M. A. 2003; A molecular phylogeny of enteric bacteria and implications for a bacterial species concept. J Evol Biol 16:1236–1248 [CrossRef]
    [Google Scholar]
  55. Willems A., Doignon-Bourcier F., Goris J., Coopman R., de Lajudie P., De Vos P., Gillis M. 2001; DNA-DNA hybridization study of Bradyrhizobium strains. Int J Syst Evol Microbiol 51:1315–1322
    [Google Scholar]
  56. Willems A., Fernandez-Lopez M., Munoz-Adelantado E., 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]
    [Google Scholar]
  57. 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 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]
    [Google Scholar]
  58. Zakhia F. 2004; Diversité des bactéries hôtes de légumineuses méditerranéennes en Tunisie et au Liban. PhD thesis Université de Montpellier, France (in French
  59. Zakhia F., Jeder H., Domergue O., Willems A., Cleyet-Marel J.-C., Gillis M., Dreyfus B., de Lajudie P. 2004; Characterisation of wild legume nodulating bacteria (LNB) in the infa-arid zone of Tunisia. Syst Appl Microbiol 27:380–395 [CrossRef]
    [Google Scholar]
  60. Zakhia F., Jeder H., Willems A., Dreyfus B., de Lajudie P. 2006; Diverse bacteria associated with root nodules of spontaneous legumes in Tunisia and first report for nifH -like gene within the genera Microbacterium and Starkeya . Microb Ecol 51:375–393 [CrossRef]
    [Google Scholar]
  61. Zeigler D. R. 2003; Gene sequences useful for predicting relatedness of whole genomes in bacteria. Int J Syst Evol Microbiol 53:1893–1900 [CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/ijsem/10.1099/ijs.0.012088-0
Loading
/content/journal/ijsem/10.1099/ijs.0.012088-0
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF

Supplementary material 2

PDF

Supplementary material 3

PDF

Supplementary material 4

PDF
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