1887

Abstract

Two Gram-negative, aerobic, non-motile, rod-shaped bacterial strains, FH13 and FH23, representing a novel group of isolated from root nodules of in Mexico, were studied by a polyphasic analysis. Phylogeny of 16S rRNA gene sequences revealed them to be members of the genus related most closely to ‘’ CCBAU 23252 (99.7 % similarity), USDA 2370 (98.6 %), and CCBAU 03386 and others ( ≤ 98.3 %). In sequence analyses of the housekeeping genes and both strains formed a subclade distinct from all defined species of the genus at sequence similarities of 82.3–94.0 %, demonstrating that they represented a novel genomic species in the genus . Mean levels of DNA–DNA relatedness between the reference strain FH13 and the type strains of related species varied between 13.0 ± 2.0 and 52.1 ± 1.2 %. The DNA G+C content of strain FH13 was 63.5 mol% ( ). The major cellular fatty acids were 16 : 0, 17 : 0 anteiso, 18 : 0, summed feature 2 (12 : 0 aldehyde/unknown 10.928) and summed feature 8 (18 : 1ω7). The fatty acid 17 : 1ω5 was unique for this strain. Some phenotypic features, such as failure to utilize adonitol, -arabinose, -fructose and -fucose, and ability to utilize -galacturonic acid and itaconic acid as carbon source, could also be used to distinguish strain FH13 from the type strains of related species. Based upon these results, a novel species, sp. nov., is proposed, with FH13 ( = CCBAU 101094 = HAMBI 3626 = LMG 28672) as the type strain.

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2016-01-01
2020-01-22
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References

  1. Altschul S. F., Madden T. L., Schäffer A. A., Zhang J., Zhang Z., Miller W., Lipman D. J.. 1997; Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res25:3389–3402[CrossRef]
    [Google Scholar]
  2. Aserse A. A., Räsänen L. A., Assefa F., Hailemariam A., Lindström K.. 2012; Phylogeny and genetic diversity of native rhizobia nodulating common bean (Phaseolus vulgaris L.) in Ethiopia. Syst Appl Microbiol35:120–131 [CrossRef][PubMed]
    [Google Scholar]
  3. Campanella J. J., Bitincka L., Smalley J.. 2003; MatGAT: an application that generates similarity/identity matrices using protein or DNA sequences. BMC Bioinformatics4:29 [CrossRef][PubMed]
    [Google Scholar]
  4. Collins M., Jones D.. 1980; Lipids in the classification and identification of coryneform bacteria containing peptidoglycans based on 2,4-diaminobutyric acid. J Appl Microbiol48:459–470
    [Google Scholar]
  5. Cowan S. T., Steel K. J.. 1965; Manual for the Identification of Medical Bacteria London: Cambridge University Press;
    [Google Scholar]
  6. De Ley J., Cattoir H., Reynaerts A.. 1970; The quantitative measurement of DNA hybridization from renaturation rates. Eur J Biochem12:133–142 [CrossRef][PubMed]
    [Google Scholar]
  7. Galtier N., Gouy M., Gautier C.. 1996; seaview phylo_win: two graphic tools for sequence alignment and molecular phylogeny. Comput Appl Biosci12:543–548[PubMed]
    [Google Scholar]
  8. Graham P. H., Sadowsky M. J., Keyser H. H., Barnet Y. M., Bradley R. S., Cooper J. E., De Ley D. J., Jarvis B. D. W., Roslycky E. B., other authors. 1991; Proposed minimal standards for the description of new genera and species of root-and stem-nodulating bacteria. Int J Syst Bacteriol41:582–587 [CrossRef]
    [Google Scholar]
  9. Guindon S., Gascuel O.. 2003; A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol52:696–704 [CrossRef][PubMed]
    [Google Scholar]
  10. Guindon S., Dufayard J. F., Lefort V., Anisimova M., Hordijk W., Gascuel O.. 2010; New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol59:307–321 [CrossRef][PubMed]
    [Google Scholar]
  11. Jiao Y. S., Yan H., Ji Z. J., Liu Y. H., Sui X. H., Wang E. T., Guo B. L., Chen W. X., Chen W. F.. 2015; Rhizobium sophorae sp. nov. and Rhizobium sophoriradicis sp. nov., nitrogen-fixing rhizobial symbionts of the medicinal legume Sophora flavescens . Int J Syst Evol Microbiol65:497–503[PubMed][CrossRef]
    [Google Scholar]
  12. 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. Microbiology147:981–993[CrossRef]
    [Google Scholar]
  13. Lin S. Y., Hung M. H., Hameed A., Liu Y. C., Hsu Y. H., Wen C. Z., Arun A. B., Busse H. J., Glaeser S. P.. otherauthors 2015; Rhizobium capsici sp. nov., isolated from root tumor of a green bell pepper (Capsicum annuum var. grossum) plant. Antonie van Leeuwenhoek107:773–784 [CrossRef][PubMed]
    [Google Scholar]
  14. Marmur J.. 1961; A procedure for the isolation of dexoxyribonucleic acid from micro-organisms. J Mol Biol3:208–218 [CrossRef]
    [Google Scholar]
  15. Marmur J., Doty P.. 1962; Determination of the base composition of deoxyribonucleic acid from its thermal denaturation temperature. J Mol Biol5:109–118 [CrossRef][PubMed]
    [Google Scholar]
  16. 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 Microbiol58:200–214 [CrossRef][PubMed]
    [Google Scholar]
  17. Minnikin D., O'Donnell A., Goodfellow M., Alderson G., Athalye M., Schaal A., Parlett J.. 1984; An integrated procedure for the extraction of bacterial isoprenoid quinones and polar lipids. J Microbiol Methods2:233–241 [CrossRef]
    [Google Scholar]
  18. Mnasri B., Saı¨di, S., Chihaoui S. A., Mhamdi R.. 2012; Sinorhizobium americanum symbiovar mediterranense is a predominant symbiont that nodulates and fixes nitrogen with common bean (Phaseolus vulgaris L.) in a Northern Tunisian field. Syst Appl Microbiol35:263–269 [CrossRef][PubMed]
    [Google Scholar]
  19. Mousavi S. A., Österman J., Wahlberg N., Nesme X., Lavire C., Vial L., Paulin L., de Lajudie P., Lindström K.. 2014; Phylogeny of the Rhizobium–Allorhizobium–Agrobacterium clade supports the delineation of Neorhizobium gen. nov. Syst Appl Microbiol37:208–215 [CrossRef][PubMed]
    [Google Scholar]
  20. Mousavi S. A., Willems A., Nesme X., de Lajudie P., Lindström K.. 2015; Revised phylogeny of Rhizobiaceae: proposal of the delineation of Pararhizobium gen. nov., and 13 new species combinations. Syst Appl Microbiol38:84–90 [CrossRef][PubMed]
    [Google Scholar]
  21. Posada D.. 2008; jModelTest: phylogenetic model averaging. Mol Biol Evol25:1253–1256 [CrossRef][PubMed]
    [Google Scholar]
  22. Quan Z. X., Bae H. S., Baek J. H., Chen W. F., Im W. T., Lee S. T.. 2005; Rhizobium daejeonense sp. nov. isolated from a cyanide treatment bioreactor. Int J Syst Evol Microbiol55:2543–2549 [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 Microbiol58:2484–2490 [CrossRef][PubMed]
    [Google Scholar]
  24. Rashid M. H., Young J. P., Everall I., Clercx P., Willems A., Santhosh Braun M., Wink M.. 2015; Average nucleotide identity of genome sequences supports the description of Rhizobium lentis sp. nov., Rhizobium bangladeshense sp. nov. and Rhizobium binae sp. nov. from lentil (Lens culinaris) nodules. Int J Syst Evol Microbiol65:3037–3045 [CrossRef][PubMed]
    [Google Scholar]
  25. Richter M., Rosselló-Móra R.. 2009; Shifting the genomic gold standard for the prokaryotic species definition. Proc Natl Acad Sci U S A106:19126–19131 [CrossRef][PubMed]
    [Google Scholar]
  26. Rogers J. S., Swofford D. L.. 1999; Multiple local maxima for likelihoods of phylogenetic trees: a simulation study. Mol Biol Evol16:1079–1085 [CrossRef][PubMed]
    [Google Scholar]
  27. Roselló-Morá R., Urdiain M., López-López A.. 2011; DNA–DNA hybrization. Methods Microbiol38:325–348 [CrossRef]
    [Google Scholar]
  28. Rozahon M., Ismayil N., Hamood B., Erkin R., Abdurahman M., Mamtimin H., Abdukerim M., Lal R., Rahman E.. 2014; Rhizobium populi sp. nov., an endophytic bacterium isolated from Populus euphratica. Int J Syst Evol Microbiol64:3215–3221 [CrossRef][PubMed]
    [Google Scholar]
  29. Saitou N., Nei M.. 1987; The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol4:406–425[PubMed]
    [Google Scholar]
  30. 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 Ecol54:1–11 [CrossRef][PubMed]
    [Google Scholar]
  31. Sasser M.. 1990; Identification of bacteria by gas chromatography of cellular fatty acids MIDI Technical Note 101; Newark, DE: MIDI Inc:
    [Google Scholar]
  32. Talbi C., Delgado M. J., Girard L., Ramírez-Trujillo A., Caballero-Mellado J., Bedmar E. J.. 2010; Burkholderia phymatum strains capable of nodulating Phaseolus vulgaris are present in Moroccan soils. Appl Environ Microbiol76:4587–4591 [CrossRef][PubMed]
    [Google Scholar]
  33. 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 Evol28:2731–2739 [CrossRef][PubMed]
    [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 Biotechnol91:169–180 [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 Res25:4876–4882 [CrossRef][PubMed]
    [Google Scholar]
  36. Tighe S. W., de Lajudie P., Dipietro K., Lindström K., Nick G., Jarvis B. D.. 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 Microbiol50:787–801 [CrossRef][PubMed]
    [Google Scholar]
  37. Verástegui-Valdés M. M., Zhang Y. J., Rivera-Orduña F. N., Cheng H. P., Sui X. H., Wang E. T.. 2014; Microsymbionts of Phaseolus vulgaris in acid and alkaline soils of Mexico. Syst Appl Microbiol37:605–612 [CrossRef][PubMed]
    [Google Scholar]
  38. Vincent J. M.. 1970; A Manual for the Practical Study of Root Nodule Bacteria Oxford: Blackwell Scientific;
    [Google Scholar]
  39. Vinuesa P., Silva C., Lorite M. J., Izaguirre-Mayoral M. L., Bedmar E. J., Martínez-Romero E.. 2005; 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 Microbiol28:702–716 [CrossRef][PubMed]
    [Google Scholar]
  40. Wayne L. G., Brenner D. J., 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; International Committee on Systematic Bacteriology. Report of the ad hoc committee on reconciliation of approaches to bacterial systematics. Int J Syst Bacteriol37:463–464 [CrossRef]
    [Google Scholar]
  41. Zhang X. X., Tang X., Sheirdil R. A., Sun L., Ma X. T.. 2014; Rhizobium rhizoryzae sp. nov., isolated from rice roots. Int J Syst Evol Microbiol64:1373–1377 [CrossRef][PubMed]
    [Google Scholar]
  42. Zhang Y. J., Zheng W. T., Everall I., Yong Y. P., Zhang X. X., Tian C. F., Sui X. H., Wang E. T., Chen W. X.. 2015; Rhizobium anhuiense sp. nov., isolated from effective nodule of Vicia faba and Pisum sativum . Int J Syst Evol Microbiol65:2960–2967 [CrossRef]
    [Google Scholar]
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