1887

INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY logo

Volume 69, Issue 12

sp. nov., a nitrogen-fixing lineage isolated from nodules of the caesalpinioid species and characterized by tolerance to high temperature Free

Abstract

The symbioses between legumes and nitrogen-fixing rhizobia make the greatest contribution to the global nitrogen input via the process of biological nitrogen fixation (BNF). stands out as the main genus nodulating basal Caesalpinioideae. We performed a polyphasic study with 11 strains isolated from root nodules of , an annual multi-functional native legume of the USA. In the 16S rRNA gene phylogeny the strains were clustered in the superclade. The results of analysis of the intergenic transcribed spacer (ITS) indicated less than 89.9 % similarity to other species. Multilocus sequence analysis (MLSA) with four housekeeping genes (, , and ) confirmed the new group, sharing less than 95.2 % nucleotide identity with other species. The MLSA with 10 housekeeping genes (, , , , , , , , and ) indicated as the closest species. Noteworthy, high genetic diversity among the strains was confirmed in the analyses of ITS, MLSA and BOX-PCR. Average nucleotide identity and digital DNA–DNA hybridization values were below the threshold of described species, of 89.7 and 40 %, respectively. In the and phylogenies, the strains were grouped together, but with an indication of horizontal gene transfer, showing higher similarity to and . Other phenotypic, genotypic and symbiotic properties were evaluated, and the results altogether support the description of the CNPSo strains as representatives of the new species sp. nov., with CNPSo 3426 (=USDA 10052=U686=CL 20) as the type strain.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): ANI , biological nitrogen fixation , Caesalpinioideae , MLSA and nodulation
© 2019 The Authors
Loading

Article metrics loading...

/content/journal/ijsem/10.1099/ijsem.0.003697
2019-12-01
2024-04-20
Loading full text...

Full text loading...

/deliver/fulltext/ijsem/69/12/3863.html?itemId=/content/journal/ijsem/10.1099/ijsem.0.003697&mimeType=html&fmt=ahah

References

  1. Ormeño-Orrillo E, Hungria M, Martínez-Romero E. Dinitrogen-fixing prokaryotes. In Rosenberg E. (editor) The Prokaryotes – Prokaryotic Physiology and Biochemistry Berlin Heidelberg: Springer-Verlag; 2013 pp. 427–451
     [Google Scholar]
  2. Ahnia H, Bourebaba Y, Durán D, Boulila F, Palacios JM et al. Bradyrhizobium algeriense sp. nov., a novel species isolated from effective nodules of Retama sphaerocarpa from Northeastern Algeria. Syst Appl Microbiol 2018; 41:333–339 [View Article][PubMed]
     [Google Scholar]
  3. Araújo J, Flores-Félix JD, Igual JM, Peix A, González-Andrés F et al. Bradyrhizobium cajani sp. nov. isolated from nodules of Cajanus cajan . Int J Syst Evol Microbiol 2017; 67:2236–2241 [View Article][PubMed]
     [Google Scholar]
  4. Aserse A, Woyke T, Kyrpides N, Whitman WB, Lindstrom K. Draft genome sequences of Bradyrhizobium shewense sp. nov. ERR11 T and Bradyrhizobium yuanmingense CCBAU 10071T. Stand Genomic Sci 2017; 12:1–14
     [Google Scholar]
  5. Bünger W, Grönemeyer JL, Sarkar A, Reinhold-Hurek B. Bradyrhizobium ripae sp. nov., a nitrogen-fixing symbiont isolated from nodules of wild legumes in Namibia. Int J Syst Evol Microbiol 2018; 68:3688–3695 [View Article][PubMed]
     [Google Scholar]
  6. Helene LCF, Delamuta JRM, Ribeiro RA, Hungria M. Bradyrhizobium mercantei sp. nov., a nitrogen-fixing symbiont isolated from nodules of Deguelia costata (syn. Lonchocarpus costatus). Int J Syst Evol Microbiol 2017; 67:1827–1834 [View Article][PubMed]
     [Google Scholar]
  7. Martins da Costa E, Azarias Guimarães A, Soares de Carvalho T, Louzada Rodrigues T, de Almeida Ribeiro PR et al. Bradyrhizobium forestalis sp. nov., an efficient nitrogen-fixing bacterium isolated from nodules of forest legume species in the Amazon. Arch Microbiol 2018; 200:743–752 [View Article][PubMed]
     [Google Scholar]
  8. de Matos GF, Zilli JE, de Araújo JLS, Parma MM, Melo IS et al. Bradyrhizobium sacchari sp. nov., a legume nodulating bacterium isolated from sugarcane roots. Arch Microbiol 2017; 199:1251–1258 [View Article][PubMed]
     [Google Scholar]
  9. Michel DC, Passos SR, Simões-Araujo JL, Baraúna AC, da Silva K et al. Bradyrhizobium centrolobii and Bradyrhizobium macuxiense sp. nov. isolated from Centrolobium paraense grown in soil of Amazonia, Brazil. Arch Microbiol 2017; 199:657–664 [View Article]
     [Google Scholar]
  10. Hungria M, Menna P, Bradyrhizobium D. the ancestor of all rhizobia: phylogeny of housekeeping and nitrogen-fixation genes. In de Bruijn FJ. (editor) Biological Nitrogen Fixation New Jersey: John Wiley, Sons, Inc.; 2015 pp. 191–202
     [Google Scholar]
  11. Parker MA. The spread of Bradyrhizobium lineages across host legume clades: from Abarema to Zygia. Microb Ecol 2015; 69:630–640 [View Article][PubMed]
     [Google Scholar]
  12. Sprent JI, James EK. Legume evolution: where do nodules and mycorrhizas fit in?. Plant Physiol 2007; 144:575–581 [View Article][PubMed]
     [Google Scholar]
  13. Allen ON, Allen EK. The Leguminosae: A sourcebook of Characteristics, Uses, and Nodulation Madison/London, U.S.A. /U.K: University of Wisconsin Press/MacMillan Publishers Ltd; 1981
     [Google Scholar]
  14. Faria SM, Franco AA, Jesus RM, Menandro Mdes, Baitello JB et al. New nodulating legume trees from south-east brazil. New Phytologist 1984; 98:317–328 [View Article]
     [Google Scholar]
  15. Naisbitt T, James EK, Sprent JI. The evolutionary significance of the legume genus Chamaecrista, as determined by nodule structure. New Phytologist 1992; 122:487–492 [View Article]
     [Google Scholar]
  16. Sprent JI, Ardley J, James EK. Biogeography of nodulated legumes and their nitrogen-fixing symbionts. New Phytol 2017; 215:40–56 [View Article][PubMed]
     [Google Scholar]
  17. Diabate M, Munive A, de Faria SM, Ba A, Dreyfus B et al. Occurrence of nodulation in unexplored leguminous trees native to the West African tropical rainforest and inoculation response of native species useful in reforestation. New Phytol 2005; 166:231–239 [View Article][PubMed]
     [Google Scholar]
  18. de Faria SM, Diedhiou AG, de Lima HC, Ribeiro RD, Galiana A et al. Evaluating the nodulation status of leguminous species from the Amazonian forest of Brazil. J Exp Bot 2010; 61:3119–3127 [View Article][PubMed]
     [Google Scholar]
  19. Gehlot HS, Panwar D, Tak N, Tak A, Sankhla IS et al. Nodulation of legumes from the Thar desert of India and molecular characterization of their rhizobia. Plant Soil 2012; 357:227–243 [View Article]
     [Google Scholar]
  20. Parker MA, Kennedy DA. Diversity and relationships of bradyrhizobia from legumes native to eastern North America. Can J Microbiol 2006; 52:1148–1157 [View Article][PubMed]
     [Google Scholar]
  21. Moreira FM, Haukka K, Young JP. Biodiversity of rhizobia isolated from a wide range of forest legumes in Brazil. Mol Ecol 1998; 7:889–895 [View Article][PubMed]
     [Google Scholar]
  22. Parker MA, Rousteau A. Molecular Phylogenetics and Evolution Mosaic origins of Bradyrhizobium legume symbionts on the Caribbean island of Guadeloupe. Mol Phylogenet Evol 2014; 77:110–115
     [Google Scholar]
  23. Santos JM, Casaes Alves PA, Silva VC, Kruschewsky Rhem MF, James EK et al. Diverse genotypes of Bradyrhizobium nodulate herbaceous Chamaecrista (Moench) (Fabaceae, Caesalpinioideae) species in Brazil. Syst Appl Microbiol 2017; 40:69–79 [View Article][PubMed]
     [Google Scholar]
  24. Rathi S, Tak N, Bissa G, Chouhan B, Ojha A et al. Selection of Bradyrhizobium or Ensifer symbionts by the native Indian caesalpinioid legume Chamaecrista pumila depends on soil pH and other edaphic and climatic factors. FEMS Microbiol Ecol 2018; 94:1–17 [View Article]
     [Google Scholar]
  25. Somasegaran P, Hoben H. Methods in Legume-Rhizobium Technology. Handbook for Rhizobia Springer Verlag; 1985 pp. 450
     [Google Scholar]
  26. Morris JB. Showy partridge pea [Chamaecrista fasciculata (Michx.) Greene] with potential for cultivation as a multi-functional species in the United States. Genetic Resources and Crop Evolution 2012; 59:1577–1581 [View Article]
     [Google Scholar]
  27. Hungria M, O’Hara GW, Zilli JE et al. Isolation and growth of rhizobia. Working with rhizobia 2016; 315:2016
     [Google Scholar]
  28. Delamuta JR, Ribeiro RA, Ormeño-Orrillo E, Melo IS, Martínez-Romero E et al. Polyphasic evidence supporting the reclassification of Bradyrhizobium japonicum group Ia strains as Bradyrhizobium diazoefficiens sp. nov. Int J Syst Evol Microbiol 2013; 63:3342–3351 [View Article][PubMed]
     [Google Scholar]
  29. Laguerre G, Nour SM, Macheret V, Sanjuan J, Drouin P et al. Classification of rhizobia based on nodC and nifH gene analysis reveals a close phylogenetic relationship among Phaseolus vulgaris symbionts. Microbiology 2001; 147:981–993 [View Article][PubMed]
     [Google Scholar]
  30. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Mol Biol Evol 2013; 30:2725–2729 [View Article][PubMed]
     [Google Scholar]
  31. Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 2004; 32:1792–1797 [View Article][PubMed]
     [Google Scholar]
  32. Darriba D, Taboada GL, Doallo R, Posada D. jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 2012; 9:772 [View Article][PubMed]
     [Google Scholar]
  33. Zwickl DJ. Genetic algorithm approaches for the phylogenetic analysis of large biological sequence datasets under the maximum likelihood criterion. University of Texas Eletronic Theses and Dissertations 2006
     [Google Scholar]
  34. Felsenstein J. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 1985; 39:1985783–791 [View Article][PubMed]
     [Google Scholar]
  35. Tamura K, Nei M. Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol 1993; 10:512-26 [View Article][PubMed]
     [Google Scholar]
  36. Hall T. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 1999; 41:95–98
     [Google Scholar]
  37. Delamuta JR, Ribeiro RA, Araújo JL, Rouws LF, Zilli JÉ et al. Bradyrhizobium stylosanthis sp. nov., comprising nitrogen-fixing symbionts isolated from nodules of the tropical forage legume Stylosanthes spp. Int J Syst Evol Microbiol 2016; 66:3078–3087 [View Article][PubMed]
     [Google Scholar]
  38. Menna P, Barcellos FG, Hungria M. 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 2009; 59:2934–2950 [View Article][PubMed]
     [Google Scholar]
  39. Willems A, Coopman R, Gillis M. Comparison of sequence analysis of 16S-23S rDNA spacer regions, AFLP analysis and DNA-DNA hybridizations in Bradyrhizobium . Int J Syst Evol Microbiol 2001; 51:623–632 [View Article][PubMed]
     [Google Scholar]
  40. Tavaré S. Some probabilistic and statistical problems in the analysis of DNA sequences. Lectures Math Life Sci 1986; 17:57–86
     [Google Scholar]
  41. Durán D, Rey L, Mayo J, Zúñiga-Dávila D, Imperial J et al. Bradyrhizobium paxllaeri sp. nov. and Bradyrhizobium icense sp. nov., nitrogen-fixing rhizobial symbionts of Lima bean (Phaseolus lunatus L.) in Peru. Int J Syst Evol Microbiol 2014; 64:2072–2078 [View Article][PubMed]
     [Google Scholar]
  42. Menna P, Hungria M. Phylogeny of nodulation and nitrogen-fixation genes in Bradyrhizobium: supporting evidence for the theory of monophyletic origin, and spread and maintenance by both horizontal and vertical transfer. Int J Syst Evol Microbiol 2011; 61:3052–3067 [View Article][PubMed]
     [Google Scholar]
  43. Barcellos FG, Menna P, da Silva Batista JS, Hungria M. Evidence of horizontal transfer of symbiotic genes from a Bradyrhizobium japonicum inoculant strain to indigenous diazotrophs Sinorhizobium (Ensifer) fredii and Bradyrhizobium elkanii in a Brazilian Savannah soil. Appl Environ Microbiol 2007; 73:2635–2643 [View Article][PubMed]
     [Google Scholar]
  44. Batista JS, Hungria M, Barcellos FG, Ferreira MC, Mendes IC. Variability in Bradyrhizobium japonicum and B. elkanii seven years after introduction of both the exotic microsymbiont and the soybean host in a cerrados soil. Microb Ecol 2007; 53:270–284 [View Article][PubMed]
     [Google Scholar]
  45. Vinuesa P, Silva C, Lorite MJ, Izaguirre-Mayoral ML, Bedmar EJ et al. 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 2005; 28:702–716 [View Article][PubMed]
     [Google Scholar]
  46. Remigi P, Zhu J, Young JPW, Masson-Boivin C. Symbiosis within Symbiosis: evolving nitrogen-fixing legume symbionts. Trends Microbiol 2016; 24:63–75 [View Article][PubMed]
     [Google Scholar]
  47. Rodriguez-R LM, Konstantinidis KT. The enveomics collection: a toolbox for specialized analyses of microbial genomes and metagenomes microbial genomes and metagenomes. PeerJ Prepr 2016; 4:1–15
     [Google Scholar]
  48. Gurevich A, Saveliev V, Vyahhi N, Tesler G. QUAST: quality assessment tool for genome assemblies. Bioinformatics 2013; 29:1072–1075 [View Article][PubMed]
     [Google Scholar]
  49. Konstantinidis KT, Tiedje JM. Genomic insights that advance the species definition for prokaryotes. Proc Natl Acad Sci USA 2005; 102:2567–2572 [View Article][PubMed]
     [Google Scholar]
  50. Goris J, Konstantinidis KT, Klappenbach JA, Coenye T, Vandamme P et al. DNA-DNA hybridization values and their relationship to whole-genome sequence similarities. Int J Syst Evol Microbiol 2007; 57:81–91 [View Article][PubMed]
     [Google Scholar]
  51. Meier-Kolthoff JP, Auch AF, Klenk HP, Göker M. Genome sequence-based species delimitation with confidence intervals and improved distance functions. BMC Bioinformatics 2013; 14:60–14 [View Article][PubMed]
     [Google Scholar]
  52. Richter M, Rosselló-Móra R. Shifting the genomic gold standard for the prokaryotic species definition. Proc Natl Acad Sci USA 2009; 106:19126–19131 [View Article][PubMed]
     [Google Scholar]
  53. Chun J, Oren A, Ventosa A, Christensen H, Arahal DR et al. Proposed minimal standards for the use of genome data for the taxonomy of prokaryotes. Int J Syst Evol Microbiol 2018; 68:461–466 [View Article][PubMed]
     [Google Scholar]
  54. Meier-Kolthoff JP, Klenk HP, Göker M. Taxonomic use of DNA G+C content and DNA-DNA hybridization in the genomic age. Int J Syst Evol Microbiol 2014; 64:352–356 [View Article][PubMed]
     [Google Scholar]
  55. Xu LM, Ge C, Cui Z, Li J, Fan H. Bradyrhizobium liaoningense sp. nov., isolated from the root nodules of soybeans. Int J Syst Bacteriol 1995; 45:706–711 [View Article][PubMed]
     [Google Scholar]
  56. Kaschuk G, Hungria M, Andrade DS, Campo RJ. Genetic diversity of rhizobia associated with common bean (Phaseolus vulgaris L.) grown under no-tillage and conventional systems in Southern Brazil. Applied Soil Ecology 2006; 32:210–220 [View Article]
     [Google Scholar]
  57. Sneath PHA, Sokal RR. Numerical taxonomy: the principles and practice of numerical classification. San Francisco: Freeman 1973; 573:
     [Google Scholar]
  58. Jaccard P. The distribution of the flora in the alpine zone.1. New Phytologist 1912; 11:37–50 [View Article]
     [Google Scholar]
  59. MIDI Sherlock Microbial Identification System Operating Manual, version 4.0. Newark: MIDI, Inc; 2001
     [Google Scholar]
  60. Tighe SW, de Lajudie P, Dipietro K, Lindström K, Nick G et al. 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 2000; 50:787–801 [View Article][PubMed]
     [Google Scholar]
  61. Xu LM, Ge C, Cui Z, Li J, Fan H et al. Bradyrhizobium liaoningense sp. nov., isolated from the root nodules of soybeans. Int J Syst Bacteriol 1995; 45:706–711 [View Article][PubMed]
     [Google Scholar]
  62. Zhang YM, Li Y, Chen WF, Wang ET, Sui XH et al. Bradyrhizobium huanghuaihaiense sp. nov., an effective symbiotic bacterium isolated from soybean (Glycine max L.) nodules. Int J Syst Evol Microbiol 2012; 62:1951–1957 [View Article][PubMed]
     [Google Scholar]
  63. Yu X, Cloutier S, Tambong JT, Bromfield ES. Bradyrhizobium ottawaense sp. nov., a symbiotic nitrogen fixing bacterium from root nodules of soybeans in Canada. Int J Syst Evol Microbiol 2014; 64:3202–3207 [View Article][PubMed]
     [Google Scholar]
  64. Wang JY, Wang R, Zhang YM, Liu HC, Chen WF et al. Bradyrhizobium daqingense sp. nov., isolated from soybean nodules. Int J Syst Evol Microbiol 2013; 63:616–624 [View Article][PubMed]
     [Google Scholar]
  65. Zilli JE, Baraúna AC, da Silva K, de Meyer SE, Farias EN et al. Bradyrhizobium neotropicale sp. nov., isolated from effective nodules of Centrolobium paraense . Int J Syst Evol Microbiol 2014; 64:3950–3957 [View Article][PubMed]
     [Google Scholar]
  66. Li YH, Wang R, Zhang XX, Young JP, Wang ET et al. Bradyrhizobium guangdongense sp. nov. and Bradyrhizobium guangxiense sp. nov., isolated from effective nodules of peanut. Int J Syst Evol Microbiol 2015; 65:4655–4661 [View Article][PubMed]
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/ijsem/10.1099/ijsem.0.003697
Loading
Bradyrhizobium frederickii sp. nov., a nitrogen-fixing lineage isolated from nodules of the caesalpinioid species Chamaecrista fasciculata and characterized by tolerance to high temperature in vitro
Int J Syst Evol Microbiol 69, 3863 (2019); https://doi.org/10.1099/ijsem.0.003697
/content/journal/ijsem/10.1099/ijsem.0.003697
/content/journal/ijsem/10.1099/ijsem.0.003697
Loading

Data & Media loading...

Supplements

Supplementary File 1

PDF

Most cited 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