1887

Abstract

strains are associated with soil, plants and animals, and known mainly by their pathogenicity. We studied 14 strains isolated from nodules of healthy soybean and common bean plants in Brazil, Mexico, Ecuador and Mozambique. Sequence analysis of the 16S rRNA gene positioned the strains as , but with low phylogenetic resolution. Multilocus sequence analysis (MLSA) of three partial housekeeping genes (, and ) positioned the strains in four distinct clades, with , , and sp. genomospecies G1. Analysis by BOX-PCR revealed high intraspecies diversity. Genomic analysis of representative strains of the three clades indicated that they carry the protelomerase gene, and MLSA analysis with six complete housekeeping genes (, , , , and ), as well as average nucleotide identity (less than 90 % with closest species) and digital DNA–DNA hybridization (less than 41 % with closest species) revealed that strain CNPSo 675 and sp. genomospecies G1 compose a new species. Other phenotypic and genotypic characteristics were determined for the new clade. Although not able to re-nodulate the host, we hypothesize that several strains of are endophytes in legume nodules, where they might contribute to plant growth. Our data support the description of the CNPSo 675 and sp. genomospecies G1 strains as a new species, for which the name is proposed. The type strain is CNPSo 675 (=UMR 1457=LMG 31642) and is also deposited in other culture collections.

Funding
This study was supported by the:
  • Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (Award 001)
    • Principle Award Recipient: Anderson José Scherer
  • Conselho Nacional de Desenvolvimento Científico e Tecnológico (Award 400468/2016-6)
    • Principle Award Recipient: Mariangela Hungria
  • INCT-Plant-Growth Promoting Microorganisms for Agricultural Sustainability and Environmental Responsibility (Award CNPq 465133/2014-2, Fundação Araucária-STI-043/2019, CAPES)
    • Principle Award Recipient: Mariangela Hungria
  • Empresa Brasileira de Pesquisa Agropecuária
    • Principle Award Recipient: Mariangela Hungria
Loading

Article metrics loading...

/content/journal/ijsem/10.1099/ijsem.0.004278
2020-06-22
2024-04-23
Loading full text...

Full text loading...

/deliver/fulltext/ijsem/70/7/4233.html?itemId=/content/journal/ijsem/10.1099/ijsem.0.004278&mimeType=html&fmt=ahah

References

  1. Ramírez-Bahena MH, Vial L, Lassalle F, Diel B, Chapulliot D et al. Single acquisition of protelomerase gave rise to speciation of a large and diverse clade within the Agrobacterium/Rhizobium supercluster characterized by the presence of a linear chromid. Mol Phylogenet Evol 2014; 73:202–207 [View Article][PubMed]
    [Google Scholar]
  2. Escobar MA, Dandekar AM. Agrobacterium tumefaciens as an agent of disease. Trends Plant Sci 2003; 8:380–386 [View Article][PubMed]
    [Google Scholar]
  3. Suzuki K, Tanaka K, Yamamoto S, Kiyokawa K, Moriguchi K et al. Ti and Ri plasmids. In Schwartz E. editor Microbial Megaplasmids Berlin, Heidelberg: Springer; 2009 pp 133–147
    [Google Scholar]
  4. Otten L, Burr T, Szegedi E. Agrobacterium: a disease-causing bacterium. In Tzfira T, Citovsky V. (editors) Agrobacterium: From Biology to Biotechnology New York, USA: Springer; 2008 pp 1–46
    [Google Scholar]
  5. Platt TG, Morton ER, Barton IS, Bever JD, Fuqua C. Ecological dynamics and complex interactions of Agrobacterium megaplasmids. Front Plant Sci 2014; 5:635 [View Article][PubMed]
    [Google Scholar]
  6. Zhao L, Fan M, Zhang D, Yang R, Zhang F et al. Distribution and diversity of rhizobia associated with wild soybean (Glycine soja Sieb. & Zucc.) in Northwest China. Syst Appl Microbiol 2014; 37:449–456 [View Article][PubMed]
    [Google Scholar]
  7. Cummings SP, Gyaneshwar P, Vinuesa P, Farruggia FT, Andrews M et al. Nodulation of Sesbania species by Rhizobium (Agrobacterium) strain IRBG74 and other rhizobia. Environ Microbiol 2009; 11:2510–2525 [View Article][PubMed]
    [Google Scholar]
  8. Aujoulat F, Jumas-Bilak E, Masnou A, Sallé F, Faure D et al. Multilocus sequence-based analysis delineates a clonal population of Agrobacterium (Rhizobium) radiobacter (Agrobacterium tumefaciens) of human origin. J Bacteriol 2011; 193:2608–2618 [View Article][PubMed]
    [Google Scholar]
  9. Le TT, Murugesan K, Nam I-H, Jeon J-R, Chang Y-S. Degradation of dibenzofuran via multiple dioxygenation by a newly isolated Agrobacterium sp. PH-08. J Appl Microbiol 2014; 116:542–553 [View Article][PubMed]
    [Google Scholar]
  10. Tzfira T, Citovsky V. Agrobacterium-mediated genetic transformation of plants: biology and biotechnology. Curr Opin Biotechnol 2006; 17:147–154 [View Article][PubMed]
    [Google Scholar]
  11. Young JM, Kuykendall LD, Martínez-Romero E, Kerr A, Sawada H. A revision of Rhizobium Frank 1889, with an emended description of the genus, and the inclusion of all species of Agrobacterium Conn 1942 and Allorhizobium undicola de Lajudie et al. 1998 as new combinations: Rhizobium radiobacter, R. rhizogenes, R. rubi, R. undicola and R. vitis . Int J Syst Evol Microbiol 2001; 51:89–103 [View Article][PubMed]
    [Google Scholar]
  12. Farrand SK, van Berkum PB, Oger P. Agrobacterium is a definable genus of the family Rhizobiaceae. Int J Syst Evol Microbiol 2003; 53:1681–1687 [View Article][PubMed]
    [Google Scholar]
  13. Lindstrom K, Young JPW. International committee on systematics of prokaryotes; Sub-committee on the taxonomy of Rhizobium and Agrobacterium . Int J Syst Evol Microbiol 2011; 61:3089–3093
    [Google Scholar]
  14. Keane PJ, Kerr A, New PB. Crown gall of stone fruit II. Identification and nomenclature of Agrobacterium isolates. Aust J Biol Sci 1970; 23:585–596 [View Article]
    [Google Scholar]
  15. Kerr A, Panagopoulos CG. Biotypes of Agrobacterium radiobacter var. tumefaciens and their biological control. J Phytopathol 1977; 90:172–179 [View Article]
    [Google Scholar]
  16. Costechareyre D, Rhouma A, Lavire C, Portier P, Chapulliot D et al. Rapid and efficient identification of Agrobacterium species by recA allele analysis: Agrobacterium recA diversity. Microb Ecol 2010; 60:862–872 [View Article][PubMed]
    [Google Scholar]
  17. Lassalle F, Campillo T, Vial L, Baude J, Costechareyre D et al. Genomic species are ecological species as revealed by comparative genomics in Agrobacterium tumefaciens . Genome Biol Evol 2011; 3:762–781 [View Article][PubMed]
    [Google Scholar]
  18. Ophel K, Kerr A. Agrobacterium Vitis sp. nov. for strains of Agrobacterium biovar 3 from grapevines. Int J Syst Bacteriol 1990; 40:236–241 [View Article]
    [Google Scholar]
  19. Mousavi SA, Österman J, Wahlberg N, Nesme X, Lavire C et al. Phylogeny of the Rhizobium-Allorhizobium-Agrobacterium clade supports the delineation of Neorhizobium gen. nov. Syst Appl Microbiol 2014; 37:208–215 [View Article][PubMed]
    [Google Scholar]
  20. Mousavi SA, Willems A, Nesme X, de Lajudie P, Lindström K. Revised phylogeny of Rhizobiaceae: proposal of the delineation of Pararhizobium gen. nov., and 13 new species combinations. Syst Appl Microbiol 2015; 38:84–90 [View Article][PubMed]
    [Google Scholar]
  21. Yan J, Li Y, Han XZ, Chen WF, Zou WX et al. Agrobacterium deltaense sp. nov., an endophytic bacteria isolated from nodule of Sesbania cannabina . Arch Microbiol 2017; 199:1003–1009 [View Article][PubMed]
    [Google Scholar]
  22. Yan J, Li Y, Yan H, Chen WF, Zhang X et al. Agrobacterium salinitolerans sp. nov., a saline-alkaline-tolerant bacterium isolated from root nodule of Sesbania cannabina . Int J Syst Evol Microbiol 2017; 67:1906–1911 [View Article][PubMed]
    [Google Scholar]
  23. Flores-Félix JD, Menéndez E, Peix A, García-Fraile P, Velázquez E. History and current taxonomic status of genus Agrobacterium . Syst Appl Microbiol 2020; 43:126046 [View Article][PubMed]
    [Google Scholar]
  24. Portier P, Fischer-Le Saux M, Mougel C, Lerondelle C, Chapulliot D et al. Identification of genomic species in Agrobacterium biovar 1 by AFLP genomic markers. Appl Environ Microbiol 2006; 72:7123–7131 [View Article][PubMed]
    [Google Scholar]
  25. Mondy S, Lalouche O, Dessaux Y, Faure D. Genome sequence of the quorum-sensing-signal-producing nonpathogen Agrobacterium tumefaciens strain P4. Genome Announc 2013; 1:e00798–13 [View Article][PubMed]
    [Google Scholar]
  26. Wibberg D, Blom J, Jaenicke S, Kollin F, Rupp O et al. Complete genome sequencing of Agrobacterium sp. H13-3, the former Rhizobium lupini H13-3, reveals a tripartite genome consisting of a circular and a linear chromosome and an accessory plasmid but lacking a tumor-inducing Ti-plasmid. J Biotechnol 2011; 155:50–62 [View Article][PubMed]
    [Google Scholar]
  27. Huang Y-Y, Cho S-T, Lo W-S, Wang Y-C, Lai E-M et al. Complete genome sequence of Agrobacterium tumefaciens Ach5. Genome Announc 2015; 3:e00570–15 [View Article][PubMed]
    [Google Scholar]
  28. Chen LS, Figueredo A, Pedrosa FO, Hungria M. Genetic characterization of soybean rhizobia in Paraguay. Appl Environ Microbiol 2000; 66:5099–5103 [View Article][PubMed]
    [Google Scholar]
  29. Hungria M, Chueire LMO, Megías M, Lamrabet Y, Probanza A et al. Genetic diversity of Indigenous tropical fast-growing rhizobia isolated from soybean nodules. Plant Soil 2006; 288:343–356 [View Article]
    [Google Scholar]
  30. Chibeba AM, Kyei-Boahen S, Guimarães MF, Nogueira MA, Hungria M. Isolation, characterization and selection of indigenous Bradyrhizobium strains with outstanding symbiotic performance to increase soybean yields in Mozambique. Agric Ecosyst Environ 2017; 246:291–305 [View Article][PubMed]
    [Google Scholar]
  31. Grange L, Hungria M. Genetic diversity of indigenous common bean (Phaseolus vulgaris) rhizobia in two Brazilian ecosystems. Soil Biol Biochem 2004; 36:1389–1398 [View Article]
    [Google Scholar]
  32. Ribeiro RA, Ormeño-Orrillo E, Dall'Agnol RF, Graham PH, Martínez-Romero E et al. Novel Rhizobium lineages isolated from root nodules of the common bean (Phaseolus vulgaris L.) in Andean and Mesoamerican areas. Res Microbiol 2013; 164:740–748 [View Article][PubMed]
    [Google Scholar]
  33. Costa MR, Chibeba AM, Mercante FM, Hungria M. Polyphasic characterization of rhizobia microsymbionts of common bean [Phaseolus vulgaris (L.)] isolated in Mato Grosso do Sul, a hotspot of Brazilian biodiversity. Symbiosis 2018; 76:163–176 [View Article]
    [Google Scholar]
  34. Menna P, Hungria M, Barcellos FG, Bangel EV, Hess PN et al. Molecular phylogeny based on the 16S rRNA gene of elite rhizobial strains used in Brazilian commercial inoculants. Syst Appl Microbiol 2006; 29:315–332 [View Article][PubMed]
    [Google Scholar]
  35. Binde DR, Menna P, Bangel EV, Barcellos FG, Hungria M. Rep-PCR fingerprinting and taxonomy based on the sequencing of the 16S rRNA gene of 54 elite commercial rhizobial strains. Appl Microbiol Biotechnol 2009; 83:897–908 [View Article][PubMed]
    [Google Scholar]
  36. Roma Neto IV, Ribeiro RA, Hungria M. Genetic diversity of elite rhizobial strains of subtropical and tropical legumes based on the 16S rRNA and glnII genes. World J Microbiol Biotechnol 2010; 26:1291–1302 [View Article][PubMed]
    [Google Scholar]
  37. Hungria M, O’Hara GW, Zilli JE, Araujo RS, Deaker R et al. Isolation and growth or rhizobia. In Howieson JG, Dilworth JG. (editors) Working with Rhizobia Canberra, Australia: ACIAR; 2016 pp 39–60
    [Google Scholar]
  38. Felsenstein J. Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol 1981; 17:368–376 [View Article][PubMed]
    [Google Scholar]
  39. Kumar S, Stecher G, Tamura K. MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 2016; 33:1870–1874 [View Article][PubMed]
    [Google Scholar]
  40. Edgar RC. Muscle: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 2004; 32:1792–1797 [View Article][PubMed]
    [Google Scholar]
  41. Tamura K. Estimation of the number of nucleotide substitutions when there are strong transition-transversion and G+C-content biases. Mol Biol Evol 1992; 9:678–687 [View Article][PubMed]
    [Google Scholar]
  42. Felsenstein J. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 1985; 39:783–791 [View Article][PubMed]
    [Google Scholar]
  43. Hall TA. 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]
  44. Naser SM, Dawyndt P, Hoste B, Gevers D, Vandemeulebroecke K et al. Identification of lactobacilli by pheS and rpoA gene sequence analyses. Int J Syst Evol Microbiol 2007; 57:2777–2789 [View Article][PubMed]
    [Google Scholar]
  45. Delamuta JRM, 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]
  46. Gan HM, Savka MA. One more decade of Agrobacterium taxonomy. In Gelvin S. editor Current Topics in Microbiology and Immunology Cham: Springer; 2018 pp 1–14
    [Google Scholar]
  47. Lassalle F, Planel R, Penel S, Chapulliot D, Barbe V et al. Ancestral genome estimation reveals the history of ecological diversification in Agrobacterium . Genome Biol Evol 2017; 9:3413–3431 [View Article][PubMed]
    [Google Scholar]
  48. de Lajudie PM, Andrews M, Ardley J, Eardly B, Jumas-Bilak E et al. Minimal standards for the description of new genera and species of rhizobia and agrobacteria. Int J Syst Evol Microbiol 2019; 69:1852–1863 [View Article][PubMed]
    [Google Scholar]
  49. Ormeño-Orrillo E, Servín-Garcidueñas LE, Rogel MA, González V, Peralta H et al. Taxonomy of rhizobia and agrobacteria from the Rhizobiaceae family in light of genomics. Syst Appl Microbiol 2015; 38:287–291 [View Article][PubMed]
    [Google Scholar]
  50. Scherer AJ, Delamuta JRM, Ribeiro RA, Chibeba AM, Kyei-Boahen S et al. Draft Genome Sequence of Agrobacterium deltaense strain CNPSo 3391, isolated from a soybean nodule in Mozambique. Microbiol Resour Announc 2019; 8:e01675–18 [View Article][PubMed]
    [Google Scholar]
  51. Aziz RK, Bartels D, Best AA, DeJongh M, Disz T et al. The RAST server: rapid annotations using subsystems technology. BMC Genomics 2008; 9:75 [View Article][PubMed]
    [Google Scholar]
  52. 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]
  53. Konstantinidis KT, Ramette A, Tiedje JM. Toward a more robust assessment of intraspecies diversity, using fewer genetic markers. Appl Environ Microbiol 2006; 72:7286–7293 [View Article][PubMed]
    [Google Scholar]
  54. Kim M, Oh H-S, Park S-C, Chun J. Towards a taxonomic coherence between average nucleotide identity and 16S rRNA gene sequence similarity for species demarcation of prokaryotes. Int J Syst Evol Microbiol 2014; 64:346–351 [View Article][PubMed]
    [Google Scholar]
  55. 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]
  56. Kuzmanović N, Puławska J, Prokić A, Ivanović M, Zlatković N et al. Agrobacterium arsenijevicii sp. nov., isolated from crown gall tumors on raspberry and cherry plum. Syst Appl Microbiol 2015; 38:373–378 [View Article][PubMed]
    [Google Scholar]
  57. Ribeiro RA, Martins TB, Ormeño-Orrillo E, Marçon Delamuta JR, Rogel MA et al. Rhizobium ecuadorense sp. nov., an indigenous N2-fixing symbiont of the Ecuadorian common bean (Phaseolus vulgaris L.) genetic pool. Int J Syst Evol Microbiol 2015; 65:3162–3169 [View Article][PubMed]
    [Google Scholar]
  58. Rodriguez-R LM, Konstantinidis KT. The enveomics collection: a toolbox for specialized analyses of microbial genomes and metagenomes. PeerJ Prepr 2016; 4:e1900v1
    [Google Scholar]
  59. Yoon S-H, Ha S-M, Lim J, Kwon S, Chun J. A large-scale evaluation of algorithms to calculate average nucleotide identity. Antonie van Leeuwenhoek 2017; 110:1281–1286 [View Article][PubMed]
    [Google Scholar]
  60. Meier-Kolthoff JP, Klenk H-P, 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]
  61. Meier-Kolthoff JP, Auch AF, Klenk H-P, Göker M. Genome sequence-based species delimitation with confidence intervals and improved distance functions. BMC Bioinformatics 2013; 14:60 [View Article][PubMed]
    [Google Scholar]
  62. Ormeño-Orrillo E, Menna P, Almeida LGP, Ollero FJ, Nicolás MF et al. Genomic basis of broad host range and environmental adaptability of Rhizobium tropici CIAT 899 and Rhizobium sp. PRF 81 which are used in inoculants for common bean (Phaseolus vulgaris L.). BMC Genomics 2012; 13:735 [View Article][PubMed]
    [Google Scholar]
  63. Hubber A, Vergunst AC, Sullivan JT, Hooykaas PJJ, Ronson CW. Symbiotic phenotypes and translocated effector proteins of the Mesorhizobium loti strain R7A VirB/D4 type IV secretion system. Mol Microbiol 2004; 54:561–574 [View Article][PubMed]
    [Google Scholar]
  64. Gomes DF, Batista JSdaS, Torres AR, de Souza Andrade D, Galli-Terasawa LV et al. Two-dimensional proteome reference map of Rhizobium tropici PRF 81 reveals several symbiotic determinants and strong resemblance with agrobacteria. Proteomics 2012; 12:859–863 [View Article][PubMed]
    [Google Scholar]
  65. Sneath PHA, Sokal RR. Numerical Taxonomy: The Principles and Practice of Numerical Classification San Francisco, USA: W. H. Freeman and Company; 1973 p 573 p
    [Google Scholar]
  66. Jaccard P. The distribution of the flora in the alpine zone. New Phytol 1912; 11:37–50 [View Article]
    [Google Scholar]
  67. Ormeño-Orrillo E, Martínez-Romero E. Phenotypic tests in Rhizobium species description: an opinion and (a sympatric speciation) hypothesis. Syst Appl Microbiol 2013; 36:145–147 [View Article][PubMed]
    [Google Scholar]
  68. Hungria M, Chueire Lı́gia Maria de O, Coca RG, Megı́as M. Preliminary characterization of fast growing rhizobial strains isolated from soyabean nodules in Brazil. Soil Biol Biochem 2001; 33:1349–1361 [View Article]
    [Google Scholar]
  69. Biswas JC, Ladha JK, Dazzo FB, Yanni YG, Rolfe BG. Rhizobial inoculation influences seedling vigor and yield of rice. Agron J 2000; 92:880–886 [View Article]
    [Google Scholar]
  70. Caetano-Anollés G, Bauer WD. Enhanced nodule initiation on alfalfa by wild-Rhizobium meliloti co-inoculated with nod gene mutants and other bacteria. Planta 1988; 174:385–395 [View Article][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/ijsem/10.1099/ijsem.0.004278
Loading
/content/journal/ijsem/10.1099/ijsem.0.004278
Loading

Data & Media loading...

Supplements

Supplementary material 1

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