1887

Abstract

During a survey of root-nodulating symbionts of Mimosoid species in the south-east region of Brazil, eight isolates were obtained from nodules of the legume species either from the field or following a soil trapping method with the same plant host. 16S rRNA gene as well as and phylogenetic markers placed these strains in two new clades within the genus . DNA–DNA hybridization values and analyses of average nucleotide identities of the whole genome sequence of selected strains in each clade (STM 7183 and STM 7296) showed that the two clades represented novel species of the genus . All eight isolates were further characterized using DNA base content determination, chemotaxonomic and biochemical profiling and symbiotic properties, which allowed to distinguish the novel species from known diazotrophic species of the genus . Based on genomic and phenotypic data, the names sp. nov. with type strain STM 7183 (=DSM 101189=LMG 29163) and sp. nov. with type strain STM 7296 (=DSM 101188=LMG 29351) are proposed.

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2017-02-01
2020-10-01
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References

  1. Dobritsa AP, Samadpour M. Transfer of eleven species of the genus Burkholderia to the genus Paraburkholderia and proposal of Caballeronia gen. nov. to accommodate twelve species of the genera Burkholderia and Paraburkholderia. Int J Syst Evol Microbiol 2016;66:2836–2846 [CrossRef][PubMed]
    [Google Scholar]
  2. Sawana A, Adeolu M, Gupta RS. Molecular signatures and phylogenomic analysis of the genus Burkholderia: proposal for division of this genus into the emended genus Burkholderia containing pathogenic organisms and a new genus Paraburkholderia gen. nov. harboring environmental species. Front Genet 2014;5:429 [CrossRef][PubMed]
    [Google Scholar]
  3. Eberl L, Vandamme P. Members of the genus Burkholderia: good and bad guys. F1000Res 2016;5:1007 [CrossRef]
    [Google Scholar]
  4. Peeters C, Meier-Kolthoff JP, Verheyde B, de Brandt E, Cooper VS et al. Phylogenomic study of Burkholderia glathei-like organisms, proposal of 13 novel Burkholderia species and emended descriptions of Burkholderia sordidicola, Burkholderia zhejiangensis, and Burkholderia grimmiae. Front Microbiol 2016;7:877 [CrossRef][PubMed]
    [Google Scholar]
  5. Compant S, Nowak J, Coenye T, Clément C, Ait Barka E. Diversity and occurrence of Burkholderia spp. in the natural environment. FEMS Microbiol Rev 2008;32:607–626 [CrossRef][PubMed]
    [Google Scholar]
  6. Gyaneshwar P, Hirsch AM, Moulin L, Chen WM, Elliott GN et al. Legume-nodulating betaproteobacteria: diversity, host range, and future prospects. Mol Plant Microbe Interact 2011;24:1276–1288 [CrossRef][PubMed]
    [Google Scholar]
  7. Bontemps C, Elliott GN, Simon MF, dos Reis Júnior FB, Gross E et al. Burkholderia species are ancient symbionts of legumes. Mol Ecol 2010;19:44–52 [CrossRef][PubMed]
    [Google Scholar]
  8. Elliott GN, Chen W-M, Chou J-H, Wang H-C, Sheu S-Y et al. Burkholderia phymatum is a highly effective nitrogen-fixing symbiont of Mimosa spp. and fixes nitrogen ex planta. New Phytol 2007;173:168–180 [CrossRef][PubMed]
    [Google Scholar]
  9. dos Reis FB, Simon MF, Gross E, Boddey RM, Elliott GN et al. Nodulation and nitrogen fixation by Mimosa spp. in the Cerrado and Caatinga biomes of Brazil. New Phytol 2010;186:934–946 [CrossRef][PubMed]
    [Google Scholar]
  10. Mavengere NR, Ellis AG, Le Roux JJ. Burkholderia aspalathi sp. nov., isolated from root nodules of the South African legume Aspalathus abietina Thunb. Int J Syst Evol Microbiol 2014;64:1906–1912 [CrossRef][PubMed]
    [Google Scholar]
  11. Martínez-Aguilar L, Salazar-Salazar C, Méndez RD, Caballero-Mellado J, Hirsch AM et al. Burkholderia caballeronis sp. nov., a nitrogen fixing species isolated from tomato (Lycopersicon esculentum) with the ability to effectively nodulate Phaseolus vulgaris. Antonie van Leeuwenhoek 2013;104:1063–1071 [CrossRef][PubMed]
    [Google Scholar]
  12. Chen WM, Moulin L, Bontemps C, Vandamme P, Béna G et al. Legume symbiotic nitrogen fixation by β-proteobacteria is widespread in nature. J Bacteriol 2003;185:7266–7272 [CrossRef][PubMed]
    [Google Scholar]
  13. Sheu SY, Chou JH, Bontemps C, Elliott GN, Gross E et al. Burkholderia diazotrophica sp. nov., isolated from root nodules of Mimosa spp. native to North East Brazil. Int J Syst Evol Microbiol 2013;63:435–441 [CrossRef][PubMed]
    [Google Scholar]
  14. De Meyer SE, Cnockaert M, Ardley JK, van Wyk B-E, Vandamme PA et al. Burkholderia dilworthii sp. nov., isolated from Lebeckia ambigua root nodules. Int J Syst Evol Microbiol 2014;64:1090–1095 [CrossRef][PubMed]
    [Google Scholar]
  15. Chen W-M, James EK, Coenye T, Chou J-H, Barrios E et al. Burkholderia mimosarum sp. nov., isolated from root nodules of Mimosa spp. from Taiwan and South America. Int J Syst Evol Microbiol 2006;56:1847–1851 [CrossRef][PubMed]
    [Google Scholar]
  16. Chen W-M, de Faria SM, James EK, Elliott GN, Lin K-Y et al. Burkholderia nodosa sp. nov., isolated from root nodules of the woody Brazilian legumes Mimosa bimucronata and Mimosa scabrella. Int J Syst Evol Microbiol 2007;57:1055–1059 [CrossRef][PubMed]
    [Google Scholar]
  17. De Oliveira Cunha C, Goda Zuleta LF, Paula de Almeida LG, Prioli Ciapina L, Lustrino Borges W et al. Complete genome sequence of Burkholderia phenoliruptrix BR3459a (CLA1), a heat-tolerant, nitrogen-fixing symbiont of Mimosa flocculosa. J Bacteriol 2012;194:6675–6676 [CrossRef][PubMed]
    [Google Scholar]
  18. Vandamme P, Goris J, Chen W-M, de Vos P, Willems A. Burkholderia tuberum sp. nov. and Burkholderia phymatum sp. nov., nodulate the roots of tropical legumes. Syst Appl Microbiol 2002;25:507–512 [CrossRef][PubMed]
    [Google Scholar]
  19. De Meyer SE, Cnockaert M, Ardley JK, Trengove RD, Garau G et al. Burkholderia rhynchosiae sp. nov., isolated from Rhynchosia ferulifolia root nodules. Int J Syst Evol Microbiol 2013;63:3944–3949 [CrossRef][PubMed]
    [Google Scholar]
  20. Chen W-M, de Faria SM, Chou J-H, James EK, Elliott GN et al. Burkholderia sabiae sp. nov., isolated from root nodules of Mimosa caesalpiniifolia. Int J Syst Evol Microbiol 2008;58:2174–2179 [CrossRef][PubMed]
    [Google Scholar]
  21. de Meyer SE, Cnockaert M, Ardley JK, Maker G, Yates R et al. Burkholderia sprentiae sp. nov., isolated from Lebeckia ambigua root nodules. Int J Syst Evol Microbiol 2013;63:3950–3957 [CrossRef][PubMed]
    [Google Scholar]
  22. Sheu SY, Chou JH, Bontemps C, Elliott GN, Gross E et al. Burkholderia symbiotica sp. nov., isolated from root nodules of Mimosa spp. native to North-East Brazil. Int J Syst Evol Microbiol 2012;62:2272–2278 [CrossRef][PubMed]
    [Google Scholar]
  23. Beukes CW, Venter SN, Law IJ, Phalane FL, Steenkamp ET. South african papilionoid legumes are nodulated by diverse Burkholderia with unique nodulation and nitrogen-fixation loci. PLoS One 2013;8:e68406 [CrossRef][PubMed]
    [Google Scholar]
  24. De Meyer SE, Briscoe L, Martínez-Hidalgo P, Agapakis CM, de-Los Santos PE et al. Symbiotic Burkholderia species show diverse arrangements of nif/fix and nod genes and lack typical high-affinity cytochrome cbb3 oxidase genes. Mol Plant Microbe Interact 2016;29:609–619 [CrossRef][PubMed]
    [Google Scholar]
  25. Mishra RPN, Tisseyre P, Melkonian R, Chaintreuil C, Miché L et al. Genetic diversity of Mimosa pudica rhizobial symbionts in soils of French Guiana: investigating the origin and diversity of Burkholderia phymatum and other beta-rhizobia. FEMS Microbiol Ecol 2012;79:487–503 [CrossRef][PubMed]
    [Google Scholar]
  26. Bournaud C, de Faria SM, dos Santos JMF, Tisseyre P, Silva M et al. Burkholderia species are the most common and preferred nodulating symbionts of the piptadenia group (tribe Mimoseae). PLoS One 2013;8:e63478 [CrossRef][PubMed]
    [Google Scholar]
  27. Vincent J. A Manual for the Practical Study of Root-Nodule Bacteria, I.B.P. Han. Ltd. Oxford: Blackwell Scientific Publications; 1970
    [Google Scholar]
  28. Moulin L, Béna G, Boivin-Masson C, Stepkowski T. Phylogenetic analyses of symbiotic nodulation genes support vertical and lateral gene co-transfer within the Bradyrhizobium genus. Mol Phylogenet Evol 2004;30:720–732 [CrossRef][PubMed]
    [Google Scholar]
  29. Weisburg WG, Barns SM, Pelletier DA, Lane DJ. 16S ribosomal DNA amplification for phylogenetic study. J Bacteriol 1991;173:697–703 [CrossRef][PubMed]
    [Google Scholar]
  30. Payne GW, Vandamme P, Morgan SH, Lipuma JJ, Coenye T et al. Development of a recA gene-based identification approach for the entire Burkholderia genus. Appl Environ Microbiol 2005;71:3917–3927 [CrossRef][PubMed]
    [Google Scholar]
  31. Spilker T, Baldwin A, Bumford A, Dowson CG, Mahenthiralingam E et al. Expanded multilocus sequence typing for Burkholderia species. J Clin Microbiol 2009;47:2607–2610 [CrossRef][PubMed]
    [Google Scholar]
  32. 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 [CrossRef][PubMed]
    [Google Scholar]
  33. Pitcher DG, Saunders NA, Owen RJ. Rapid extraction of bacterial genomic DNA with guanidium thiocyanate. Lett Appl Microbiol 1989;8:151–156 [CrossRef]
    [Google Scholar]
  34. Ezaki T, Hashimoto Y, Yabuuchi E. 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 1989;39:224–229 [CrossRef]
    [Google Scholar]
  35. Goris J, Suzuki K, Vos PD, Nakase T, Kersters K. Evaluation of a microplate DNADNA hybridization method compared with the initial renaturation method. Can J Microbiol 1998;44:1148–1153 [CrossRef]
    [Google Scholar]
  36. Vallenet D, Belda E, Calteau A, Cruveiller S, Engelen S et al. MicroScope-an integrated microbial resource for the curation and comparative analysis of genomic and metabolic data. Nucleic Acids Res 2013;41:D636–D647 [CrossRef][PubMed]
    [Google Scholar]
  37. Richter M, Rosselló-Móra R. Shifting the genomic gold standard for the prokaryotic species definition. Proc Natl Acad Sci USA 2009;106:19126–19131 [CrossRef][PubMed]
    [Google Scholar]
  38. 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 [CrossRef][PubMed]
    [Google Scholar]
  39. 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 [CrossRef][PubMed]
    [Google Scholar]
  40. Sierra G. A simple method for the detection of lipolytic activity of micro-organisms and some observations on the influence of the contact between cells and fatty substrates. Antonie van Leeuwenhoek 1957;23:15–22 [CrossRef][PubMed]
    [Google Scholar]
  41. Jeffries CD, Holtman DF, Guse DG. Rapid method for determining the activity of microorganisms on nucleic acids. J Bacteriol 1957;73:590–591[PubMed]
    [Google Scholar]
  42. Vandamme P, Vancanneyt M, Pot B, Mels L, Hoste B et al. Polyphasic taxonomic study of the emended genus Arcobacter with Arcobacter butzleri comb. nov. and Arcobacter skirrowii sp. nov., an aerotolerant bacterium isolated from veterinary specimens. Int J Syst Bacteriol 1992;42:344–356 [CrossRef][PubMed]
    [Google Scholar]
  43. Rivas R, Willems A, Subba-Rao NS, Mateos PF, Dazzo FB et al. Description of Devosia neptuniae sp. nov. that nodulates and fixes nitrogen in symbiosis with Neptunia natans, an aquatic legume from India. Syst Appl Microbiol 2003;26:47–53 [CrossRef][PubMed]
    [Google Scholar]
  44. Moulin L, Klonowska A, Caroline B, Booth K, Vriezen JAC et al. Complete genome sequence of Burkholderia phymatum STM815(T), a broad host range and efficient nitrogen-fixing symbiont of Mimosa species. Stand Genomic Sci 2014;9:763–774 [CrossRef][PubMed]
    [Google Scholar]
  45. 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;64:1825 [CrossRef]
    [Google Scholar]
  46. Chain PS, Denef VJ, Konstantinidis KT, Vergez LM, Agulló L et al. Burkholderia xenovorans LB400 harbors a multi-replicon, 9.73-Mbp genome shaped for versatility. Proc Natl Acad Sci USA 2006;103:15280–15287 [CrossRef][PubMed]
    [Google Scholar]
  47. Mitter B, Petric A, Shin MW, Chain PSG, Hauberg-Lotte L et al. Comparative genome analysis of Burkholderia phytofirmans PsJN reveals a wide spectrum of endophytic lifestyles based on interaction strategies with host plants. Front Plant Sci 2013;4:120 [CrossRef][PubMed]
    [Google Scholar]
  48. Willems A, Tian R, Bräu L, Goodwin L, Han J et al. Genome sequence of Burkholderia mimosarum strain LMG 23256(T), a Mimosa pigra microsymbiont from Anso, Taiwan. Stand Genomic Sci 2014;9:484–494 [CrossRef][PubMed]
    [Google Scholar]
  49. Zuleta LF, Cunha CO, de Carvalho FM, Ciapina LP, Souza RC et al. The complete genome of Burkholderia phenoliruptrix strain BR3459a, a symbiont of Mimosa flocculosa: highlighting the coexistence of symbiotic and pathogenic genes. BMC Genomics 2014;15:535 [CrossRef][PubMed]
    [Google Scholar]
  50. Viallard V, Poirier I, Cournoyer B, Haurat J, Wiebkin S et al. Burkholderia graminis sp. nov., a rhizospheric Burkholderia species, and reassessment of [Pseudomonas] phenazinium, [Pseudomonas] pyrrocinia and [Pseudomonas] glathei as Burkholderia. Int J Syst Bacteriol 1998;48:549–563 [CrossRef][PubMed]
    [Google Scholar]
  51. Coenye T, Henry D, Speert DP, Vandamme P. Burkholderia phenoliruptrix sp. nov., to accommodate the 2,4,5-trichlorophenoxyacetic acid and halophenol-degrading strain AC1100. Syst Appl Microbiol 2004;27:623–627 [CrossRef][PubMed]
    [Google Scholar]
  52. Goris J, de Vos P, Caballero-Mellado J, Park J, Falsen E et al. Classification of the biphenyl- and polychlorinated biphenyl-degrading strain LB400T and relatives as Burkholderia xenovorans sp. nov. Int J Syst Evol Microbiol 2004;54:1677–1681 [CrossRef][PubMed]
    [Google Scholar]
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