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Antonie van Leeuwenhoek

, Volume 110, Issue 6, pp 727–736 | Cite as

Reassessment of the taxonomic position of Burkholderia andropogonis and description of Robbsia andropogonis gen. nov., comb. nov.

  • Lucilene Lopes-Santos
  • Daniel Bedo Assumpção Castro
  • Mariana Ferreira-Tonin
  • Daniele Bussioli Alves Corrêa
  • Bevan Simon Weir
  • Duckchul Park
  • Laura Maria Mariscal Ottoboni
  • Júlio Rodrigues Neto
  • Suzete Aparecida Lanza Destéfano
Original Paper

Abstract

The phylogenetic classification of the species Burkholderia andropogonis within the Burkholderia genus was reassessed using 16S rRNA gene phylogenetic analysis and multilocus sequence analysis (MLSA). Both phylogenetic trees revealed two main groups, named A and B, strongly supported by high bootstrap values (100%). Group A encompassed all of the Burkholderia species complex, whi.le Group B only comprised B. andropogonis species, with low percentage similarities with other species of the genus, from 92 to 95% for 16S rRNA gene sequences and 83% for conserved gene sequences. Average nucleotide identity (ANI), tetranucleotide signature frequency, and percentage of conserved proteins POCP analyses were also carried out, and in the three analyses B. andropogonis showed lower values when compared to the other Burkholderia species complex, near 71% for ANI, from 0.484 to 0.724 for tetranucleotide signature frequency, and around 50% for POCP, reinforcing the distance observed in the phylogenetic analyses. Our findings provide an important insight into the taxonomy of B. andropogonis. It is clear from the results that this bacterial species exhibits genotypic differences and represents a new genus described herein as Robbsia andropogonis gen. nov., comb. nov.

Keywords

Bacterial disease Genome sequence MLSA 16S rRNA gene 

Notes

Acknowledgements

We thank the São Paulo Research Foundation (FAPESP) for financial support (Grant #2011/12222-2 and #2011/50813-2).

Supplementary material

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Supplementary material 1 (XLSX 13 kb)
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Supplementary material 2 (XLSX 49 kb)
10482_2017_842_MOESM3_ESM.docx (62 kb)
Supplementary material 3 (DOCX 62 kb)

References

  1. Almeida IMG, Berian LOS, Sannazzaro AM, Rodrigues Neto J (2009) Mancha bacteriana em Ruscus sp. causada por Burkholderia andropogonis no Brasil. Trop Plant Pathol 34:339–342CrossRefGoogle Scholar
  2. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment searchtool. J Mol Biol 215:403–410CrossRefPubMedGoogle Scholar
  3. Bohlin J, Skjerve E, Ussery DW (2008) Reliability and applications of statistical methods based on oligonucleotide frequencies in bacterial and archaeal genomes. BMC Genom 9:104CrossRefGoogle Scholar
  4. Castresana J (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 17(4):540–552CrossRefPubMedGoogle Scholar
  5. Coenye T, Gevers D, Van de Peer Y, Vandamme P, Swings J (2005) Towards a prokaryotic genomic taxonomy. FEMS Microbiol Rev 29(2):147–167CrossRefPubMedGoogle Scholar
  6. Cother EJ, Noble D, Peters BJ, Albiston A, Ash GJ (2004) A new bacterial disease of jojoba (Simmondsia chinensis) caused by Burkholderia andropogonis. Plant Pathol 53:129–135CrossRefGoogle Scholar
  7. Darriba D, Taboada GL, Doallo R, Posada D (2011) ProtTest 3: fast selection of best-fit models of protein evolution. Bioinformatics 27:1164–1165CrossRefPubMedPubMedCentralGoogle Scholar
  8. Dobritsa AP, Samadpour M (2016) 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 66:2836–2846CrossRefPubMedGoogle Scholar
  9. Duan YP, Sun X, Zhou LJ, Gabriel DW, Benyon LS, Gottwald T (2009) Bacterial brown leaf spot of citrus, a new disease caused by Burkholderia andropogonis. Plant Dis 93:607–614CrossRefGoogle Scholar
  10. Estrada-de los Santos P, Vinuesa P, Aguilar LM, Hirsch AM, Caballero-Mellado J (2013) Phylogenetic analysis of Burkholderia species by multilocus sequence analysis. Curr Microbiol 67:51–60CrossRefPubMedGoogle Scholar
  11. European and Mediterranean Plant Protection Organization (2014). PQR-EPPO database on quarantine pests. European and Mediterranean Plant Protection Organization, Paris, France. https://www.eppo.int/DATABASES/pqr/pqr.htm
  12. Euzéby JP (1997) List of bacterial names with standing in nomenclature: a folder available on the Internet. Int J Syst Bacteriol 47:590–592CrossRefPubMedGoogle Scholar
  13. Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791CrossRefGoogle Scholar
  14. Fuerst JA, Hayward AC (1969) The sheathed flagellum of Pseudomonas stizolobii. J Clin Microbiol 59:239–245Google Scholar
  15. Gillis M, van Van T, Bardin R, Goor M, Hebbar P, Willems A, Segers P, Kersters K, Heulin T, Fernandez MP (1995) Polyphasic taxonomy in the genus Burkholderia leading to an emended description of the genus and proposition of Burkholderia vietnamiensis sp. nov. for N2-fixing isolates from rice in Vietnam. Int J Syst Evol Microbiol 45:274–289Google Scholar
  16. Gitaitis RD, Miller J, Wells HD (1983) Bacterial leaf spot of clover in Georgia. Plant Dis 67:913–914CrossRefGoogle Scholar
  17. Goris J, Konstantinidis KT, Klappenbach JA, Coenye T, Vandamme P, Tiedje JM (2007) DNA–DNA hybridization values and their relationship to whole-genome sequence similarities. Int J Syst Evol Microbiol 57:81–91CrossRefPubMedGoogle Scholar
  18. Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704CrossRefPubMedGoogle Scholar
  19. Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98Google Scholar
  20. Hall N (2007) Advanced sequencing technologies and their wide impact in microbiology. J Exp Biol 210(9):1518–1525CrossRefPubMedGoogle Scholar
  21. Hyatt D, Chen GL, Locascio PF, Land ML, Larimer FW, Hauser LJ (2010) Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinform 11(1):119CrossRefGoogle Scholar
  22. Kim M, Oh H, Park S, Chun J (2014) Towards a taxonomic coherence between average nucleotide identity and 16S rRNA gene sequence similarity for species demarcation of prokaryotes. Int J Syst Evol Microbiol 64:346–351CrossRefPubMedGoogle Scholar
  23. Konstantinidis KT, Tiedje JM (2005) Towards a genome-based taxonomy for prokaryotes. J Bacteriol 187(18):6258–6264CrossRefPubMedPubMedCentralGoogle Scholar
  24. Konstantinidis KT, Ramette A, Tiedje JM (2006) The bacterial species definition in the genomic era. Philos Trans R Soc B 361(1475):1929–1940CrossRefGoogle Scholar
  25. Lane DJ (1991) 16S/23S rRNA sequencing. In: Stackebrandt E, Goodfellow M (eds) Nucleic acid techniques in bacterial systematics. Wiley, New York, pp 115–147Google Scholar
  26. Li X, De Boer SH (2005) First report of Burkholderia andropogonis causing leaf spots of Bouganinvillea sp. in Hong Kong and clover in Canada. Plant Dis 89:1132CrossRefGoogle Scholar
  27. Li X, Dorsch M, Del Dot T, Sly LI, Stackebrandt E, Hayward AC (1993) Phylogenetic studies of the rRNA group II pseudomonads based on 16S rRNA gene sequences. J Appl Bacteriol 74:324–329CrossRefGoogle Scholar
  28. Lopes-Santos L, Castro DBA, Ottoboni LMM, Park D, Weir BS, Destéfano SAL (2015) Draft genome sequence of Burkholderia andropogonis type strain ICMP2807, isolated from Sorghum bicolor. Genome Announc 3(3):1–2CrossRefGoogle Scholar
  29. Maeda Y, Shinohara H, Kiba A, Ohnishi K, Furuya N, Kawamura Y, Ezaky T, Vandamme P, Tsushima S, Hikichi Y (2006) Phylogenetic study and multiplex PCR-based detection of Burkholderia plantarii, Burkholderia glumae and Burkholderia gladioli using gyrB and rpoD sequences. Int J Syst Evol Microbiol 56:1031–1038CrossRefPubMedGoogle Scholar
  30. Mitchell RE (1994) Dihydrorhizobitoxine, a minor product of Pseudomonas andropogonis. Phytochemistry 37:373–375CrossRefGoogle Scholar
  31. Moffett ML, Hayward AC, Fahy PC (1986) Five new hosts of Pseudomonas andropogonis occurring in eastern Australia: host range and characterization of isolates. Plant Pathol 35:34–43CrossRefGoogle Scholar
  32. Okazaki S, Nukui N, Sugawara M, Minamisawa K (2004) Rhizobial strategies to enhance symbiotic interaction: rhizobitoxine and 1-aminocyclopropane-1-carboxylate deaminase. Microbes Environ 19:99–111CrossRefGoogle Scholar
  33. Palleroni NJ (1984) Genus I Pseudomonas Migula. In: Krieg NR, Holt JG (eds) Bergey’s Manual of Systematic and Bacteriology, vol 1. Williams and Wilkins, Baltimore, pp 141–199Google Scholar
  34. Patel JB (2001) 16S rRNA gene sequencing for bacterial pathogen identification in the clinical laboratory. Mol Diagn 6:313–321CrossRefPubMedGoogle Scholar
  35. Payne GW, Vandamme P, Morgan SH, LiPuma JJ, Coenye T, Weightmann AJ, Hefim Jones T, Mahenthiralingam E (2005) Development of a recA gene-based identification approach for the entire Burkholderia genus. Appl Environ Microbiol 71:3917–3927CrossRefPubMedPubMedCentralGoogle Scholar
  36. Pays T, Berger E, Mitricia I, Nakamura LK, Cohan FM (2000) Protein coding genes as molecular markers for ecologically distinct populations: the casa of two Bacillus species. Int J Syst Bacteriol 50:1021–1028CrossRefGoogle Scholar
  37. Pitcher DG, Saunders NA, Owen RJ (1989) Rapid extraction of bacterial genomic DNA with guanidium thiocyanate. Lett Appl Microbiol 8:151–156CrossRefGoogle Scholar
  38. Pride DT, Meinersmann RJ, Wassenaar TM, Blaser MJ (2003) Evolutionary implications of microbial genome tetranucleotide frequency biases. Genome Res 13(2):145–158CrossRefPubMedPubMedCentralGoogle Scholar
  39. Qin Q, Xie B, Zhang X, Chen X, Zhou B, Zhou J, Zhang Y (2014) A proposed genus boundary for the prokaryotes based on genomic insights. J Bacteriol 196(12):2210–2215CrossRefPubMedPubMedCentralGoogle Scholar
  40. Richter M, Rosselló-Móra R (2009) Shifting the genomic gold standard for the prokaryotic species definition. Proc Natl Acad Sci 106(45):19126–19131CrossRefPubMedPubMedCentralGoogle Scholar
  41. Rodrigues Neto J, Figueiredo P, Mariotto PR, Robbs CF (1981) Pseudomons andropogonis (Smith 1911) Stapp 1928, agente causal da “mancha bacteriana escura” em folhas de cafeeiro (Coffea arabica L.). Instituto Biológico 48:31–36Google Scholar
  42. Sawana  A, Adeolu M, Gupta RS (2014) 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 5:429CrossRefPubMedPubMedCentralGoogle Scholar
  43. Sievers F, Wilm A, Dineen DG, Gibson TJ, Karplus K, Li W, Lopez R, McWilliam H, Remmert M, Söding J, Thompson JD, Higgins DG (2011) Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol Syst Biol 7(1):539CrossRefPubMedPubMedCentralGoogle Scholar
  44. Smith EF (1911) Bacteria in relation to plant diseases. Carnegie Institute Publications, Washington, DCGoogle Scholar
  45. Stackebrandt E, Goebel EB (1994) Taxonomic note: a place for DNA-DNA reassociation and 16S rRNA sequence analysis in the present species definition in bacteriology. Int J Syst Bacteriol 44:846–849CrossRefGoogle Scholar
  46. Stevens FL (1925) Plant disease fungi. MacMillan, New YorkGoogle Scholar
  47. Suárez-Moreno ZR, Caballero-Mellado J, Coutinho BG, Mendonça-Previato L, James EK, Venturi V (2012) Common features of environmental and potentially beneficial plant-associated Burkholderia. Microb Ecol 63:249–266CrossRefPubMedGoogle Scholar
  48. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA 6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729CrossRefPubMedPubMedCentralGoogle Scholar
  49. Tayeb LA, Lefevre M, Passet V, Diancourt L, Brisse S, Grimont PAD (2008) Comparative phylogenies of Burkholderia, Ralstonia, Comamonas, Brevundimonas and related organisms derived from rpoB, gyrB and rrs gene sequences. Res Microbiol 159:169–177CrossRefPubMedGoogle Scholar
  50. Teeling H, Meyerdierks A, Bauer M, Amann R, Glöckner FO (2004) Application of tetranucleotide frequencies for the assignment of genomic fragments. Environ Microbiol 6:938–947CrossRefPubMedGoogle Scholar
  51. Tindall BJ, Rosselló-Móra R, Busse HJ, Ludwig W, Kampfer P (2010) Notes on the characterization of prokaryote strains for taxonomic purposes. Int J Syst Evol Microbiol 60:249–266CrossRefPubMedGoogle Scholar
  52. Ullstrup AJ (1960) Bacterial stripe of corn. Phytopathology 50:906–910Google Scholar
  53. Van Passel MWJ, Kuramae EE, Luyf ACM, Bart A, Boekhout T (2006) The reach of the genome signature in prokaryotes. BMC Evol Biol 6:84CrossRefPubMedPubMedCentralGoogle Scholar
  54. Vial L, Groleau MC, Dekimpe V, Déziel E (2007) Burkholderia diversity and versatility: an inventory of the extracellular products. J Microbiol Biotechnol 17:1407–1429PubMedGoogle Scholar
  55. Viallard V, Poirier I, Cournoyer B, Haurat J, Wiebkin S, Ophel-Keller K, Balandreau J (1998) Burkholderia graminis sp. nov., a rhizospheric Burkholderia species, and reassessment of [Pseudomonas] phenazinium, [Pseudomonas] pyrrocinia and [Pseudomonas] glathei as Burkholderia. Int J Syst Bacteriol 48:549–563CrossRefPubMedGoogle Scholar
  56. Wu M, Scott AJ (2012) Phylogenomic analysis of bacterial and archaeal sequences with AMPHORA2. Bioinformatics 28(7):1033–1034CrossRefPubMedGoogle Scholar
  57. Yabuuchi E, Kosako Y, Oyaizu J, Yano I, Hotta H, Hashimoto Y, Ezaki T, Arakawa M (1992) Proposal of Burkholderia gen. nov. and transfer of seven species of the genus Pseudomonas homology group II to the new genus, with the type species Burkholderia cepacia (Palleroni & Holmes 1981) comb. nov. Microbiol Immunol 36:1251–1275CrossRefPubMedGoogle Scholar
  58. Yabuuchi E, Kosako Y, Yano I, Hotta H, Nishiuchi Y (1995) Transfer of two Burkholderia and an Alkaligenes species to Ralstonia gen. Nov.: proposal of Ralstonia pickettii (Ralston, Palleroni and Doudoroff, 1973) comb. Nov., Ralstonia solanacearum (Smith, 1896) comb. Nov. and Ralstonia eutropha (Davis, 1969) comb. Nov. Microbiol Immunol 39:897–904CrossRefPubMedGoogle Scholar
  59. Yarza P, Richter M, Peplies J, Euzeby J, Amann R, Schleifer KH, Ludwig W, Glockner FO, Rossello-Mora R (2008) The all-species living tree project: a 16S rRNA-based phylogenetic tree of all sequenced type strains. Syst Appl Microbiol 31:241–250CrossRefPubMedGoogle Scholar
  60. Zeigler DR (2003) Gene sequences useful for predicting relatedness of whole genomes in bacteria. Int J Syst Bacteriol 53:1893–1900CrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2017

Authors and Affiliations

  • Lucilene Lopes-Santos
    • 1
  • Daniel Bedo Assumpção Castro
    • 3
  • Mariana Ferreira-Tonin
    • 1
  • Daniele Bussioli Alves Corrêa
    • 1
  • Bevan Simon Weir
    • 2
  • Duckchul Park
    • 2
  • Laura Maria Mariscal Ottoboni
    • 3
  • Júlio Rodrigues Neto
    • 1
  • Suzete Aparecida Lanza Destéfano
    • 1
  1. 1.Laboratório de Bacteriologia VegetalInstituto BiológicoCampinasBrazil
  2. 2.Landcare ResearchAucklandNew Zealand
  3. 3.Centro de Biologia Molecular e Engenharia GenéticaUniversidade Estadual de Campinas - UNICAMPCampinasBrazil

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