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.
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References
Almeida IMG, Berian LOS, Sannazzaro AM, Rodrigues Neto J (2009) Mancha bacteriana em Ruscus sp. causada por Burkholderia andropogonis no Brasil. Trop Plant Pathol 34:339–342
Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment searchtool. J Mol Biol 215:403–410
Bohlin J, Skjerve E, Ussery DW (2008) Reliability and applications of statistical methods based on oligonucleotide frequencies in bacterial and archaeal genomes. BMC Genom 9:104
Castresana J (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 17(4):540–552
Coenye T, Gevers D, Van de Peer Y, Vandamme P, Swings J (2005) Towards a prokaryotic genomic taxonomy. FEMS Microbiol Rev 29(2):147–167
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 53:129–135
Darriba D, Taboada GL, Doallo R, Posada D (2011) ProtTest 3: fast selection of best-fit models of protein evolution. Bioinformatics 27:1164–1165
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 66:2836–2846
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 93:607–614
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 67:51–60
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
Euzéby JP (1997) List of bacterial names with standing in nomenclature: a folder available on the Internet. Int J Syst Bacteriol 47:590–592
Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791
Fuerst JA, Hayward AC (1969) The sheathed flagellum of Pseudomonas stizolobii. J Clin Microbiol 59:239–245
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 45:274–289
Gitaitis RD, Miller J, Wells HD (1983) Bacterial leaf spot of clover in Georgia. Plant Dis 67:913–914
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 57:81–91
Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704
Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98
Hall N (2007) Advanced sequencing technologies and their wide impact in microbiology. J Exp Biol 210(9):1518–1525
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):119
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 64:346–351
Konstantinidis KT, Tiedje JM (2005) Towards a genome-based taxonomy for prokaryotes. J Bacteriol 187(18):6258–6264
Konstantinidis KT, Ramette A, Tiedje JM (2006) The bacterial species definition in the genomic era. Philos Trans R Soc B 361(1475):1929–1940
Lane DJ (1991) 16S/23S rRNA sequencing. In: Stackebrandt E, Goodfellow M (eds) Nucleic acid techniques in bacterial systematics. Wiley, New York, pp 115–147
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 89:1132
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 74:324–329
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):1–2
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 56:1031–1038
Mitchell RE (1994) Dihydrorhizobitoxine, a minor product of Pseudomonas andropogonis. Phytochemistry 37:373–375
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 35:34–43
Okazaki S, Nukui N, Sugawara M, Minamisawa K (2004) Rhizobial strategies to enhance symbiotic interaction: rhizobitoxine and 1-aminocyclopropane-1-carboxylate deaminase. Microbes Environ 19:99–111
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 141–199
Patel JB (2001) 16S rRNA gene sequencing for bacterial pathogen identification in the clinical laboratory. Mol Diagn 6:313–321
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 71:3917–3927
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 50:1021–1028
Pitcher DG, Saunders NA, Owen RJ (1989) Rapid extraction of bacterial genomic DNA with guanidium thiocyanate. Lett Appl Microbiol 8:151–156
Pride DT, Meinersmann RJ, Wassenaar TM, Blaser MJ (2003) Evolutionary implications of microbial genome tetranucleotide frequency biases. Genome Res 13(2):145–158
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):2210–2215
Richter M, Rosselló-Móra R (2009) Shifting the genomic gold standard for the prokaryotic species definition. Proc Natl Acad Sci 106(45):19126–19131
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 48:31–36
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 5:429
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):539
Smith EF (1911) Bacteria in relation to plant diseases. Carnegie Institute Publications, Washington, DC
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 44:846–849
Stevens FL (1925) Plant disease fungi. MacMillan, New York
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 63:249–266
Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA 6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729
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 159:169–177
Teeling H, Meyerdierks A, Bauer M, Amann R, Glöckner FO (2004) Application of tetranucleotide frequencies for the assignment of genomic fragments. Environ Microbiol 6:938–947
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 60:249–266
Ullstrup AJ (1960) Bacterial stripe of corn. Phytopathology 50:906–910
Van Passel MWJ, Kuramae EE, Luyf ACM, Bart A, Boekhout T (2006) The reach of the genome signature in prokaryotes. BMC Evol Biol 6:84
Vial L, Groleau MC, Dekimpe V, Déziel E (2007) Burkholderia diversity and versatility: an inventory of the extracellular products. J Microbiol Biotechnol 17:1407–1429
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 48:549–563
Wu M, Scott AJ (2012) Phylogenomic analysis of bacterial and archaeal sequences with AMPHORA2. Bioinformatics 28(7):1033–1034
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 36:1251–1275
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 39:897–904
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 31:241–250
Zeigler DR (2003) Gene sequences useful for predicting relatedness of whole genomes in bacteria. Int J Syst Bacteriol 53:1893–1900
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We thank the São Paulo Research Foundation (FAPESP) for financial support (Grant #2011/12222-2 and #2011/50813-2).
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The 16S rRNA gene sequence of B. andropogonis Type strain IBSBF 199 determined in this study was deposited in the GenBank/EMBL/DDBJ databases under the accession number KM083264.
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Lopes-Santos, L., Castro, D.B.A., Ferreira-Tonin, M. et al. Reassessment of the taxonomic position of Burkholderia andropogonis and description of Robbsia andropogonis gen. nov., comb. nov.. Antonie van Leeuwenhoek 110, 727–736 (2017). https://doi.org/10.1007/s10482-017-0842-6
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DOI: https://doi.org/10.1007/s10482-017-0842-6