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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

Amandeep Sawana, Mobolaji Adeolu, Radhey S. Gupta

Frontiers in Genetics · 2014

doi:10.3389/fgene.2014.00429

Abstract

The genus Burkholderia contains large number of diverse species which include many clinically important organisms, phytopathogens, as well as environmental species. However, currently, there is a paucity of biochemical or molecular characteristics which can reliably distinguish different groups of Burkholderia species. We report here the results of detailed phylogenetic and comparative genomic analyses of 45 sequenced species of the genus Burkholderia. In phylogenetic trees based upon concatenated sequences for 21 conserved proteins as well as 16S rRNA gene sequence based trees, members of the genus Burkholderia grouped into two major clades. Within these main clades a number of smaller clades including those corresponding to the clinically important Burkholderia cepacia complex (BCC) and the Burkholderia pseudomallei groups were also clearly distinguished. Our comparative analysis of protein sequences from Burkholderia spp. has identified 42 highly specific molecular markers in the form of conserved sequence indels (CSIs) that are uniquely found in a number of well-defined groups of Burkholderia spp. Six of these CSIs are specific for a group of Burkholderia spp. (referred to as Clade I in this work) which contains all clinically relevant members of the genus (viz. the BCC and the B. pseudomallei group) as well as the phytopathogenic Burkholderia spp. The second main clade (Clade II), which is composed of environmental Burkholderia species, is also distinguished by 2 identified CSIs that are specific for this group. Additionally, our work has also identified multiple CSIs that serve to clearly demarcate a number of smaller groups of Burkholderia spp. including 3 CSIs that are specific for the B. cepacia complex, 4 CSIs that are uniquely found in the B. pseudomallei group, 5 CSIs that are specific for the phytopathogenic Burkholderia spp. and 22 other CSI that distinguish two groups within Clade II. The described molecular markers provide highly specific means for the demarcation of different groups of Burkholderia spp. and they also offer novel and useful targets for the development of diagnostic assays for the clinically important members of the BCC or the pseudomallei groups. Based upon the results of phylogenetic analyses, the identified CSIs and the pathogenicity profile of Burkholderia species, we are proposing a division of the genus Burkholderia into two genera. In this new proposal, the emended genus Burkholderia will correspond to the Clade I and it will contain only the clinically relevant and phytopathogenic Burkholderia species. All other Burkholderia spp., which are primarily environmental, will be transferred to a new genus Paraburkholderia gen. nov.

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    Tavaré S. (1986 ). Some probabilistic and statistical problems in the analysis of DNA sequences, in Lectures on Mathematics in the Life Sciences, 17 Edn, ed Miura R. M. (Providence (RI): American Mathematical Society), 57–86.

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    Tian Y. Kong B. H. Liu S. L. Li C. L. Yu R. Liu L.. (2013 ). Burkholderia grimmiae sp. nov., isolated from a xerophilous moss (Grimmia montana). Int. J. Syst. Evol. Microbiol. 63(Pt 6), 2108–2113.

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    Vandamme P. Dawyndt P. (2011 ). Classification and identification of the Burkholderia cepacia complex: past, present and future. Syst. Appl. Microbiol. 34, 87–95.

    Not in our library10.1016/j.syapm.2010.10.002

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    Vandamme P. De Brandt E. Houf K. Salles J. F. van Elsas J. D. Spilker T.. (2013 ). Burkholderia humi sp. nov., Burkholderia choica sp. nov., Burkholderia telluris sp. nov., Burkholderia terrestris sp. nov. and Burkholderia udeis sp. nov.: Burkholderia glathei-like bacteria from soil and rhizosphere soil. Int. J. Syst. Evol. Microbiol. 63(Pt 12), 4707–4718.

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    Vandamme P. Goris J. Chen W. M. de Vos P. Willems A. (2002b ). Burkholderia tuberum sp. nov. andBurkholderia phymatum sp. nov., nodulate the roots of tropical legumes. Syst. Appl. Microbiol. 25, 507–512.

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    Vandamme P. Goris J. Chen W.-M. De Vos P. Willems A. (2002a ). Burkholderia tuberum sp. nov. and Burkholderia phymatum sp. nov., nodulate the roots of tropical legumes. Syst. Appl. Microbiol. 25, 507–512.

    Not in our library10.1078/07232020260517634

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    Vandamme P. Holmes B. Vancanneyt M. Coenye T. Hoste B. Coopman R.. (1997 ). Occurrence of multiple genomovars of Burkholderia cepacia in cystic fibrosis patients and proposal of Burkholderia multivorans sp. nov. Int. J. Syst. Bacteriol. 47, 1188–1200.

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    Vandamme P. Opelt K. Knöchel N. Berg C. Schönmann S. De Brandt E.. (2007 ). Burkholderia bryophila sp. nov. andBurkholderia megapolitana sp. nov., moss-associated species with antifungal and plant-growth-promoting properties. Int. J. Syst. Evol. Microbiol. 57, 2228–2235.

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  108. 108.

    Vanlaere E. van der Meer J. R. Falsen E. Salles J. F. De Brandt E. Vandamme P. (2008 ). Burkholderia sartisoli sp. nov., isolated from a polycyclic aromatic hydrocarbon-contaminated soil. Int. J. Syst. Evol. Microbiol. 58, 420–423.

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    Van Oevelen S. De Wachter R. Vandamme P. Robbrecht E. Prinsen E. (2002a ). Identification of the bacterial endosymbionts in leaf galls of Psychotria (Rubiaceae, angiosperms) and proposal of'Candidatus Burkholderia kirkii'sp. nov. Int. J. Syst. Evol. Microbiol. 52, 2023–2027.

    Not in our library10.1099/ijs.0.02103-0

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    Van Oevelen S. De Wachter R. Vandamme P. Robbrecht E. Prinsen E. (2002b ). Identification of the bacterial endosymbionts in leaf galls of Psychotria (Rubiaceae, angiosperms) and proposal of ‘Candidatus Burkholderia kirkii’ sp. nov. Int. J. Syst. Evol. Microbiol. 52(Pt 6), 2023–2027.

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    Van Oevelen S. De Wachter R. Vandamme P. Robbrecht E. Prinsen E. (2004 ). ‘Candidatus Burkholderia calva’ and ‘Candidatus Burkholderia nigropunctata’ as leaf gall endosymbionts of African Psychotria. Int. J. Syst. Evol. Microbiol. 54, 2237–2239.

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    Weilharter A. Mitter B. Shin M. V. Chain P. S. Nowak J. Sessitsch A. (2011 ). Complete genome sequence of the plant growth-promoting endophyteBurkholderia phytofirmans strain PsJN. J. Bacteriol. 193, 3383–3384.

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    Not in our library10.1111/j.1574-6968.2007.00949.x

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    Not in our library10.1038/nrmicro1385

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    Wong S. Y. Paschos A. Gupta R. S. Schellhorn H. E. (2014 ). Insertion/deletion-based approach for the detection of Escherichia coli O157:H7 in freshwater environments. Environ. Sci. Technol. 48, 11462–11470.

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    Wu D. Hugenholtz P. Mavromatis K. Pukall R. Dalin E. Ivanova N. N.. (2009 ). A phylogeny-driven genomic encyclopaedia of Bacteria and Archaea. Nature 462, 1056–1060.

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    Yabuuchi E. Kosako Y. Oyaizu H. Yano I. Hotta H. Hashimoto Y.. (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 and Holmes 1981) comb. nov. Microbiol. Immunol. 36, 1251–1275.

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    Yabuuchi E. Kosako Y. Oyaizu H. Yano I. Hotta H. Hashimoto Y. (1993 ). Burkholderia gen. nov. validation of the publication of new names and new combinations previously effectively published outside the IJSB, List no 43. Int. J. Syst. Bacteriol. 43, 398–399

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    Yarza P. Richter M. Peplies J. Euzeby J. Amann R. Schleifer K. H.. (2008 ). The All-Species Living Tree project: A 16S rRNA-based phylogenetic tree of all sequenced type strains. Syst. Appl. Microbiol. 31, 241–250.

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    Yoo S.-H. Kim B.-Y. Weon H.-Y. Kwon S.-W. Go S.-J. Stackebrandt E. (2007 ). Burkholderia soli sp. nov., isolated from soil cultivated with Korean ginseng. Int. J. Syst. Evol. Microbiol. 57, 122–125.

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    Zhang H. Hanada S. Shigematsu T. Shibuya K. Kamagata Y. Kanagawa T.. (2000 ). Burkholderia kururiensis sp. nov., a trichloroethylene (TCE)-degrading bacterium isolated from an aquifer polluted with TCE. Int. J. Syst. Evol. Microbiol. 50, 743–749.

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