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Comparative Genomics of Burkholderia Singularis Sp. Nov., a Low G+C Content, Free-Living Bacterium That Defies Taxonomic Dissection of the Genus Burkholderia

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Comparative Genomics of Burkholderia Singularis Sp. Nov., a Low G+C Content, Free-Living Bacterium That Defies Taxonomic Dissection of the Genus Burkholderia Charles Darwin University Comparative Genomics of Burkholderia singularis sp. nov., a Low G+C Content, Free- Living Bacterium That Defies Taxonomic Dissection Of The Genus Burkholderia Vandamme, Peter; Peeters, Charlotte; Smet, Birgit De; Price, Erin P.; Sarovich, Derek S.; Henry, Deborah A.; Hird, Trevor J.; Zlosnik, James E.A.; Mayo, Mark; Warner, Jeffrey; Baker, Anthony; Currie, Bart J.; Carlier, Aurélien Published in: Frontiers in Microbiology DOI: 10.3389/fmicb.2017.01679 Published: 01/09/2017 Document Version Publisher's PDF, also known as Version of record Link to publication Citation for published version (APA): Vandamme, P., Peeters, C., Smet, B. D., Price, E. P., Sarovich, D. S., Henry, D. A., Hird, T. J., Zlosnik, J. E. A., Mayo, M., Warner, J., Baker, A., Currie, B. J., & Carlier, A. (2017). Comparative Genomics of Burkholderia singularis sp. nov., a Low G+C Content, Free-Living Bacterium That Defies Taxonomic Dissection Of The Genus Burkholderia. Frontiers in Microbiology, 8, 1-14. [1679]. https://doi.org/10.3389/fmicb.2017.01679 General rights Copyright and moral rights for the publications made accessible in the public portal are retained by the authors and/or other copyright owners and it is a condition of accessing publications that users recognise and abide by the legal requirements associated with these rights. • Users may download and print one copy of any publication from the public portal for the purpose of private study or research. • You may not further distribute the material or use it for any profit-making activity or commercial gain • You may freely distribute the URL identifying the publication in the public portal Take down policy If you believe that this document breaches copyright please contact us providing details, and we will remove access to the work immediately and investigate your claim. Download date: 24. Sep. 2021 fmicb-08-01679 September 4, 2017 Time: 15:24 # 1 ORIGINAL RESEARCH published: 06 September 2017 doi: 10.3389/fmicb.2017.01679 Comparative Genomics of Burkholderia singularis sp. nov., a Low GCC Content, Free-Living Bacterium That Defies Taxonomic Dissection of the Genus Burkholderia Peter Vandamme1*, Charlotte Peeters1, Birgit De Smet1, Erin P. Price2,3, Derek S. Sarovich2,3, Deborah A. Henry4, Trevor J. Hird4, James E. A. Zlosnik4, Mark Mayo2, Jeffrey Warner5, Anthony Baker6, Bart J. Currie2 and Aurélien Carlier1 1 Laboratory of Microbiology, Department of Biochemistry and Microbiology, Faculty of Sciences, Ghent University, Ghent, Belgium, 2 Global and Tropical Health Division, Menzies School of Health Research, Darwin, NT, Australia, 3 Centre for Animal Health Innovation, Faculty of Science, Health, Education and Engineering, University of the Sunshine Coast, Sippy Downs, QLD, Australia, 4 Centre for Understanding and Preventing Infection in Children, Department of Pediatrics, University of British Columbia, Vancouver, BC, Canada, 5 College of Public Health, Medical and Veterinary Sciences, Australian Institute of Tropical Health and Medicine, James Cook University, Townsville, QLD, Australia, 6 Tasmanian Institute of Agriculture, Edited by: University of Tasmania, Hobart, TAS, Australia Svetlana N. Dedysh, Winogradsky Institute of Microbiology, Russian Academy of Sciences, Russia Four Burkholderia pseudomallei-like isolates of human clinical origin were examined by Reviewed by: a polyphasic taxonomic approach that included comparative whole genome analyses. Paulina Estrada De Los Santos, The results demonstrated that these isolates represent a rare and unusual, novel Instituto Politécnico Nacional, Mexico Burkholderia species for which we propose the name B. singularis. The type strain is Prabhu B. Patil, T T Institute of Microbial Technology LMG 28154 (DCCUG 65685 ). Its genome sequence has an average mol% GCC (CSIR), India content of 64.34%, which is considerably lower than that of other Burkholderia species. *Correspondence: The reduced GCC content of strain LMG 28154T was characterized by a genome Peter Vandamme [email protected] wide AT bias that was not due to reduced GC-biased gene conversion or reductive genome evolution, but might have been caused by an altered DNA base excision Specialty section: repair pathway. B. singularis can be differentiated from other Burkholderia species This article was submitted to Evolutionary and Genomic by multilocus sequence analysis, MALDI-TOF mass spectrometry and a distinctive Microbiology, biochemical profile that includes the absence of nitrate reduction, a mucoid appearance a section of the journal on Columbia sheep blood agar, and a slowly positive oxidase reaction. Comparisons Frontiers in Microbiology with publicly available whole genome sequences demonstrated that strain TSV85, an Received: 31 May 2017 Accepted: 21 August 2017 Australian water isolate, also represents the same species and therefore, to date, Published: 06 September 2017 B. singularis has been recovered from human or environmental samples on three Citation: continents. Vandamme P, Peeters C, De Smet B, Price EP, Sarovich DS, Keywords: Burkholderia singularis, whole genome sequence, cystic fibrosis microbiology, comparative Henry DA, Hird TJ, Zlosnik JEA, genomics, Burkholderia pseudomallei complex, Burkholderia cepacia complex Mayo M, Warner J, Baker A, Currie BJ and Carlier A (2017) Comparative Genomics INTRODUCTION of Burkholderia singularis sp. nov., a Low GCC Content, Free-Living A variety of Gram-negative non-fermenting bacteria can colonize the lungs of patients with cystic Bacterium That Defies Taxonomic Dissection of the Genus Burkholderia. fibrosis (CF) (Lipuma, 2010; Parkins and Floto, 2015). The majority of these bacteria are considered Front. Microbiol. 8:1679. opportunists but correct species identification is paramount for the management of infections in doi: 10.3389/fmicb.2017.01679 these patients. More than twenty Burkholderia species have been retrieved from respiratory samples Frontiers in Microbiology| www.frontiersin.org 1 September 2017| Volume 8| Article 1679 fmicb-08-01679 September 4, 2017 Time: 15:24 # 2 Vandamme et al. Burkholderia singularis sp. nov. of patients with CF, with B. cenocepacia and B. pseudomallei the in 2008. Strains were grown aerobically on Tryptone Soya Agar major concerns (O’Carroll et al., 2003; Lipuma, 2010). When (Oxoid) and were routinely incubated at 28◦C. Cultures were the genus Burkholderia was created in 1992 it consisted of only preserved in MicroBankTM vials at −80◦C until lyophilization. seven species which were primarily known as human, animal, and plant pathogens (Yabuuchi et al., 1992). They proved, 16S rRNA Gene Sequence Analysis however, to be metabolically versatile and biotechnologically The 16S rRNA gene sequences of strains LMG 28154T and appealing, and a large number of novel Burkholderia species LMG 28155 were determined as described by Vandamme et al. were subsequently isolated and formally named. The genus (2007). Sequence assembly was performed using the BioNumerics Burkholderia now comprises about 100 validly named species1 v7 software. EzBioCloud was used to identify the nearest and many uncultivated candidate species, which occupy neighbor taxa with validly published names (Yoon et al., 2017). extremely diverse ecological niches (Coenye and Vandamme, The 16S rRNA sequences of two strains without taxonomic 2003; Compant et al., 2008; Suarez-Moreno et al., 2012). standing, i.e., Burkholderia sp. TSV85 (GenBank accession Although their metabolic potential can be exploited for GCA_001523725.1) and Burkholderia sp. TSV86 (GenBank biocontrol, bioremediation and plant growth promotion, accession GCA_001522865.1), were retrieved from their whole Burkholderia species are notorious opportunistic pathogens genome sequences as preliminary analysis of genome sequences in immunocompromised patients and cause pseudo-outbreaks indicated a close phylogenetic relationship to strain LMG 28154T. through their impressive capacity to contaminate pharmaceutical The 16S rRNA sequences of strains LMG 28154T, LMG 28155, products (Coenye and Vandamme, 2003; Torbeck et al., 2011; TSV85, TSV86 and Burkholderia representatives (1011–1610 bp) Depoorter et al., 2016). The use of Burkholderia in agricultural were aligned against the SILVA SSU reference database using applications is therefore controversial and considerable effort SINA v1.2.112 (Pruesse et al., 2012). Phylogenetic analysis was has been invested to discriminate beneficial from clinical conducted using MEGA7 (Kumar et al., 2016). All positions with Burkholderia strains (Baldwin et al., 2007; Mahenthiralingam <95% site coverage were eliminated, resulting in a total of 1311 et al., 2008). Recently, the phylogenetic diversity within positions in the final dataset. The statistical reliability of tree this genus, as revealed through comparative 16S ribosomal topologies was evaluated by bootstrapping analysis based on 1000 RNA (rRNA) gene studies, was used to subdivide this replicates. genus into Burkholderia sensu stricto (which comprises the majority of human pathogens) and several novel genera, i.e., MLST Analysis Paraburkholderia, Caballeronia, and Robbsia (Sawana et al., MLST analysis was based on the method described by Spilker 2014; Dobritsa and Samadpour, 2016; Lopes-Santos et al., 2017). et al.(2009) with small modifications as described earlier (Peeters This 16S rRNA sequence based subdivision was supported by a et al., 2013). Nucleotide sequences of each allele, allelic profiles difference in genomic GCC content: Burkholderia sensu stricto and sequence
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