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Genome Data Provides High Support for Generic Boundaries in Burkholderia Sensu Lato.

ABSTRACT: Although the taxonomy of Burkholderia has been extensively scrutinized, significant uncertainty remains regarding the generic boundaries and composition of this large and heterogeneous taxon. Here we used the amino acid and nucleotide sequences of 106 conserved proteins from 92 species to infer robust maximum likelihood phylogenies with which to investigate the generic structure of Burkholderia sensu lato. These data unambiguously supported five distinct lineages, of which four correspond to Burkholderia sensu stricto and the newly introduced genera Paraburkholderia, Caballeronia, and Robbsia. The fifth lineage was represented by P. rhizoxinica. Based on these findings, we propose 13 new combinations for those species previously described as members of Burkholderia but that form part of Caballeronia. These findings also suggest revision of the taxonomic status of P. rhizoxinica as it is does not form part of any of the genera currently recognized in Burkholderia sensu lato. From a phylogenetic point of view, Burkholderia sensu stricto has a sister relationship with the Caballeronia+Paraburkholderia clade. Also, the lineages represented by P. rhizoxinica and R. andropogonis, respectively, emerged prior to the radiation of the Burkholderia sensu stricto+Caballeronia+Paraburkholderia clade. Our findings therefore constitute a solid framework, not only for supporting current and future taxonomic decisions, but also for studying the evolution of this assemblage of medically, industrially and agriculturally important species.

SUBMITTER: Beukes CW

PROVIDER: S-EPMC5483467 | biostudies-literature | 2017

REPOSITORIES: biostudies-literature

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Genome Data Provides High Support for Generic Boundaries in Burkholderia Sensu Lato.

Beukes Chrizelle W CW Palmer Marike M Manyaka Puseletso P Chan Wai Y WY Avontuur Juanita R JR van Zyl Elritha E Huntemann Marcel M Clum Alicia A Pillay Manoj M Palaniappan Krishnaveni K Varghese Neha N Mikhailova Natalia N Stamatis Dimitrios D Reddy T B K TBK Daum Chris C Shapiro Nicole N Markowitz Victor V Ivanova Natalia N Kyrpides Nikos N Woyke Tanja T Blom Jochen J Whitman William B WB Venter Stephanus N SN Steenkamp Emma T ET

Frontiers in microbiology 20170626

Although the taxonomy of Burkholderia has been extensively scrutinized, significant uncertainty remains regarding the generic boundaries and composition of this large and heterogeneous taxon. Here we used the amino acid and nucleotide sequences of 106 conserved proteins from 92 species to infer robust maximum likelihood phylogenies with which to investigate the generic structure of Burkholderia sensu lato. These data unambiguously supported five distinct lineages, of which four cor ...[more]

PMID: 28694797

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Project description:BackgroundBacillus cereus sensu lato (s. l.) is an ecologically diverse bacterial group of medical and agricultural significance. In this study, I use publicly available genomes and novel bioinformatic workflows to characterize the B. cereus s. l. pan-genome and perform the largest phylogenetic and population genetic analyses of this group to date in terms of the number of genes and taxa included. With these fundamental data in hand, I identify genes associated with particular phenotypic traits (i.e., "pan-GWAS" analysis), and quantify the degree to which taxa sharing common attributes are phylogenetically clustered.MethodsA rapid k-mer based approach (Mash) was used to create reduced representations of selected Bacillus genomes, and a fast distance-based phylogenetic analysis of this data (FastME) was performed to determine which species should be included in B. cereus s. l. The complete genomes of eight B. cereus s. l. species were annotated de novo with Prokka, and these annotations were used by Roary to produce the B. cereus s. l. pan-genome. Scoary was used to associate gene presence and absence patterns with various phenotypes. The orthologous protein sequence clusters produced by Roary were filtered and used to build HaMStR databases of gene models that were used in turn to construct phylogenetic data matrices. Phylogenetic analyses used RAxML, DendroPy, ClonalFrameML, PAUP*, and SplitsTree. Bayesian model-based population genetic analysis assigned taxa to clusters using hierBAPS. The genealogical sorting index was used to quantify the phylogenetic clustering of taxa sharing common attributes.ResultsThe B. cereus s. l. pan-genome currently consists of ≈60,000 genes, ≈600 of which are "core" (common to at least 99% of taxa sampled). Pan-GWAS analysis revealed genes associated with phenotypes such as isolation source, oxygen requirement, and ability to cause diseases such as anthrax or food poisoning. Extensive phylogenetic analyses using an unprecedented amount of data produced phylogenies that were largely concordant with each other and with previous studies. Phylogenetic support as measured by bootstrap probabilities increased markedly when all suitable pan-genome data was included in phylogenetic analyses, as opposed to when only core genes were used. Bayesian population genetic analysis recommended subdividing the three major clades of B. cereus s. l. into nine clusters. Taxa sharing common traits and species designations exhibited varying degrees of phylogenetic clustering.ConclusionsAll phylogenetic analyses recapitulated two previously used classification systems, and taxa were consistently assigned to the same major clade and group. By including accessory genes from the pan-genome in the phylogenetic analyses, I produced an exceptionally well-supported phylogeny of 114 complete B. cereus s. l. genomes. The best-performing methods were used to produce a phylogeny of all 498 publicly available B. cereus s. l. genomes, which was in turn used to compare three different classification systems and to test the monophyly status of various B. cereus s. l. species. The majority of the methodology used in this study is generic and could be leveraged to produce pan-genome estimates and similarly robust phylogenetic hypotheses for other bacterial groups.

Project description:Burkholderia sensu lato is a collection of closely related genera within the family Burkholderiaceae that includes species of environmental, industrial, biotechnological, and clinical importance. Multiple species within the complex are the source of diverse specialized metabolites, many of which have been identified through genome mining of their biosynthetic gene clusters (BGCs). However, the full, true genomic diversity of these species and genera, and their biosynthetic capacity have not been investigated. This study sought to cluster and classify over 4000 Burkholderia sensu lato genome assemblies into distinct genomic taxa representing named and uncharacterized species. We delineated 235 species groups by average nucleotide identity analyses that formed seven distinct phylogenomic clades, representing the genera of Burkholderia sensu lato: Burkholderia, Paraburkholderia, Trinickia, Caballeronia, Mycetohabitans, Robbsia, and Pararobbisa. A total of 137 genomic taxa aligned with named species possessing a sequenced type strain, while 93 uncharacterized species groups were demarcated. The 95% ANI threshold proved capable of delineating most genomic species and was only increased to resolve several closely related species. These analyses enabled the assessment of species classifications of over 4000 genomes, and the correction of over 400 genome taxonomic assignments in public databases into existing and uncharacterized genomic species groups. These species groups were genome mined for BGCs, their specialized metabolite capacity calculated per species and genus, and the number of distinct BGCs per species estimated through kmer-based de-replication. Mycetohabitans species dedicated a larger proportion of their relatively small genomes to specialized metabolite biosynthesis, while Burkholderia species harbored more BGCs on average per genome and possessed the most distinct BGCs per species compared to the remaining genera. Exploring the hidden genomic diversity of this important multi-genus complex contributes to our understanding of their taxonomy and evolutionary relationships, and supports future efforts toward natural product discovery.

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Genome Data Provides High Support for Generic Boundaries in Burkholderia Sensu Lato.

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Genome Data Provides High Support for Generic Boundaries in <i>Burkholderia</i> Sensu Lato.

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