Chromids Aid Genome Expansion and Functional Diversification in the Family Burkholderiaceae

Abstract

The multipartite genome structure is found in a diverse group of important symbiotic and pathogenic bacteria; however, the advantage of this genome structure remains incompletely understood. Here, we perform comparative genomics of hundreds of finished β-proteobacterial genomes to study the role and emergence of multipartite genomes. Nearly all essential secondary replicons (chromids) of the β-proteobacteria are found in the family Burkholderiaceae. These replicons arose from just two plasmid acquisition events, and they were likely stabilized early in their evolution by the presence of core genes, at least some of which were likely acquired through an inter-replicon translocation event. On average, Burkholderiaceae genera with multipartite genomes had a larger total genome size, but smaller chromosome, than genera without secondary replicons. Pangenome-level functional enrichment analyses suggested that inter-replicon functional biases are partially driven by the enrichment of secondary replicons in the accessory pangenome fraction. Nevertheless, the small overlap in orthologous groups present in each replicon's pangenome indicates a clear functional separation of the replicons. Chromids appeared biased to environmental adaptation, as the functional categories enriched on chromids were also over-represented on the chromosomes of the environmental genera (Paraburkholderia, Cupriavidus) compared to the pathogenic genera (Burkholderia, Ralstonia). Using ancestral state reconstruction, it was predicted that the rate of accumulation of modern-day genes by chromids was more rapid than the rate of gene accumulation by the chromosomes. Overall, the data are consistent with a model where the primary advantage of secondary replicons is in facilitating increased rates of gene acquisition through horizontal gene transfer, consequently resulting in a replicon enriched in genes associated with adaptation to novel environments..

Mining of Cyanobacterial Genomes Indicates That Plasmids Are Involved in the Production of Natural Products

“…One of the proposed functions of these large replicons is to increase genome plasticity through the rapid acquisition or loss of genes by HGT [61]. Here, chromids occurred in approximately 15% of the analyzed cyanobacterial genomes, and therefore seem to be more widespread in cyanobacteria than in other phyla [48].…”

Nonadaptive radiation of the gut microbiome in an adaptive radiation of Cyprinodon pupfishes with minor shifts for scale-eating

“…3-4). Burkholderiaceae is a family of proteobacteria which contains many human and animal pathogens (diCenzo et al 2019), plant and insect symbionts (Gyaneshwar et al 2011;Takeshita and Kikuchi 2017), and can be found in soil, water, and polluted environments (Coenye and Vandamme 2003;Estrada-de los Santos et al 2016). They also include some collagenase-producing bacteria, such as Burkholderia pseudomallei (Uni-ProtKB -A3P3M6; Rainbow et al 2004), which is the causative agent of melioidosis in humans (Holden et al 2004).…”

Nonadaptive radiation of the gut microbiome in an adaptive radiation ofCyprinodonpupfishes with minor shifts for scale-eating

“…3-4). Burkholderiaceae is a family of proteobacteria which contains many human and animal pathogens (diCenzo et al 2019), plant and insect symbionts (Gyaneshwar et al 2011; Takeshita and Kikuchi 2017), and can be found in soil, water, and polluted environments (Coenye and Vandamme 2003; Estrada-de los Santos et al 2016). They also include some collagenase-producing bacteria, such as Burkholderia pseudomallei (UniProtKB – A3P3M6; Rainbow et al 2004), which is the causative agent of melioidosis in humans (Holden et al 2004).…”