Department of Biology, University of Florence, Sesto Fiorentino, Florence, Italy.
Mol Biol Evol. 2019 Mar 1;36(3):562-574. doi: 10.1093/molbev/msy248.
Multipartite genomes, containing at least two large replicons, are found in diverse bacteria; however, the advantage of this genome structure remains incompletely understood. Here, we perform comparative genomics of hundreds of finished β-proteobacterial genomes to gain insights into the role and emergence of multipartite genomes. Almost 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. 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 interreplicon 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 indicated a clear functional separation of the replicons. Chromids appeared biased to environmental adaptation, as the functional categories enriched on chromids were also overrepresented on the chromosomes of the environmental genera (Paraburkholderia and Cupriavidus) compared with the pathogenic genera (Burkholderia and 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 replicons enriched in genes associated with adaptation to novel environments.
多组分基因组包含至少两个大型复制子，存在于多种细菌中；然而，这种基因组结构的优势仍不完全清楚。在这里，我们对数百个已完成的β变形菌基因组进行比较基因组学分析，以深入了解多组分基因组的作用和出现。β变形菌的几乎所有必需的次级复制子（染色体）都存在于伯克霍尔德氏菌科中。这些复制子源自两次质粒获得事件，并且它们在进化早期可能由于核心基因的存在而得到稳定。平均而言，具有多组分基因组的伯克霍尔德氏菌科属的总基因组大小较大，但染色体较小，而没有次级复制子的属则较小。泛基因组水平的功能富集分析表明，复制子之间的功能偏向部分是由辅助泛基因组部分中次级复制子的富集驱动的。然而，每个复制子的泛基因组中存在的同源基因组的小重叠表明复制子之间存在明显的功能分离。染色体似乎偏向于环境适应，因为在染色体上富集的功能类别在环境属（Paraburkholderia 和 Cupriavidus）中也比在病原属（Burkholderia 和 Ralstonia）中更为丰富。通过祖先状态重建预测，染色体积累现代基因的速率比染色体积累基因的速率更快。总的来说，数据与以下模型一致：次级复制子的主要优势在于促进通过水平基因转移增加基因的获得速度，从而导致复制子富含与适应新环境相关的基因。
