Instituto Gulbenkian de Ciência, Oeiras, Portugal.
Marine Biodiversity Group, Naturalis Biodiversity Center, Leiden, The Netherlands.
Mol Biol Evol. 2019 Dec 1;36(12):2714-2736. doi: 10.1093/molbev/msz175.
Bacteria of the Firmicutes phylum are able to enter a developmental pathway that culminates with the formation of highly resistant, dormant endospores. Endospores allow environmental persistence, dissemination and for pathogens, are also infection vehicles. In both the model Bacillus subtilis, an aerobic organism, and in the intestinal pathogen Clostridioides difficile, an obligate anaerobe, sporulation mobilizes hundreds of genes. Their expression is coordinated between the forespore and the mother cell, the two cells that participate in the process, and is kept in close register with the course of morphogenesis. The evolutionary mechanisms by which sporulation emerged and evolved in these two species, and more broadly across Firmicutes, remain largely unknown. Here, we trace the origin and evolution of sporulation using the genes known to be involved in the process in B. subtilis and C. difficile, and estimating their gain-loss dynamics in a comprehensive bacterial macroevolutionary framework. We show that sporulation evolution was driven by two major gene gain events, the first at the base of the Firmicutes and the second at the base of the B. subtilis group and within the Peptostreptococcaceae family, which includes C. difficile. We also show that early and late sporulation regulons have been coevolving and that sporulation genes entail greater innovation in B. subtilis with many Bacilli lineage-restricted genes. In contrast, C. difficile more often recruits new sporulation genes by horizontal gene transfer, which reflects both its highly mobile genome, the complexity of the gut microbiota, and an adjustment of sporulation to the gut ecosystem.
厚壁菌门的细菌能够进入一个发育途径，最终形成高度抗性的休眠芽孢。芽孢使细菌能够在环境中存活、传播，对于病原体来说，也是感染的载体。在好氧生物模式枯草芽孢杆菌和肠道病原体艰难梭菌中，芽孢形成会动员数百个基因。它们的表达在参与该过程的前芽孢和母细胞之间进行协调，并与形态发生过程紧密相关。在这两个物种中，以及更广泛的厚壁菌门中，芽孢形成是如何出现和进化的，其进化机制在很大程度上仍然未知。在这里，我们使用枯草芽孢杆菌和艰难梭菌中已知参与该过程的基因来追溯芽孢形成的起源和进化，并在全面的细菌宏观进化框架中估计它们的增益-损耗动态。我们表明，芽孢形成的进化是由两次主要的基因增益事件驱动的，第一次发生在厚壁菌门的基部，第二次发生在枯草芽孢杆菌群和包括艰难梭菌在内的消化链球菌科的基部。我们还表明，早期和晚期的芽孢形成调控因子一直在共同进化，并且芽孢形成基因在枯草芽孢杆菌中具有更多的创新，而许多芽孢杆菌谱系受限的基因则存在于芽孢杆菌中。相比之下，艰难梭菌更频繁地通过水平基因转移招募新的芽孢形成基因，这反映了其高度可移动的基因组、肠道微生物群的复杂性以及对肠道生态系统的适应。
