Unit Evolutionary Biology of the Microbial Cell, Department of Microbiology, Institut Pasteur, UMR 2001 CNRS, Paris, France.
Hub Bioinformatics and Biostatistics, Department of Computational Biology, Institut Pasteur, USR 3756 CNRS, Paris, France.
Nat Ecol Evol. 2020 Dec;4(12):1661-1672. doi: 10.1038/s41559-020-01299-7. Epub 2020 Oct 19.
The transition between cell envelopes with one membrane (Gram-positive or monoderm) and those with two membranes (Gram-negative or diderm) is a fundamental open question in the evolution of Bacteria. Evidence of the presence of two independent diderm lineages, the Halanaerobiales and the Negativicutes, within the classically monoderm Firmicutes has blurred the monoderm/diderm divide and specifically anticipated that other members with an outer membrane (OM) might exist in this phylum. Here, by screening 1,639 genomes of uncultured Firmicutes for signatures of an OM, we highlight a third and deep branching diderm clade, the Limnochordia, strengthening the hypothesis of a diderm ancestor and the occurrence of independent transitions leading to the monoderm phenotype. Phyletic patterns of over 176,000 protein families constituting the Firmicutes pan-proteome identify those that strongly correlate with the diderm phenotype and suggest the existence of new potential players in OM biogenesis. In contrast, we find practically no largely conserved core of monoderms, a fact possibly linked to different ways of adapting to repeated OM losses. Phylogenetic analysis of a concatenation of main OM components totalling nearly 2,000 amino acid positions illustrates the common origin and vertical evolution of most diderm bacterial envelopes. Finally, mapping the presence/absence of OM markers onto the tree of Bacteria shows the overwhelming presence of diderm phyla and the non-monophyly of monoderm ones, pointing to an early origin of two-membraned cells and the derived nature of the Gram-positive envelope following multiple OM losses.
细胞膜为单层（革兰氏阳性菌或单胞菌）和双层（革兰氏阴性菌或双胞菌）之间的过渡是细菌进化中的一个基本问题。在经典的单胞菌Firmicutes 中，存在两个独立的双胞菌谱系——Halanaerobiales 和 Negativicutes 的证据，使得单胞菌/双胞菌的划分变得模糊，并特别预示着该门中可能存在其他具有外膜（OM）的成员。在这里，我们通过筛选未培养的Firmicutes 基因组中 1639 个基因组，寻找 OM 存在的特征，突出了第三个深分支的双胞菌类群——Limnochordia，这加强了双胞菌祖先和导致单胞菌表型的独立过渡的假说。构成Firmicutes 泛蛋白组的超过 176000 个蛋白质家族的系统发育模式，确定了那些与双胞菌表型强烈相关的蛋白质家族，并暗示了 OM 生物发生中存在新的潜在参与者。相比之下，我们发现实际上几乎没有大量保守的单胞菌核心，这一事实可能与适应多次 OM 损失的不同方式有关。将近 2000 个氨基酸位置的主要 OM 成分的串联系统发育分析说明了大多数双胞菌细菌包膜的共同起源和垂直进化。最后，将 OM 标志物的存在/缺失映射到细菌树中，表明压倒性的双胞菌门的存在和单胞菌门的非单系性，指向双层细胞的早期起源和革兰氏阳性菌包膜的衍生性质，这是在多次 OM 损失之后发生的。
