Institut Pasteur, Université Paris Cité, Microbiology Department, Evolutionary Biology of the Microbial Cell, 25 rue du dr Roux, 75015, Paris, France.
ISME J. 2024 Jan 8;18(1). doi: 10.1093/ismejo/wrae225.
Prokaryotic cells employ multiple protective layers crucial for defense, structural integrity, and cellular interactions in the environment. Archaea often feature an S-layer, with some species possessing additional and remarkably resistant sheaths. The archaeal sheath has been studied in Methanothrix and Methanospirillum, revealing a complex structure consisting of amyloid proteins organized into rings. Here, we conducted a comprehensive survey of sheath-forming proteins (SH proteins) across archaeal genomes. Structural modeling reveals a rich diversity of SH proteins, indicating the presence of a sheath in members of the TACK superphylum (Thermoprotei), as well as in the methanotrophic ANME-1. SH proteins are present in up to 40 copies per genome and display diverse domain arrangements suggesting multifunctional roles within the sheath, and potential involvement in cell-cell interaction with syntrophic partners. We uncover a complex evolutionary dynamic, indicating active exchange of SH proteins in archaeal communities. We find that viruses infecting sheathed archaea encode a diversity of SH-like proteins and we use them as markers to identify 580 vOTUs potentially associated with sheathed archaea. Structural modeling suggests that viral SH proteins can form complexes with the host SH proteins. We propose a previously unreported egress strategy where the expression of viral SH-like proteins may disrupt the integrity of the host sheath and facilitate viral exit during lysis. Together, our results significantly expand knowledge of the diversity and evolution of the archaeal sheath, which has been largely understudied but might have an important role in shaping microbial communities.
原核细胞采用多种保护层，这些保护层对于防御、结构完整性和细胞在环境中的相互作用至关重要。古菌通常具有 S 层，有些物种还具有额外的、具有惊人抗性的鞘。已经对 Methanothrix 和 Methanospirillum 中的古菌鞘进行了研究，揭示了一种复杂的结构，由组织成环的淀粉样蛋白组成。在这里，我们对古菌基因组中的鞘形成蛋白 (SH 蛋白) 进行了全面调查。结构建模揭示了 SH 蛋白的丰富多样性，表明 TACK 超门（热变形菌门）的成员以及产甲烷的 ANME-1 中存在鞘。SH 蛋白在每个基因组中最多存在 40 个副本，并显示出多样化的结构域排列，表明在鞘内具有多功能作用，并且可能与协同作用的伙伴进行细胞间相互作用。我们揭示了一个复杂的进化动态，表明古菌群落中 SH 蛋白的活跃交换。我们发现感染有鞘的古菌的病毒编码了多种 SH 样蛋白，我们使用它们作为标记来识别可能与有鞘的古菌相关的 580 个 vOTU。结构建模表明，病毒 SH 蛋白可以与宿主 SH 蛋白形成复合物。我们提出了一种以前未报道的出芽策略，其中病毒 SH 样蛋白的表达可能会破坏宿主鞘的完整性，并在裂解过程中促进病毒的释放。总之，我们的研究结果显著扩展了对古菌鞘的多样性和进化的认识，古菌鞘虽然研究较少，但可能在塑造微生物群落方面发挥着重要作用。
