Sheaths are diverse and abundant cell surface layers in archaea.

IF 10.8 1区 环境科学与生态学 Q1 ECOLOGY ISME Journal Pub Date : 2024-11-05 DOI:10.1093/ismejo/wrae225
Sofia Medvedeva, Guillaume Borrel, Simonetta Gribaldo
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Abstract

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.

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鞘是古细菌中种类繁多的细胞表层。
原核细胞具有多个保护层,对防御、结构完整性和细胞在环境中的相互作用至关重要。古细菌通常具有 S 层,有些种类还具有额外的、抵抗力极强的鞘。我们对 Methanothrix 和 Methanospirillum 的古菌鞘进行了研究,发现了一种由淀粉样蛋白组成的环状复杂结构。在这里,我们对整个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,表明在 TACK 超门(热蛋白门)成员以及甲烷营养型 ANME-1 中存在鞘。SH蛋白在每个基因组中有多达40个拷贝,并显示出不同的结构域排列,这表明SH蛋白在鞘内具有多功能作用,并可能参与细胞与合成伙伴的相互作用。我们发现了一种复杂的进化动态,表明在古细菌群落中 SH 蛋白的交换非常活跃。我们发现感染鞘古细菌的病毒会编码多种类型的SH蛋白,并用它们作为标记来识别可能与鞘古细菌相关的580个vOTU。结构建模表明,病毒 SH 蛋白可与宿主 SH 蛋白形成复合物。我们提出了一种以前未报道过的出膜策略,即病毒 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出膜。我们的研究结果极大地扩展了人们对古生菌鞘的多样性和进化的认识。
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来源期刊
ISME Journal
ISME Journal 环境科学-生态学
CiteScore
22.10
自引率
2.70%
发文量
171
审稿时长
2.6 months
期刊介绍: The ISME Journal covers the diverse and integrated areas of microbial ecology. We encourage contributions that represent major advances for the study of microbial ecosystems, communities, and interactions of microorganisms in the environment. Articles in The ISME Journal describe pioneering discoveries of wide appeal that enhance our understanding of functional and mechanistic relationships among microorganisms, their communities, and their habitats.
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