Sheaths are diverse and abundant cell surface layers in archaea

Area of Science:

• Microbiology
• Structural Biology
• Evolutionary Biology

Background:

• Prokaryotic cells, including Archaea, utilize protective outer layers like S-layers and sheaths for survival and interaction.
• The archaeal sheath, composed of amyloid proteins, has been characterized in specific species but its broader diversity and function remain underexplored.

Purpose of the Study:

• To conduct a comprehensive genomic survey of sheath-forming proteins (SH proteins) across archaeal lineages.
• To investigate the structural diversity, evolutionary dynamics, and potential roles of SH proteins, including their interactions with viruses.
• To identify viral proteins associated with sheathed archaea and propose novel viral egress mechanisms.

Main Methods:

• Genome-wide survey of sheath-forming protein (SH protein) genes.
• Structural modeling of diverse SH proteins and viral SH-like proteins.
• Phylogenetic analysis to understand evolutionary relationships and horizontal gene transfer.
• Bioinformatic identification of viral OTUs (vOTUs) associated with sheathed archaea.

Main Results:

• Identified a wide diversity of SH proteins, indicating sheath presence in TACK superphylum members and ANME-1 archaea.
• SH proteins exhibit varied domain arrangements, suggesting multifunctional roles in cell structure, interaction, and potential syntrophy.
• Discovered viral SH-like proteins in viruses infecting sheathed archaea, with potential for host sheath interaction and a novel lysis-driven egress strategy.

Conclusions:

• The archaeal sheath is more diverse than previously known, with significant evolutionary exchange of SH proteins within communities.
• Viral SH-like proteins represent a novel class of viral effectors with implications for host-virus interactions and viral replication cycles.
• This study expands our understanding of archaeal sheath diversity, evolution, and its impact on microbial community structure and dynamics.