Diversity, origin, and evolution of the ESCRT systems

Area of Science:

• Cell Biology
• Evolutionary Biology
• Biochemistry

Background:

• Endosomal sorting complexes required for transport (ESCRT) are crucial for eukaryotic membrane organization and protein sorting.
• Homologs of ESCRT components are found in archaea, particularly in Asgardarchaeota, the closest known archaeal relatives to eukaryotes.
• The evolutionary history and full extent of ESCRT systems in archaea remain incompletely understood.

Purpose of the Study:

• To comprehensively search for ESCRT protein homologs across archaea.
• To reconstruct the evolutionary trajectory of ESCRT systems using phylogenetic analysis and structural comparisons.
• To elucidate the ancestral state and diversification of ESCRT complexes in archaea.

Main Methods:

• Phylogenetic analysis of Vps4 ATPase (ESCRT IV) to scaffold ESCRT evolution reconstruction.
• Sensitive protein sequence analysis to identify known and novel ESCRT homologs.
• Comparison of structural models to identify functionally similar domains across archaeal groups.

Main Results:

• Identified diverse ESCRT systems in archaea outside Asgard, including proteins resembling ESCRT-I and ESCRT-II, suggesting an early origin.
• Discovered distant CdvA protein homologs in Thermoproteales, potentially involved in their cell division.
• Reconstructed an evolutionary scenario where the last archaeal common ancestor possessed a complex ESCRT system for protein sorting.

Conclusions:

• The last archaeal common ancestor likely had a sophisticated ESCRT system for protein sorting.
• ESCRT evolution in archaea diverged, with simplification in TACK and complexification in Asgardarchaeota.
• Asgardarchaeota established an ESCRT-ubiquitin system connection, previously thought to be a eukaryotic-specific trait.