Origin of eukaryotic-like Vps23 shapes an ancient functional interplay between ESCRT and ubiquitin system in Asgard archaea
Zhongyi Lu,
Siyu Zhang,
Yang Liu,
Runyue Xia,
Meng Li
Affiliations
Zhongyi Lu
Archaeal Biology Center, Institute for Advanced Study, Shenzhen University, Shenzhen 518060, China; Shenzhen Key Laboratory of Marine Microbiome Engineering, Institute for Advanced Study, Shenzhen University, Shenzhen 518060, China
Siyu Zhang
Archaeal Biology Center, Institute for Advanced Study, Shenzhen University, Shenzhen 518060, China; Shenzhen Key Laboratory of Marine Microbiome Engineering, Institute for Advanced Study, Shenzhen University, Shenzhen 518060, China
Yang Liu
Archaeal Biology Center, Institute for Advanced Study, Shenzhen University, Shenzhen 518060, China; Shenzhen Key Laboratory of Marine Microbiome Engineering, Institute for Advanced Study, Shenzhen University, Shenzhen 518060, China
Runyue Xia
Archaeal Biology Center, Institute for Advanced Study, Shenzhen University, Shenzhen 518060, China; Shenzhen Key Laboratory of Marine Microbiome Engineering, Institute for Advanced Study, Shenzhen University, Shenzhen 518060, China
Meng Li
Archaeal Biology Center, Institute for Advanced Study, Shenzhen University, Shenzhen 518060, China; Shenzhen Key Laboratory of Marine Microbiome Engineering, Institute for Advanced Study, Shenzhen University, Shenzhen 518060, China; Corresponding author
Summary: Functional interplay between the endosomal sorting complexes required for transport (ESCRT) and the ubiquitin system underlies the ubiquitin-dependent cargo-sorting pathway of the eukaryotic endomembrane system, yet its evolutionary origin remains unclear. Here, we show that a UEV-Vps23 protein family, which contains UEV and Vps23 domains, mediates an ancient ESCRT and ubiquitin system interplay in Asgard archaea. The UEV binds ubiquitin with high affinity, making the UEV-Vps23 a sensor for sorting ubiquitinated cargo. A steadiness box in the Vps23 domain undergoes ubiquitination through an Asgard E1, E2, and RING E3 cascade. The UEV-Vps23 switches between autoinhibited and active forms, regulating the ESCRT and ubiquitin system interplay. Furthermore, the shared sequence and structural homology among the UEV-Vps23, eukaryotic Vps23, and archaeal CdvA suggest a common evolutionary origin. Together, this work expands our understanding of the ancient ESCRT and ubiquitin system interplay that likely arose antedating divergent evolution between Asgard archaea and eukaryotes.
