Coevolution of Eukaryote-like Vps4 and ESCRT-III Subunits in the Asgard Archaea

ABSTRACT The emergence of the endomembrane system is a key step in the evolution of cellular complexity during eukaryogenesis. The endosomal sorting complex required for transport (ESCRT) machinery is essential and required for the endomembrane system functions in eukaryotic cells. Recently, genes e...

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Autores principales:	Zhongyi Lu, Ting Fu, Tianyi Li, Yang Liu, Siyu Zhang, Jinquan Li, Junbiao Dai, Eugene V. Koonin, Guohui Li, Huiying Chu, Meng Li
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2020
Materias:	endomembrane system Asgard archaea ESCRT eukaryogenesis evolution Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/628c1d9e344545ea91856bcedc5e2a22
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spelling	oai:doaj.org-article:628c1d9e344545ea91856bcedc5e2a222021-11-15T15:56:47ZCoevolution of Eukaryote-like Vps4 and ESCRT-III Subunits in the Asgard Archaea10.1128/mBio.00417-202150-7511https://doaj.org/article/628c1d9e344545ea91856bcedc5e2a222020-06-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00417-20https://doaj.org/toc/2150-7511ABSTRACT The emergence of the endomembrane system is a key step in the evolution of cellular complexity during eukaryogenesis. The endosomal sorting complex required for transport (ESCRT) machinery is essential and required for the endomembrane system functions in eukaryotic cells. Recently, genes encoding eukaryote-like ESCRT protein components have been identified in the genomes of Asgard archaea, a newly proposed archaeal superphylum that is thought to include the closest extant prokaryotic relatives of eukaryotes. However, structural and functional features of Asgard ESCRT remain uncharacterized. Here, we show that Vps4, Vps2/24/46, and Vps20/32/60, the core functional components of the Asgard ESCRT, coevolved eukaryote-like structural and functional features. Phylogenetic analysis shows that Asgard Vps4, Vps2/24/46, and Vps20/32/60 are closely related to their eukaryotic counterparts. Molecular dynamics simulation and biochemical assays indicate that Asgard Vps4 contains a eukaryote-like microtubule-interacting and transport (MIT) domain that binds the distinct type 1 MIT-interacting motif and type 2 MIT-interacting motif in Vps2/24/46 and Vps20/32/60, respectively. The Asgard Vps4 partly, but much more efficiently than homologs from other archaea, complements the vps4 null mutant of Saccharomyces cerevisiae, further supporting the functional similarity between the membrane remodeling machineries of Asgard archaea and eukaryotes. Thus, this work provides evidence that the ESCRT complexes from Asgard archaea and eukaryotes are evolutionarily related and functionally similar. Thus, despite the apparent absence of endomembranes in Asgard archaea, the eukaryotic ESCRT seems to have been directly inherited from an Asgard ancestor, to become a key component of the emerging endomembrane system. IMPORTANCE The discovery of Asgard archaea has changed the existing ideas on the origins of eukaryotes. Researchers propose that eukaryotic cells evolved from Asgard archaea. This hypothesis partly stems from the presence of multiple eukaryotic signature proteins in Asgard archaea, including homologs of ESCRT proteins that are essential components of the endomembrane system in eukaryotes. However, structural and functional features of Asgard ESCRT remain unknown. Our study provides evidence that Asgard ESCRT is functionally comparable to the eukaryotic counterparts, suggesting that despite the apparent absence of endomembranes in archaea, eukaryotic ESCRT was inherited from an Asgard archaeal ancestor, alongside the emergence of endomembrane system during eukaryogenesis.Zhongyi LuTing FuTianyi LiYang LiuSiyu ZhangJinquan LiJunbiao DaiEugene V. KooninGuohui LiHuiying ChuMeng LiAmerican Society for Microbiologyarticleendomembrane systemAsgard archaeaESCRTeukaryogenesisevolutionMicrobiologyQR1-502ENmBio, Vol 11, Iss 3 (2020)
institution	DOAJ
collection	DOAJ
language	EN
topic	endomembrane system Asgard archaea ESCRT eukaryogenesis evolution Microbiology QR1-502
spellingShingle	endomembrane system Asgard archaea ESCRT eukaryogenesis evolution Microbiology QR1-502 Zhongyi Lu Ting Fu Tianyi Li Yang Liu Siyu Zhang Jinquan Li Junbiao Dai Eugene V. Koonin Guohui Li Huiying Chu Meng Li Coevolution of Eukaryote-like Vps4 and ESCRT-III Subunits in the Asgard Archaea
description	ABSTRACT The emergence of the endomembrane system is a key step in the evolution of cellular complexity during eukaryogenesis. The endosomal sorting complex required for transport (ESCRT) machinery is essential and required for the endomembrane system functions in eukaryotic cells. Recently, genes encoding eukaryote-like ESCRT protein components have been identified in the genomes of Asgard archaea, a newly proposed archaeal superphylum that is thought to include the closest extant prokaryotic relatives of eukaryotes. However, structural and functional features of Asgard ESCRT remain uncharacterized. Here, we show that Vps4, Vps2/24/46, and Vps20/32/60, the core functional components of the Asgard ESCRT, coevolved eukaryote-like structural and functional features. Phylogenetic analysis shows that Asgard Vps4, Vps2/24/46, and Vps20/32/60 are closely related to their eukaryotic counterparts. Molecular dynamics simulation and biochemical assays indicate that Asgard Vps4 contains a eukaryote-like microtubule-interacting and transport (MIT) domain that binds the distinct type 1 MIT-interacting motif and type 2 MIT-interacting motif in Vps2/24/46 and Vps20/32/60, respectively. The Asgard Vps4 partly, but much more efficiently than homologs from other archaea, complements the vps4 null mutant of Saccharomyces cerevisiae, further supporting the functional similarity between the membrane remodeling machineries of Asgard archaea and eukaryotes. Thus, this work provides evidence that the ESCRT complexes from Asgard archaea and eukaryotes are evolutionarily related and functionally similar. Thus, despite the apparent absence of endomembranes in Asgard archaea, the eukaryotic ESCRT seems to have been directly inherited from an Asgard ancestor, to become a key component of the emerging endomembrane system. IMPORTANCE The discovery of Asgard archaea has changed the existing ideas on the origins of eukaryotes. Researchers propose that eukaryotic cells evolved from Asgard archaea. This hypothesis partly stems from the presence of multiple eukaryotic signature proteins in Asgard archaea, including homologs of ESCRT proteins that are essential components of the endomembrane system in eukaryotes. However, structural and functional features of Asgard ESCRT remain unknown. Our study provides evidence that Asgard ESCRT is functionally comparable to the eukaryotic counterparts, suggesting that despite the apparent absence of endomembranes in archaea, eukaryotic ESCRT was inherited from an Asgard archaeal ancestor, alongside the emergence of endomembrane system during eukaryogenesis.
format	article
author	Zhongyi Lu Ting Fu Tianyi Li Yang Liu Siyu Zhang Jinquan Li Junbiao Dai Eugene V. Koonin Guohui Li Huiying Chu Meng Li
author_facet	Zhongyi Lu Ting Fu Tianyi Li Yang Liu Siyu Zhang Jinquan Li Junbiao Dai Eugene V. Koonin Guohui Li Huiying Chu Meng Li
author_sort	Zhongyi Lu
title	Coevolution of Eukaryote-like Vps4 and ESCRT-III Subunits in the Asgard Archaea
title_short	Coevolution of Eukaryote-like Vps4 and ESCRT-III Subunits in the Asgard Archaea
title_full	Coevolution of Eukaryote-like Vps4 and ESCRT-III Subunits in the Asgard Archaea
title_fullStr	Coevolution of Eukaryote-like Vps4 and ESCRT-III Subunits in the Asgard Archaea
title_full_unstemmed	Coevolution of Eukaryote-like Vps4 and ESCRT-III Subunits in the Asgard Archaea
title_sort	coevolution of eukaryote-like vps4 and escrt-iii subunits in the asgard archaea
publisher	American Society for Microbiology
publishDate	2020
url	https://doaj.org/article/628c1d9e344545ea91856bcedc5e2a22
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Coevolution of Eukaryote-like Vps4 and ESCRT-III Subunits in the Asgard Archaea

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