Tracing back variations in archaeal ESCRT-based cell division to protein domain architectures

Frohn, Béla P.; Härtel, Tobias; Cox, Jürgen; Schwille, Petra

doi:10.1371/journal.pone.0266395

Cited by 12 publications

(19 citation statements)

References 43 publications

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“…Recent examination of CdvB protein sequences suggested that most of them harbor a C-terminal MIT interaction motif 2 (MIM2) that is conserved in Vps20/32/60 subunit class (53) (Figure 2). Most of the TACK genomes encode additional ESCRT III family proteins that, however, lack the wH extension as noticed previously (54). Furthermore, in thaumarchaea, none of the CdvB family proteins contain fused wH domains (54).…”

Section: Resultsmentioning

confidence: 60%

“…Domain boundaries for Saccharomyces cerevisiae are based on previously published structures and analyses (19, 55, 98). For archaeal proteins, domain boundaries are based either on previous analyses (22, 35, 53, 54) or on sequence analysis performed during this work as described under Methods. S. cerevisiae gene names are highlighted in red on the right.…”

Section: Introductionmentioning

confidence: 99%

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Diversity, Origin and Evolution of the ESCRT Systems

Makarova,

Tobiasson,

Wolf

et al. 2024

Preprint

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Endosomal Sorting Complexes Required for Transport (ESCRT) play key roles in protein sorting between membrane-bounded compartments of eukaryotic cells. Homologs of many ESCRT components are identifiable in various groups of archaea, especially in Asgardarchaeota, the archaeal phylum that is currently considered to include the closest relatives of eukaryotes, but not in bacteria. We performed a comprehensive search for ESCRT protein homologs in archaea and reconstructed ESCRT evolution using the phylogenetic tree of Vps4 ATPase (ESCRT IV) as a scaffold, using sensitive protein sequence analysis and comparison of structural models to identify previously unknown ESCRT proteins. Several distinct groups of ESCRT systems in archaea outside of Asgard were identified, including proteins structurally similar to ESCRT-I and ESCRT-II, and several other domains involved in protein sorting in eukaryotes, suggesting an early origin of these components. Additionally, distant homologs of CdvA proteins were identified in Thermoproteales which are likely components of the uncharacterized cell division system in these archaea. We propose an evolutionary scenario for the origin of eukaryotic and Asgard ESCRT complexes from ancestral building blocks, namely, the Vps4 ATPase, ESCRT-III components, wH (winged helix-turn-helix fold) and possibly also coiled-coil, and Vps28-like domains. The Last Archaeal Common Ancestor likely encompassed a complex ESCRT system that was involved in protein sorting. Subsequent evolution involved either simplification, as in the TACK superphylum, where ESCRT was co-opted for cell division, or complexification as in Asgardarchaeota. In Asgardarchaeota, the connection between ESCRT and the ubiquitin system that was previously considered a eukaryotic signature was already established.ImportanceAll eukaryotic cells possess complex intracellular membrane organization. ESCRT (Endosomal Sorting Complexes Required for Transport) plays a central role in membrane remodeling which is essential for cellular functionality in eukaryotes. Recently, it has been shown that Asgard archaea, the archaeal phylum that includes the closest known relatives of eukaryotes, encode homologs of many components of the ESCRT systems. We employed protein sequence and structure comparisons to reconstruct the evolution of ESCRT systems in archaea and identified several previously unknown homologs of ESCRT subunits, some of which can be predicted to participate in cell division. The results of this reconstruction indicate that the Last Archaeal Common ancestor already encoded a complex ESCRT system that was involved in protein sorting. In Asgard archaea, ESCRT systems evolved towards greater complexity, and in particular, the connection between ESCRT and the ubiquitin system that was previously considered a eukaryotic signature was established.

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Section: Resultsmentioning

confidence: 60%

Section: Introductionmentioning

confidence: 99%

Diversity, Origin and Evolution of the ESCRT Systems

Makarova,

Tobiasson,

Wolf

et al. 2024

Preprint

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“…ESCRT-mediated membrane remodeling is a conserved phenomenon in the cytoplasm of all eukaryotic cells. However, the recent biochemical characterization of eukaryotic-like ESCRT-I, ESCRT-II, and ESCRT-III components in Asgard archaea suggests a pre-eukaryotic origin for the ESCRT machinery (42)(43)(44). In line with this hypothesis, recent structural analyses have highlighted PspA, a bacterial protein important for membrane integrity, and VIPP1, a critical protein for thylakoid biogenesis in cyanobacteria and chloroplasts of photosynthetic eukaryotes, as members of the ESCRT-III family of proteins, capable of inducing membrane deformation upon binding (18,19,21).…”

Section: Discussion-mentioning

confidence: 99%

A conserved ESCRT-II-like protein participates in the biogenesis and maintenance of thylakoid membranes

Yilmazer,

Vetrano,

Eicke

et al. 2023

Preprint

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Thylakoids are membrane-bound compartments located in cyanobacteria and chloroplasts of plants and algae. They play an indispensable role in the light-driven reactions that enable photosynthetic organisms to convert water and carbon dioxide into oxygen and sugars. The biogenesis and maintenance of thylakoid membranes is a critical yet underappreciated area of research. One of the few known critical regulators of this process, VIPP1 (Vesicle-Inducing Protein in Plastids 1), was recently shown to be structurally similar to ESCRT-III proteins-the first evidence for ESCRT-like (Endosomal Sorting Complex Required for Transport) machinery in chloroplasts. Here, we used an affinity purification approach in two distantly related photosynthetic eukaryotes, the green alga Chlamydomonas reinhardtii and the plant Arabidopsis thaliana, to discover proteins that interact with VIPP1. Among several newly identified proteins, we focused on a highly conserved but uncharacterized protein (VIPP1-Associated protein 1, VIA1) that robustly interacts with VIPP1 in both systems. VIA1 is predicted to contain a winged-helix domain, a characteristic feature of ESCRT-II proteins that mediates the interaction with ESCRT-III proteins. The absence of VIA1 causes thylakoid swelling upon exposure to high light in Chlamydomonas and defective thylakoid biogenesis in the newly emerging leaf tissue in Arabidopsis, thereby delaying chloroplast development in this tissue. We propose that VIA1 is part of a previously unrecognized chloroplast ESCRT-like system that plays a critical role in forming, remodeling, and repairing photosynthetic membranes.

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“…While all other archaea encode only for homologs of the ESCRT-III/VPS4 module, Asgard archaea encode for homologs of the complete ESCRT system (ESCRT-I-III and VPS4) (6,7). Additionally, the sequence of Asgard ESCRT-III/VPS4 proteins is more closely related to those of eukaryotes than to other archaeal ESCRT systems (the CDV system) (5,20). Lastly, VPS4 homologs of Asgard archaea were shown to functionally interact with eukaryotic ESCRTs in both yeast and mammalian cells (5,26).…”

Section: Introductionmentioning

confidence: 99%

“…Reduced, simplified ESCRT-III systems have been identified in prokaryotes including in bacteria and archaea (named Vipp1 and PspA in bacteria and CdvB in archaea) (7, 20, 21). While the bacterial homologs were shown to remodel membranes in vitro, no VPS4 was identified in this system so far, and whether these distant homologs can sever membranes has not been clarified.…”

Section: Introductionmentioning

confidence: 99%

The Asgard archaeal ESCRT-III system forms helical filaments and remodels eukaryotic membranes, shedding light on the emergence of eukaryogenesis

Melnikov

Nachmias

Halbi

et al. 2022

Preprint

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The ESCRT machinery mediate membrane remodeling in numerous processes in cells including cell division and nuclear membrane reformation. The identification of ESCRT homologs in Asgard archaea, currently considered the closest ancestor of eukaryotes, suggests a role for ESCRTs in the membrane remodeling processes that occurred during eukaryogenesis. Yet, the function of these distant ESCRT homologs is mostly unresolved. Here we show that Asgard ESCRT-III proteins self-assemble into homo- and hetero- helical tubes, a hallmark of the eukaryotic ESCRT system. Asgard ESCRT-III tube assembly was facilitated in the presence of DNA and inhibited by DNAase. Notably, Asgard ESCRT-III filaments remodeled eukaryotic-like membrane vesicles, also in the presence of DNA, indicating an ancient role for the ESCRT complex in membrane remodeling, that may involve DNA binding. The ability of Asgard archaeal ESCRTs to remodel eukaryotic-like membranes, places them at the junction between prokaryotes and eukaryotes, substantiating a role for ESCRTs in eukaryogenesis

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Tracing back variations in archaeal ESCRT-based cell division to protein domain architectures

Cited by 12 publications

References 43 publications

Diversity, Origin and Evolution of the ESCRT Systems

Diversity, Origin and Evolution of the ESCRT Systems

A conserved ESCRT-II-like protein participates in the biogenesis and maintenance of thylakoid membranes

The Asgard archaeal ESCRT-III system forms helical filaments and remodels eukaryotic membranes, shedding light on the emergence of eukaryogenesis

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