start-ver=1.4
cd-journal=joma
no-vol=
cd-vols=
no-issue=
article-no=
start-page=117
end-page=33
dt-received=
dt-revised=
dt-accepted=
dt-pub-year=2020
dt-pub=20200818
dt-online=
en-article=
kn-article=
en-subject=
kn-subject=
en-title=
kn-title=Insights into the evolution of regulated actin dynamics via characterization of primitive gelsolin/cofilin proteins from Asgard archaea
en-subtitle=
kn-subtitle=
en-abstract=
kn-abstract=Asgard archaea genomes contain potential eukaryotic-like genes that provide intriguing insight for the evolution of eukaryotes. The eukaryotic actin polymerization/depolymerization cycle is critical for providing force and structure in many processes, including membrane remodeling. In general, Asgard genomes encode two classes of actin-regulating proteins from sequence analysis, profilins and gelsolins. Asgard profilins were demonstrated to regulate actin filament nucleation. Here, we identify actin filament severing, capping, annealing and bundling, and monomer sequestration activities by gelsolin proteins from Thorarchaeota (Thor), which complete a eukaryotic-like actin depolymerization cycle, and indicate complex actin cytoskeleton regulation in Asgard organisms. Thor gelsolins have homologs in other Asgard archaea and comprise one or two copies of the prototypical gelsolin domain. This appears to be a record of an initial preeukaryotic gene duplication event, since eukaryotic gelsolins are generally comprise three to six domains. X-ray structures of these proteins in complex with mammalian actin revealed similar interactions to the first domain of human gelsolin or cofilin with actin. Asgard two-domain, but not one-domain, gelsolins contain calcium-binding sites, which is manifested in calcium-controlled activities. Expression of two-domain gelsolins in mammalian cells enhanced actin filament disassembly on ionomycin-triggered calcium release. This functional demonstration, at the cellular level, provides evidence for a calcium-controlled Asgard actin cytoskeleton, indicating that the calcium-regulated actin cytoskeleton predates eukaryotes. In eukaryotes, dynamic bundled actin filaments are responsible for shaping filopodia and microvilli. By correlation, we hypothesize that the formation of the protrusions observed from Lokiarchaeota cell bodies may involve the gelsolin-regulated actin structures.
en-copyright=
kn-copyright=

en-aut-name=Ak?lCaner
en-aut-sei=Ak?l
en-aut-mei=Caner
kn-aut-name=
kn-aut-sei=
kn-aut-mei=
aut-affil-num=1
ORCID=

en-aut-name=TranLinh T.
en-aut-sei=Tran
en-aut-mei=Linh T.
kn-aut-name=
kn-aut-sei=
kn-aut-mei=
aut-affil-num=2
ORCID=

en-aut-name=Orhant-PriouxMagali
en-aut-sei=Orhant-Prioux
en-aut-mei=Magali
kn-aut-name=
kn-aut-sei=
kn-aut-mei=
aut-affil-num=3
ORCID=

en-aut-name=BaskaranYohendran
en-aut-sei=Baskaran
en-aut-mei=Yohendran
kn-aut-name=
kn-aut-sei=
kn-aut-mei=
aut-affil-num=4
ORCID=

en-aut-name=ManserEdward
en-aut-sei=Manser
en-aut-mei=Edward
kn-aut-name=
kn-aut-sei=
kn-aut-mei=
aut-affil-num=5
ORCID=

en-aut-name=BlanchoinLaurent
en-aut-sei=Blanchoin
en-aut-mei=Laurent
kn-aut-name=
kn-aut-sei=
kn-aut-mei=
aut-affil-num=6
ORCID=

en-aut-name=RobinsonRobert C.
en-aut-sei=Robinson
en-aut-mei=Robert C.
kn-aut-name=
kn-aut-sei=
kn-aut-mei=
aut-affil-num=7
ORCID=

affil-num=1
en-affil=Institute of Molecular and Cell Biology, Agency for Science, Technology and Research
kn-affil=

affil-num=2
en-affil=Research Institute for Interdisciplinary Science, Okayama University
kn-affil=

affil-num=3
en-affil=CytomorphoLab, Interdisciplinary Research Institute of Grenoble
kn-affil=

affil-num=4
en-affil=aInstitute of Molecular and Cell Biology, Agency for Science, Technology and Research
kn-affil=

affil-num=5
en-affil=aInstitute of Molecular and Cell Biology, Agency for Science, Technology and Research
kn-affil=

affil-num=6
en-affil=CytomorphoLab, Interdisciplinary Research Institute of Grenoble
kn-affil=

affil-num=7
en-affil=cResearch Institute for Interdisciplinary Science, Okayama University
kn-affil=
en-keyword=actin
kn-keyword=actin
en-keyword=gelsolin
kn-keyword=gelsolin
en-keyword=Asgard archaea
kn-keyword=Asgard archaea
en-keyword=eukaryogenesis
kn-keyword=eukaryogenesis
en-keyword=X-ray crystallography
kn-keyword=X-ray crystallography
END