TY - JOUR
T1 - Structural and biochemical evidence for the emergence of a calcium-regulated actin cytoskeleton prior to eukaryogenesis
AU - Akıl, Caner
AU - Tran, Linh T.
AU - Orhant-Prioux, Magali
AU - Baskaran, Yohendran
AU - Senju, Yosuke
AU - Takeda, Shuichi
AU - Chotchuang, Phatcharin
AU - Muengsaen, Duangkamon
AU - Schulte, Albert
AU - Manser, Edward
AU - Blanchoin, Laurent
AU - Robinson, Robert C.
N1 - Funding Information:
We thank Professor Jian-Ren Shen and Professor Yuichiro Takahashi for use of reagents and access to equipment, and Hiroyuki Imachi and Masaru Nobu for sharing MK-D1 sequence data. We thank Yoshihito Kitaoku for implementing the in-house version of AF2. This work was supported by JST CREST, grant number JPMJCR19S5, Japan; by the Japan Society for the Promotion of Science (JSPS), grant number JP20H00476 and 20K06589 (YS), by the Moore-Simons Project on the Origin of the Eukaryotic Cell, grant number GBMF9743; by A*STAR, Singapore National Medical Research Council (NMRC grant OFIRG/0067/2018); by Vidyasirimedhi Institute of Science and Technology (VISTEC); and by Wesco Scientific Promotion Foundation (YS). We thank the experimental facility and the technical services provided by the Synchrotron Radiation Protein Crystallography Facility of the National Core Facility Program for Biotechnology, Ministry of Science and Technology and the National Synchrotron Radiation Research Center, a national user facility supported by the Ministry of Science and Technology, Taiwan, ROC.
Publisher Copyright:
© 2022, The Author(s).
PY - 2022/12
Y1 - 2022/12
N2 - Charting the emergence of eukaryotic traits is important for understanding the characteristics of organisms that contributed to eukaryogenesis. Asgard archaea and eukaryotes are the only organisms known to possess regulated actin cytoskeletons. Here, we determined that gelsolins (2DGels) from Lokiarchaeota (Loki) and Heimdallarchaeota (Heim) are capable of regulating eukaryotic actin dynamics in vitro and when expressed in eukaryotic cells. The actin filament severing and capping, and actin monomer sequestering, functionalities of 2DGels are strictly calcium controlled. We determined the X-ray structures of Heim and Loki 2DGels bound actin monomers. Each structure possesses common and distinct calcium-binding sites. Loki2DGel has an unusual WH2-like motif (LVDV) between its two gelsolin domains, in which the aspartic acid coordinates a calcium ion at the interface with actin. We conclude that the calcium-regulated actin cytoskeleton predates eukaryogenesis and emerged in the predecessors of the last common ancestor of Loki, Heim and Thorarchaeota.
AB - Charting the emergence of eukaryotic traits is important for understanding the characteristics of organisms that contributed to eukaryogenesis. Asgard archaea and eukaryotes are the only organisms known to possess regulated actin cytoskeletons. Here, we determined that gelsolins (2DGels) from Lokiarchaeota (Loki) and Heimdallarchaeota (Heim) are capable of regulating eukaryotic actin dynamics in vitro and when expressed in eukaryotic cells. The actin filament severing and capping, and actin monomer sequestering, functionalities of 2DGels are strictly calcium controlled. We determined the X-ray structures of Heim and Loki 2DGels bound actin monomers. Each structure possesses common and distinct calcium-binding sites. Loki2DGel has an unusual WH2-like motif (LVDV) between its two gelsolin domains, in which the aspartic acid coordinates a calcium ion at the interface with actin. We conclude that the calcium-regulated actin cytoskeleton predates eukaryogenesis and emerged in the predecessors of the last common ancestor of Loki, Heim and Thorarchaeota.
UR - http://www.scopus.com/inward/record.url?scp=85137067491&partnerID=8YFLogxK
UR - http://www.scopus.com/inward/citedby.url?scp=85137067491&partnerID=8YFLogxK
U2 - 10.1038/s42003-022-03783-1
DO - 10.1038/s42003-022-03783-1
M3 - Article
C2 - 36045281
AN - SCOPUS:85137067491
SN - 2399-3642
VL - 5
JO - Communications Biology
JF - Communications Biology
IS - 1
M1 - 890
ER -