TY - JOUR
T1 - A Eukaryote-Wide Perspective on the Diversity and Evolution of the ARF GTPase Protein Family
AU - Vargová, Romana
AU - Wideman, Jeremy G.
AU - Derelle, Romain
AU - Klimeš, Vladimír
AU - Kahn, Richard A.
AU - Dacks, Joel B.
AU - Eliáš, Marek
N1 - Funding Information:
We thank Eunsoo Kim (American Museum of Natural History, New York) for an access to a genome assembly of Goniomonas avonlea prior to publication and Vladimír Hampl (Charles University in Prague) for his permission to use sequences from an unpublished genome assembly of Paratrimastix pyriformis. This work was supported by Czech Science Foundation (Grant No. 20-27648S); ERD Funds (Project OPVVV CZ.02.1.01/0.0/0.0/16_019/0000759) (Centre for Research of Pathogenicity and Virulence of Parasites); and the infrastructure grant CZ.1.05/2.1.00/19.0388 (Přístroje IET). Work in the Kahn Lab was supported by a grant from the National Institutes of Health (NIH R35GM122568). Work in the Dacks Lab was supported by grants from the Natural Sciences and Engineering Research Council of Canada (RES0021028, RES0043758, RES0046091). J.B.D. is the Canada Research Chair (Tier Ii) in Evolutionary Cell Biology.
Funding Information:
We thank Eunsoo Kim (AmericanMuseum of Natural History, New York) for an access to a genome assembly of Goniomonas avonlea prior to publication and Vladimir Hampl (Charles University in Prague) for his permission to use sequences from an unpublished genome assembly of Paratrimastix pyriformis. This work was supported by Czech Science Foundation (Grant No. 20-27648S); ERD Funds (Project OPVVV CZ.02.1.01/0.0/0.0/16-019/0000759) (Centre for Research of Pathogenicity and Virulence of Parasites); and the infrastructure grant CZ.1.05/2.1.00/ 19.0388 (Pr?stroje IET). Work in the Kahn Lab was supported by a grant from the National Institutes of Health (NIH R35GM122568). Work in the Dacks Lab was supported by grants from the Natural Sciences and Engineering Research Council of Canada (RES0021028, RES0043758, RES0046091). J.B.D. is the Canada Research Chair (Tier Ii) in Evolutionary Cell Biology.
Publisher Copyright:
© 2021 The Author(s).
PY - 2021/8/1
Y1 - 2021/8/1
N2 - The evolution of eukaryotic cellular complexity is interwoven with the extensive diversification of many protein families. One key family is the ARF GTPases that act in eukaryote-specific processes, including membrane traffic, tubulin assembly, actin dynamics, and cilia-related functions. Unfortunately, our understanding of the evolution of this family is limited. Sampling an extensive set of available genome and transcriptome sequences, we have assembled a data set of over 2,000 manually curated ARF family genes from 114 eukaryotic species, including many deeply diverged protist lineages, and carried out comprehensive molecular phylogenetic analyses. These reconstructed as many as 16 ARF family members present in the last eukaryotic common ancestor, nearly doubling the previously inferred ancient system complexity. Evidence for the wide occurrence and ancestral origin of Arf6, Arl13, and Arl16 is presented for the first time. Moreover, Arl17, Arl18, and SarB, newly described here, are absent from well-studied model organisms and as a result their function(s) remain unknown. Analyses of our data set revealed a previously unsuspected diversity of membrane association modes and domain architectures within the ARF family. We detail the step-wise expansion of the ARF family in the metazoan lineage, including discovery of several new animal-specific family members. Delving back to its earliest evolution in eukaryotes, the resolved relationship observed between the ARF family paralogs sets boundaries for scenarios of vesicle coat origins during eukaryogenesis. Altogether, our work fundamentally broadens the understanding of the diversity and evolution of a protein family underpinning the structural and functional complexity of the eukaryote cells.
AB - The evolution of eukaryotic cellular complexity is interwoven with the extensive diversification of many protein families. One key family is the ARF GTPases that act in eukaryote-specific processes, including membrane traffic, tubulin assembly, actin dynamics, and cilia-related functions. Unfortunately, our understanding of the evolution of this family is limited. Sampling an extensive set of available genome and transcriptome sequences, we have assembled a data set of over 2,000 manually curated ARF family genes from 114 eukaryotic species, including many deeply diverged protist lineages, and carried out comprehensive molecular phylogenetic analyses. These reconstructed as many as 16 ARF family members present in the last eukaryotic common ancestor, nearly doubling the previously inferred ancient system complexity. Evidence for the wide occurrence and ancestral origin of Arf6, Arl13, and Arl16 is presented for the first time. Moreover, Arl17, Arl18, and SarB, newly described here, are absent from well-studied model organisms and as a result their function(s) remain unknown. Analyses of our data set revealed a previously unsuspected diversity of membrane association modes and domain architectures within the ARF family. We detail the step-wise expansion of the ARF family in the metazoan lineage, including discovery of several new animal-specific family members. Delving back to its earliest evolution in eukaryotes, the resolved relationship observed between the ARF family paralogs sets boundaries for scenarios of vesicle coat origins during eukaryogenesis. Altogether, our work fundamentally broadens the understanding of the diversity and evolution of a protein family underpinning the structural and functional complexity of the eukaryote cells.
KW - ARF family
KW - GTPases
KW - eukaryotic cell
KW - evolution
KW - last eukaryotic common ancestor
KW - posttranslational modifications
UR - http://www.scopus.com/inward/record.url?scp=85114384910&partnerID=8YFLogxK
UR - http://www.scopus.com/inward/citedby.url?scp=85114384910&partnerID=8YFLogxK
U2 - 10.1093/gbe/evab157
DO - 10.1093/gbe/evab157
M3 - Article
C2 - 34247240
AN - SCOPUS:85114384910
VL - 13
JO - Genome Biology and Evolution
JF - Genome Biology and Evolution
SN - 1759-6653
IS - 8
M1 - evab157
ER -