Eukaryotic RNA-guided endonucleases evolved from a unique clade of bacterial enzymes

Yoon, Peter H.; Skopintsev, Petr; Shi, Honglue; Chen, LinXing; Adler, Benjamin A.; Al-Shimary, Muntathar; Craig, Rory J.; Loi, Kenneth J.; DeTurk, Evan C.; Li, Zheng; Amerasekera, Jasmine; Trinidad, Marena; Nisonoff, Hunter; Chen, Kai; Lahiri, Arushi; Boger, Ron; Jacobsen, Steve; Banfield, Jillian F.; Doudna, Jennifer A.

doi:10.1093/nar/gkad1053

Eukaryotic RNA-guided endonucleases evolved from a unique clade of bacterial enzymes

Journal Article · Thu Nov 16 00:00:00 EST 2023 · Nucleic Acids Research

DOI:https://doi.org/10.1093/nar/gkad1053· OSTI ID:2212840

Yoon, Peter H.; Skopintsev, Petr; ; Chen, LinXing; ; Al-Shimary, Muntathar; Craig, Rory J.; Loi, Kenneth J.; DeTurk, Evan C.; Li, Zheng; Amerasekera, Jasmine; Trinidad, Marena; Nisonoff, Hunter; ; Lahiri, Arushi; Boger, Ron; ; Banfield, Jillian F.;

Abstract

RNA-guided endonucleases form the crux of diverse biological processes and technologies, including adaptive immunity, transposition, and genome editing. Some of these enzymes are components of insertion sequences (IS) in the IS200/IS605 and IS607 transposon families. Both IS families encode a TnpA transposase and a TnpB nuclease, an RNA-guided enzyme ancestral to CRISPR-Cas12s. In eukaryotes, TnpB homologs occur as two distinct types, Fanzor1s and Fanzor2s. We analyzed the evolutionary relationships between prokaryotic TnpBs and eukaryotic Fanzors, which revealed that both Fanzor1s and Fanzor2s stem from a single lineage of IS607 TnpBs with unusual active site arrangement. The widespread nature of Fanzors implies that the properties of this particular lineage of IS607 TnpBs were particularly suited to adaptation in eukaryotes. Biochemical analysis of an IS607 TnpB and Fanzor1s revealed common strategies employed by TnpBs and Fanzors to co-evolve with their cognate transposases. Collectively, our results provide a new model of sequential evolution from IS607 TnpBs to Fanzor2s, and Fanzor2s to Fanzor1s that details how genes of prokaryotic origin evolve to give rise to new protein families in eukaryotes.

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Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE; USDOE Laboratory Directed Research and Development (LDRD) Program; USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science (BSS)

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 2212840

Alternate ID(s):: OSTI ID: 2439563

Journal Information:: Nucleic Acids Research, Journal Name: Nucleic Acids Research Journal Issue: 22 Vol. 51; ISSN 0305-1048

Publisher:: Oxford University PressCopyright Statement

Country of Publication:: United Kingdom

Language:: English

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