Eukaryotic RNA-guided endonucleases evolved from a unique clade of bacterial enzymes-Reference-Cited by-同舟云学术

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

Published:2023-11-16 Issue:22 Volume:51 Page:12414-12427
ISSN:0305-1048
Container-title:Nucleic Acids Research
language:en
Short-container-title:

Author:

Yoon Peter H¹²,Skopintsev Petr²³,Shi Honglue²⁴^ORCID,Chen LinXing²⁵,Adler Benjamin A²³^ORCID,Al-Shimary Muntathar¹²,Craig Rory J³,Loi Kenneth J¹²,DeTurk Evan C²³,Li Zheng⁶,Amerasekera Jasmine⁷,Trinidad Marena²⁴,Nisonoff Hunter⁸,Chen Kai¹²^ORCID,Lahiri Arushi¹²,Boger Ron²³,Jacobsen Steve⁶⁹^ORCID,Banfield Jillian F²⁵,Doudna Jennifer A¹²³⁴¹⁰¹¹¹²¹³^ORCID

Affiliation:

1. Department of Molecular and Cell Biology, University of California , Berkeley ; Berkeley , CA , USA

2. Innovative Genomics Institute; University of California , Berkeley , CA , USA

3. California Institute for Quantitative Biosciences (QB3), University of California , Berkeley , CA , USA

4. Howard Hughes Medical Institute, University of California , Berkeley ; Berkeley, CA , USA

5. Department of Earth and Planetary Science, University of California , Berkeley , CA , USA

6. Department of Molecular, Cell and Developmental Biology, University of California , Los Angeles, CA , USA

7. Department of Human Genetics, University of California , Los Angeles, CA , USA

8. Center for Computational Biology, University of California , Berkeley ; Berkeley, CA, USA

9. Howard Hughes Medical Institute, University of California , Los Angeles CA , USA

10. Gladstone Institutes ; San Francisco , CA , USA

11. Gladstone-UCSF Institute of Genomic Immunology ; San Francisco , CA , USA

12. Molecular Biophysics and Integrated Bioimaging Division, Lawrence Berkeley National Laboratory ; Berkeley , CA , USA

13. Department of Chemistry, University of California , Berkeley ; Berkeley , CA , USA

Abstract

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.

Funder

Somatic Cell Genome Editing Program of the Common Fund of the National Institutes of Health

Swiss National Science Foundation Mobility fellowship

The Jane Coffin Childs Fund for Medical Research

National Institute of Health

m-CAFEs Microbial Community Analysis & Functional Evaluation in Soils

Lawrence Berkeley National Laboratory

US Department of Energy, Office of Science, Office of Biological & Environmental Research

U.S. Department of Energy

Publisher

Oxford University Press (OUP)

Subject