Guide-independent DNA Cleavage by Archaeal Argonaute from Methanocaldococcus Jannaschii

Overview

Journal Nat Microbiol

Specialties Microbiology
Parasitology

Date 2017 Mar 21

PMID 28319081

Citations 60

Authors

Adrian Zander

Sarah Willkomm

Sapir Ofer

Marleen van Wolferen

Luisa Egert

Sabine Buchmeier

Sarah Stockl

Philip Tinnefeld

Sabine Schneider

Andreas Klingl

Sonja-Verena Albers

Finn Werner

Dina Grohmann

Affiliations

Soon will be listed here.

Abstract

Prokaryotic Argonaute proteins acquire guide strands derived from invading or mobile genetic elements, via an unknown pathway, to direct guide-dependent cleavage of foreign DNA. Here, we report that Argonaute from the archaeal organism Methanocaldococcus jannaschii (MjAgo) possesses two modes of action: the canonical guide-dependent endonuclease activity and a non-guided DNA endonuclease activity. The latter allows MjAgo to process long double-stranded DNAs, including circular plasmid DNAs and genomic DNAs. Degradation of substrates in a guide-independent fashion primes MjAgo for subsequent rounds of DNA cleavage. Chromatinized genomic DNA is resistant to MjAgo degradation, and recombinant histones protect DNA from cleavage in vitro. Mutational analysis shows that key residues important for guide-dependent target processing are also involved in guide-independent MjAgo function. This is the first characterization of guide-independent cleavage activity for an Argonaute protein potentially serving as a guide biogenesis pathway in a prokaryotic system.

Citing Articles

Structural basis of ssDNA-guided NADase activation of prokaryotic SPARTA system.

Hu R, Guo C, Liu X, Lin Y, Yang Z, Li Z Nucleic Acids Res. 2025; 53(4).

PMID: 39997222 PMC: 11851103. DOI: 10.1093/nar/gkaf110.

Structural and mechanistic insights into the activation of a short prokaryotic argonaute system from archaeon Sulfolobus islandicus.

Dai Z, Chen Y, Guan Z, Chen X, Tan K, Yang K Nucleic Acids Res. 2025; 53(3).

PMID: 39898546 PMC: 11788926. DOI: 10.1093/nar/gkaf059.

Multiplexed food-borne pathogen detection using an argonaute-mediated digital sensor based on a magnetic-bead-assisted imaging transcoding system.

Wang Z, Cheng X, Ma A, Jiang F, Chen Y Nat Food. 2025; 6(2):170-181.

PMID: 39748032 DOI: 10.1038/s43016-024-01082-y.

The role of prokaryotic argonautes in resistance to type II topoisomerases poison ciprofloxacin.

Galivondzhyan A, Sutormin D, Panteleev V, Kulbachinskiy A, Severinov K Biochem Soc Trans. 2024; 52(5):2157-2166.

PMID: 39446311 PMC: 11555693. DOI: 10.1042/BST20240094.

Catalytically active prokaryotic Argonautes employ phospholipase D family proteins to strengthen immunity against different genetic invaders.

Cheng F, Wu A, Li Z, Xu J, Cao X, Yu H mLife. 2024; 3(3):403-416.

PMID: 39359674 PMC: 11442185. DOI: 10.1002/mlf2.12138.

References

Chandradoss S, Schirle N, Szczepaniak M, MacRae I, Joo C . A Dynamic Search Process Underlies MicroRNA Targeting. Cell. 2015; 162(1):96-107. PMC: 4768356. DOI: 10.1016/j.cell.2015.06.032. View

Willkomm S, Zander A, Grohmann D, Restle T . Mechanistic Insights into Archaeal and Human Argonaute Substrate Binding and Cleavage Properties. PLoS One. 2016; 11(10):e0164695. PMC: 5065165. DOI: 10.1371/journal.pone.0164695. View

Wagner M, Berkner S, Ajon M, Driessen A, Lipps G, Albers S . Expanding and understanding the genetic toolbox of the hyperthermophilic genus Sulfolobus. Biochem Soc Trans. 2009; 37(Pt 1):97-101. DOI: 10.1042/BST0370097. View

Nakanishi K, Weinberg D, Bartel D, Patel D . Structure of yeast Argonaute with guide RNA. Nature. 2012; 486(7403):368-74. PMC: 3853139. DOI: 10.1038/nature11211. View

Willkomm S, Oellig C, Zander A, Restle T, Keegan R, Grohmann D . Structural and mechanistic insights into an archaeal DNA-guided Argonaute protein. Nat Microbiol. 2017; 2:17035. DOI: 10.1038/nmicrobiol.2017.35. View

Meister G . Argonaute proteins: functional insights and emerging roles. Nat Rev Genet. 2013; 14(7):447-59. DOI: 10.1038/nrg3462. View

Zander A, Holzmeister P, Klose D, Tinnefeld P, Grohmann D . Single-molecule FRET supports the two-state model of Argonaute action. RNA Biol. 2014; 11(1):45-56. PMC: 3929424. DOI: 10.4161/rna.27446. View

Wang Y, Sheng G, Juranek S, Tuschl T, Patel D . Structure of the guide-strand-containing argonaute silencing complex. Nature. 2008; 456(7219):209-13. PMC: 4689319. DOI: 10.1038/nature07315. View

Parker J . How to slice: snapshots of Argonaute in action. Silence. 2010; 1(1):3. PMC: 2835997. DOI: 10.1186/1758-907X-1-3. View

10.

Wagner M, van Wolferen M, Wagner A, Lassak K, Meyer B, Reimann J . Versatile Genetic Tool Box for the Crenarchaeote Sulfolobus acidocaldarius. Front Microbiol. 2012; 3:214. PMC: 3374326. DOI: 10.3389/fmicb.2012.00214. View

11.

Miyoshi T, Ito K, Murakami R, Uchiumi T . Structural basis for the recognition of guide RNA and target DNA heteroduplex by Argonaute. Nat Commun. 2016; 7:11846. PMC: 4919518. DOI: 10.1038/ncomms11846. View

12.

Loenen W, Dryden D, Raleigh E, Wilson G, Murray N . Highlights of the DNA cutters: a short history of the restriction enzymes. Nucleic Acids Res. 2013; 42(1):3-19. PMC: 3874209. DOI: 10.1093/nar/gkt990. View

13.

Olovnikov I, Chan K, Sachidanandam R, Newman D, Aravin A . Bacterial argonaute samples the transcriptome to identify foreign DNA. Mol Cell. 2013; 51(5):594-605. PMC: 3809076. DOI: 10.1016/j.molcel.2013.08.014. View

14.

Elbashir S, Lendeckel W, Tuschl T . RNA interference is mediated by 21- and 22-nucleotide RNAs. Genes Dev. 2001; 15(2):188-200. PMC: 312613. DOI: 10.1101/gad.862301. View

15.

Elkayam E, Kuhn C, Tocilj A, Haase A, Greene E, Hannon G . The structure of human argonaute-2 in complex with miR-20a. Cell. 2012; 150(1):100-10. PMC: 3464090. DOI: 10.1016/j.cell.2012.05.017. View

16.

Schirle N, MacRae I . The crystal structure of human Argonaute2. Science. 2012; 336(6084):1037-40. PMC: 3521581. DOI: 10.1126/science.1221551. View

17.

Cheloufi S, Dos Santos C, Chong M, Hannon G . A dicer-independent miRNA biogenesis pathway that requires Ago catalysis. Nature. 2010; 465(7298):584-9. PMC: 2995450. DOI: 10.1038/nature09092. View

18.

Gao F, Shen X, Jiang F, Wu Y, Han C . DNA-guided genome editing using the Natronobacterium gregoryi Argonaute. Nat Biotechnol. 2016; 34(7):768-73. DOI: 10.1038/nbt.3547. View

19.

Elbashir S, Harborth J, Lendeckel W, Yalcin A, Weber K, Tuschl T . Duplexes of 21-nucleotide RNAs mediate RNA interference in cultured mammalian cells. Nature. 2001; 411(6836):494-8. DOI: 10.1038/35078107. View

20.

Swarts D, Hegge J, Hinojo I, Shiimori M, Ellis M, Dumrongkulraksa J . Argonaute of the archaeon Pyrococcus furiosus is a DNA-guided nuclease that targets cognate DNA. Nucleic Acids Res. 2015; 43(10):5120-9. PMC: 4446448. DOI: 10.1093/nar/gkv415. View