A long look at short prokaryotic Argonautes

Koopal, Balwina; Mutte, Sumanth K.; Swarts, Daan C.

doi:10.1016/j.tcb.2022.10.005

Cited by 35 publications

(34 citation statements)

References 99 publications

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“…In this work we focus on the truncated long-B 8 prokaryotic Argonaute AfAgo (also known as AfPIWI or Af1318 31 , 32 ) encoded by a hyperthermophilic archaeon Archaeoglobus fulgidus 8 . Although phylogenetically classified as a truncated long-B pAgo, AfAgo contains only MID and catalytically inactive PIWI domains in a single polypeptide chain, akin to typical short pAgos, and could therefore be considered a pseudo-short pAgo 33 . Even though AfAgo is one of the first and one of the best structurally characterized prokaryotic Argonautes, with an apo-, DNA-, and two RNA-bound structures currently available 31 , 32 , 34 , 35 , its guide/target preferences remain undefined.…”

Section: Introductionmentioning

confidence: 99%

Structural basis for sequence-specific recognition of guide and target strands by the Archaeoglobus fulgidus Argonaute protein

Manakova

Golovinas

Pocevičiūtė

et al. 2023

Sci Rep

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Argonaute (Ago) proteins are found in all three domains of life. The best-characterized group is eukaryotic Argonautes (eAgos). Being the structural core of RNA interference machinery, they use guide RNA molecules for RNA targeting. Prokaryotic Argonautes (pAgos) are more diverse, both in terms of structure (there are eAgo-like ‘long’ and truncated ‘short’ pAgos) and mechanism, as many pAgos are specific for DNA, not RNA guide and/or target strands. Some long pAgos act as antiviral defence systems. Their defensive role was recently demonstrated for short pAgo-encoding systems SPARTA and GsSir2/Ago, but the function and action mechanisms of all other short pAgos remain unknown. In this work, we focus on the guide and target strand preferences of AfAgo, a truncated long-B Argonaute protein encoded by an archaeon Archaeoglobus fulgidus. We demonstrate that AfAgo associates with small RNA molecules carrying 5′-terminal AUU nucleotides in vivo, and characterize its affinity to various RNA and DNA guide/target strands in vitro. We also present X-ray structures of AfAgo bound to oligoduplex DNAs that provide atomic details for base-specific AfAgo interactions with both guide and target strands. Our findings broaden the range of currently known Argonaute-nucleic acid recognition mechanisms.

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Section: Introductionmentioning

confidence: 99%

Structural basis for sequence-specific recognition of guide and target strands by the Archaeoglobus fulgidus Argonaute protein

Manakova

Golovinas

Pocevičiūtė

et al. 2023

Sci Rep

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“…Short pAgos are inactive as a result of the mutation of the catalytic tetrad, and their functions have been a mystery for a long time until most recently. It was reported that short pAgos and a (preduso)short pAgo from Sulfolobus islandicus (Si) that shares the same domain architecture as short pAgos but is not classified into the short group by the phylogenetic analysis 21 , constitute defense systems together with their associated proteins [22][23][24][25] . These defense systems confer immunity against viruses and plasmids via an abortive infection (Abi) response.…”

Section: Introductionmentioning

confidence: 99%

Long-B prokaryotic Argonaute systems employ various effectors to confer immunity via abortive infection

Song

Lei

Liu

et al. 2023

Preprint

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Argonaute proteins (Agos) bind short nucleic acids as guides and are directed by them to recognize target complementary nucleic acids. Prokaryotic Agos (pAgos) are extremely diverse, with potential functions in microbial defense. The functions and mechanisms of a group of full-length yet inactive pAgos, long-B pAgos, remain enigmatic. Here, we show that most long-B pAgos constitute cell suicide systems together with their various associated proteins, including nucleases, Sir2-domain-containing proteins and trans-membrane proteins, respectively. Among them, the long-B pAgo-nuclease system utilizes an RNA-programmed and target-recognition-activated collateral DNA cleavage activity to sense invaders and kill the infected cells. This results in depletion of the invading plasmid from the cell population. Together, our data indicate that the long-B pAgo systems induce cell death with various effector proteins after recognition of invading nucleic acids, corresponding to an immune response via abortive infection.

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“…Short pAgos are inactive as a result of the mutation of the catalytic tetrad, and their functions have been a mystery for a long time until most recently. It was reported that short pAgos and a (preduso)short pAgo from Sulfolobus islandicus (Si) constitute defense systems together with their associated proteins [20][21][22][23][24] . These short pAgos systems confer immunity against viruses and plasmids via an abortive infection (Abi) response 25 , a defense strategy kills the infected cells or induces cell dormancy to suppress the spreading of the invaders 26 .…”

Section: Introductionmentioning

confidence: 99%

Inactive long prokaryotic Argonaute systems employ various effectors to confer immunity via abortive infection

Song

Lei

Liu

et al. 2023

Preprint

View full text Add to dashboard Cite

Argonaute proteins (Agos) bind short nucleic acids as guides and are directed by them to recognize target complementary nucleic acids. Prokaryotic Agos (pAgos) are extremely diverse, with potential functions in microbial defense. The functions and mechanisms of a group of full-length yet inactive pAgos, long-B pAgos, remain enigmatic. Here, we show that most long-B pAgos constitute cell suicide systems together with their various associated proteins, including nucleases, Sir2-domain-containing proteins and trans-membrane proteins, respectively. Among them, the long-B pAgo-nuclease system utilizes an RNA-programmed and target-recognition-activated collateral DNA cleavage activity to sense invaders and mediate genomic DNA degradation. This kills the infected cells and results in depletion of the invader from the cell population. The data indicate that the long-B pAgo systems induce cell death with various effector proteins after recognition of invading nucleic acids, corresponding to an immune response via abortive infection.

show abstract

A long look at short prokaryotic Argonautes

Cited by 35 publications

References 99 publications

Structural basis for sequence-specific recognition of guide and target strands by the Archaeoglobus fulgidus Argonaute protein

Structural basis for sequence-specific recognition of guide and target strands by the Archaeoglobus fulgidus Argonaute protein

Long-B prokaryotic Argonaute systems employ various effectors to confer immunity via abortive infection

Inactive long prokaryotic Argonaute systems employ various effectors to confer immunity via abortive infection

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