Anti-CRISPR proteins encoded by archaeal lytic viruses inhibit subtype I-D immunity

Fei He; Yuvaraj Bhoobalan; Lan B. Van; Anders Lynge Kjeldsen; Matteo Dedola; Kira S. Makarova; Eugene V. Koonin; Ditlev E. Brodersen; Xu Peng

doi:10.1038/s41564-018-0120-z

Anti-CRISPR proteins encoded by archaeal lytic viruses inhibit subtype I-D immunity

Fei He, Yuvaraj Bhoobalan, Lan B. Van, Anders Lynge Kjeldsen, Matteo Dedola, Kira S. Makarova, Eugene V. Koonin, Ditlev E. Brodersen, Xu Peng^*

^*Corresponding author for this work

Functional Genomics

63 Citations (Scopus)

Abstract

Viruses employ a range of strategies to counteract the prokaryotic adaptive immune system, clustered regularly interspaced short palindromic repeats and CRISPR-associated proteins (CRISPR-Cas), including mutational escape and physical blocking of enzymatic function using anti-CRISPR proteins (Acrs). Acrs have been found in many bacteriophages but so far not in archaeal viruses, despite the near ubiquity of CRISPR-Cas systems in archaea. Here, we report the functional and structural characterization of two archaeal Acrs from the lytic rudiviruses, SIRV2 and SIRV3. We show that a 4 kb deletion in the SIRV2 genome dramatically reduces infectivity in Sulfolobus islandicus LAL14/1 that carries functional CRISPR-Cas subtypes I-A, I-D and III-B. Subsequent insertion of a single gene from SIRV3, gp02 (AcrID1), which is conserved in the deleted fragment, successfully restored infectivity. We demonstrate that AcrID1 protein inhibits the CRISPR-Cas subtype I-D system by interacting directly with Cas10d protein, which is required for the interference stage. Sequence and structural analysis of AcrID1 show that it belongs to a conserved family of compact, dimeric αβ-sandwich proteins characterized by extreme pH and temperature stability and a tendency to form protein fibres. We identify about 50 homologues of AcrID1 in four archaeal viral families demonstrating the broad distribution of this group of anti-CRISPR proteins.

Original language	English
Journal	Nature Microbiology
Volume	3
Issue number	4
Pages (from-to)	461-469
Number of pages	9
ISSN	2058-5276
DOIs	https://doi.org/10.1038/s41564-018-0120-z
Publication status	Published - 2018

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title = "Anti-CRISPR proteins encoded by archaeal lytic viruses inhibit subtype I-D immunity",

abstract = "Viruses employ a range of strategies to counteract the prokaryotic adaptive immune system, clustered regularly interspaced short palindromic repeats and CRISPR-associated proteins (CRISPR-Cas), including mutational escape and physical blocking of enzymatic function using anti-CRISPR proteins (Acrs). Acrs have been found in many bacteriophages but so far not in archaeal viruses, despite the near ubiquity of CRISPR-Cas systems in archaea. Here, we report the functional and structural characterization of two archaeal Acrs from the lytic rudiviruses, SIRV2 and SIRV3. We show that a 4 kb deletion in the SIRV2 genome dramatically reduces infectivity in Sulfolobus islandicus LAL14/1 that carries functional CRISPR-Cas subtypes I-A, I-D and III-B. Subsequent insertion of a single gene from SIRV3, gp02 (AcrID1), which is conserved in the deleted fragment, successfully restored infectivity. We demonstrate that AcrID1 protein inhibits the CRISPR-Cas subtype I-D system by interacting directly with Cas10d protein, which is required for the interference stage. Sequence and structural analysis of AcrID1 show that it belongs to a conserved family of compact, dimeric αβ-sandwich proteins characterized by extreme pH and temperature stability and a tendency to form protein fibres. We identify about 50 homologues of AcrID1 in four archaeal viral families demonstrating the broad distribution of this group of anti-CRISPR proteins.",

author = "Fei He and Yuvaraj Bhoobalan and Van, {Lan B.} and Kjeldsen, {Anders Lynge} and Matteo Dedola and Makarova, {Kira S.} and Koonin, {Eugene V.} and Brodersen, {Ditlev E.} and Xu Peng",

note = "Publisher Correction: Anti-CRISPR proteins encoded by archaeal lytic viruses inhibit subtype I-D immunity",

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doi = "10.1038/s41564-018-0120-z",

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T1 - Anti-CRISPR proteins encoded by archaeal lytic viruses inhibit subtype I-D immunity

AU - He, Fei

AU - Bhoobalan, Yuvaraj

AU - Van, Lan B.

AU - Kjeldsen, Anders Lynge

AU - Dedola, Matteo

AU - Makarova, Kira S.

AU - Koonin, Eugene V.

AU - Brodersen, Ditlev E.

AU - Peng, Xu

N1 - Publisher Correction: Anti-CRISPR proteins encoded by archaeal lytic viruses inhibit subtype I-D immunity

PY - 2018

Y1 - 2018

N2 - Viruses employ a range of strategies to counteract the prokaryotic adaptive immune system, clustered regularly interspaced short palindromic repeats and CRISPR-associated proteins (CRISPR-Cas), including mutational escape and physical blocking of enzymatic function using anti-CRISPR proteins (Acrs). Acrs have been found in many bacteriophages but so far not in archaeal viruses, despite the near ubiquity of CRISPR-Cas systems in archaea. Here, we report the functional and structural characterization of two archaeal Acrs from the lytic rudiviruses, SIRV2 and SIRV3. We show that a 4 kb deletion in the SIRV2 genome dramatically reduces infectivity in Sulfolobus islandicus LAL14/1 that carries functional CRISPR-Cas subtypes I-A, I-D and III-B. Subsequent insertion of a single gene from SIRV3, gp02 (AcrID1), which is conserved in the deleted fragment, successfully restored infectivity. We demonstrate that AcrID1 protein inhibits the CRISPR-Cas subtype I-D system by interacting directly with Cas10d protein, which is required for the interference stage. Sequence and structural analysis of AcrID1 show that it belongs to a conserved family of compact, dimeric αβ-sandwich proteins characterized by extreme pH and temperature stability and a tendency to form protein fibres. We identify about 50 homologues of AcrID1 in four archaeal viral families demonstrating the broad distribution of this group of anti-CRISPR proteins.

AB - Viruses employ a range of strategies to counteract the prokaryotic adaptive immune system, clustered regularly interspaced short palindromic repeats and CRISPR-associated proteins (CRISPR-Cas), including mutational escape and physical blocking of enzymatic function using anti-CRISPR proteins (Acrs). Acrs have been found in many bacteriophages but so far not in archaeal viruses, despite the near ubiquity of CRISPR-Cas systems in archaea. Here, we report the functional and structural characterization of two archaeal Acrs from the lytic rudiviruses, SIRV2 and SIRV3. We show that a 4 kb deletion in the SIRV2 genome dramatically reduces infectivity in Sulfolobus islandicus LAL14/1 that carries functional CRISPR-Cas subtypes I-A, I-D and III-B. Subsequent insertion of a single gene from SIRV3, gp02 (AcrID1), which is conserved in the deleted fragment, successfully restored infectivity. We demonstrate that AcrID1 protein inhibits the CRISPR-Cas subtype I-D system by interacting directly with Cas10d protein, which is required for the interference stage. Sequence and structural analysis of AcrID1 show that it belongs to a conserved family of compact, dimeric αβ-sandwich proteins characterized by extreme pH and temperature stability and a tendency to form protein fibres. We identify about 50 homologues of AcrID1 in four archaeal viral families demonstrating the broad distribution of this group of anti-CRISPR proteins.

UR - http://10.1038/s41564-018-0184-9

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DO - 10.1038/s41564-018-0120-z

M3 - Journal article

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SN - 2058-5276

VL - 3

SP - 461

EP - 469

JO - Nature Microbiology

JF - Nature Microbiology

IS - 4

ER -

Anti-CRISPR proteins encoded by archaeal lytic viruses inhibit subtype I-D immunity

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