Targeting of temperate phages drives loss of type I CRISPR–Cas systems

Rollie, Clare; Chevallereau, Anne; Watson, Bridget N. J.; Chyou, Te‐yuan; Fradet, Olivier; McLeod, Isobel; Fineran, Peter C.; Brown, C. M.; Gandon, Sylvain; Westra, Edze R.

doi:10.1038/s41586-020-1936-2

Cited by 82 publications

(93 citation statements)

References 35 publications

(57 reference statements)

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“…For each host defense system microbes have evolved, however, viruses appear to have developed a countermeasure, such as the anti-restriction, anti-CRISPR and anti-toxin systems (Dolgin, 2019;Rollie et al, 2020). While these viral countermeasure systems have been largely described for genera not normally found in the rumen, for example, Pseudomonas and Mycobacterium (Dedrick et al, 2017;Landsberger et al, 2018).…”

Section: Maintenance Of Microbial Diversitymentioning

confidence: 99%

Rumen Virus Populations: Technological Advances Enhancing Current Understanding

et al. 2020

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The rumen contains a multi-kingdom, commensal microbiome, including protozoa, bacteria, archaea, fungi and viruses, which enables ruminant herbivores to ferment and utilize plant feedstuffs that would be otherwise indigestible. Within the rumen, virus populations are diverse and highly abundant, often outnumbering the microbial populations that they both predate on and co-exist with. To date the research effort devoted to understanding rumen-associated viral populations has been considerably less than that given to the other microbial populations, yet their contribution to maintaining microbial population balance, intra-ruminal microbial lysis, fiber breakdown, nutrient cycling and genetic transfer may be highly significant. This review follows the technological advances which have contributed to our current understanding of rumen viruses and drawing on knowledge from other environmental and animal-associated microbiomes, describes the known and potential roles and impacts viruses have on rumen function and speculates on the future directions of rumen viral research.

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Section: Maintenance Of Microbial Diversitymentioning

confidence: 99%

Rumen Virus Populations: Technological Advances Enhancing Current Understanding

et al. 2020

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“…It has been suggested that following the integration of an STS, the CRISPR-Cas system must become inactivated in order to survive, and that this phenomenon could explain the abundance of highly degraded CRISPR systems that contain cas pseudogenes (12). Recent experimental evolution studies have shown that large genomic deletions encompassing the entire CRISPR-Cas locus can occur as a consequence of auto-immunity to prophages (35).…”

Section: Self-targeting Spacers (Sts) Are Often Found In Crispr-encodmentioning

confidence: 99%

Prophages are associated with extensive CRISPR-Cas auto-immunity

Nóbrega

Walinga

Dutilh

et al. 2020

Preprint

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CRISPR-Cas systems require discriminating self from non-self DNA during adaptation and interference. Yet, multiple cases have been reported of bacteria containing self-targeting spacers (STS), i.e. CRISPR spacers targeting protospacers on the same genome. STS may reflect potential auto-immunity as an unwanted side effect of CRISPR-Cas defense, or a gene regulatory mechanism. Here we investigated the incidence, distribution, and evasion of STS in over 100,000 bacterial genomes. We found STS in all CRISPR-Cas types and in one fifth of all CRISPR-carrying bacteria. Notably, up to 40% of I-B and I-F CRISPR-Cas systems contained STS. We observed that STS-containing genomes almost always carry a prophage and that STS map to prophage regions in more than half of the cases. Despite carrying STS, genetic deterioration of CRISPR-Cas systems appears to be rare, suggesting a level of tolerance to STS by other mechanisms such as anti-CRISPR proteins and target mutations. We propose a scenario where it is common and perhaps beneficial to acquire an STS against a prophage, and this may trigger more extensive STS buildup by primed spacer acquisition in type I systems, without detrimental autoimmunity effects. The mechanisms of auto-immunity evasion create tolerance to STS-targeted prophages, and contribute both to viral dissemination and bacterial diversification.

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“…Bacteria that express acrs can tolerate "self-targeting" spacers that, in the absence of CRISPR-Cas inhibition, would otherwise cause lethal genomic cleavage (Bondy-Denomy et al, 2013;Vercoe et al, 2013;Xu et al, 2019;Rollie et al, 2020). The presence of these selftargeting spacers can therefore be used to identify bacterial genomes that likely encode anti-CRISPR proteins capable of inhibiting their endogenous CRISPR system (Rauch et al, 2017;Marino et al, 2018;Watters et al, 2018Watters et al, , 2020.…”

Section: Resultsmentioning

confidence: 99%

Discovery of multiple anti-CRISPRs uncovers anti-defense gene clustering in mobile genetic elements

Pinilla‐Redondo

Shehreen

Marino

et al. 2020

Preprint

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Many prokaryotes employ CRISPR-Cas systems to combat invading mobile genetic elements (MGEs). In response, some MGEs have evolved Anti-CRISPR (Acr) proteins to bypass this immunity, yet the diversity, distribution and spectrum of activity of this immune evasion strategy remain largely unknown. Here, we uncover 11 new type I anti-CRISPR genes encoded on numerous chromosomal and extrachromosomal mobile genetic elements within Enterobacteriaceae and Pseudomonas. Candidate genes were identified adjacent to anti-CRISPR associated gene 5 (aca5) and assayed against a panel of six type I systems: I-F (Pseudomonas, Pectobacterium, and Serratia), I-E (Pseudomonas and Serratia), and I-C (Pseudomonas), revealing the type I-F and/or I-E acr genes and a new aca (aca9). We find that acr genes not only associate with other acr genes, but also with inhibitors of distinct bacterial defense systems. These genomic regions appear to be "anti-defense islands", reminiscent of the clustered arrangement of "defense islands" in prokaryotic genomes. Our findings expand on the diversity of CRISPR-Cas inhibitors and reveal the potential exploitation of acr loci neighborhoods for identifying new anti-defense systems.

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Targeting of temperate phages drives loss of type I CRISPR–Cas systems

Cited by 82 publications

References 35 publications

Rumen Virus Populations: Technological Advances Enhancing Current Understanding

Rumen Virus Populations: Technological Advances Enhancing Current Understanding

Prophages are associated with extensive CRISPR-Cas auto-immunity

Discovery of multiple anti-CRISPRs uncovers anti-defense gene clustering in mobile genetic elements

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