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

Clare Rollie (), Anne Chevallereau (), Bridget N. J. Watson, Te-yuan Chyou, Olivier Fradet, Isobel McLeod, Peter C. Fineran, Chris M. Brown, Sylvain Gandon and Edze R. Westra ()
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Clare Rollie: University of Exeter
Anne Chevallereau: University of Exeter
Bridget N. J. Watson: University of Exeter
Te-yuan Chyou: University of Otago
Olivier Fradet: University of Exeter
Isobel McLeod: University of Exeter
Peter C. Fineran: University of Otago
Chris M. Brown: University of Otago
Sylvain Gandon: CNRS, EPHE, IRD, Université Paul Valéry Montpellier 3
Edze R. Westra: University of Exeter

Nature, 2020, vol. 578, issue 7793, 149-153

Abstract: Abstract On infection of their host, temperate viruses that infect bacteria (bacteriophages; hereafter referred to as phages) enter either a lytic or a lysogenic cycle. The former results in lysis of bacterial cells and phage release (resulting in horizontal transmission), whereas lysogeny is characterized by the integration of the phage into the host genome, and dormancy (resulting in vertical transmission)1. Previous co-culture experiments using bacteria and mutants of temperate phages that are locked in the lytic cycle have shown that CRISPR–Cas systems can efficiently eliminate the invading phages2,3. Here we show that, when challenged with wild-type temperate phages (which can become lysogenic), type I CRISPR–Cas immune systems cannot eliminate the phages from the bacterial population. Furthermore, our data suggest that, in this context, CRISPR–Cas immune systems are maladaptive to the host, owing to the severe immunopathological effects that are brought about by imperfect matching of spacers to the integrated phage sequences (prophages). These fitness costs drive the loss of CRISPR–Cas from bacterial populations, unless the phage carries anti-CRISPR (acr) genes that suppress the immune system of the host. Using bioinformatics, we show that this imperfect targeting is likely to occur frequently in nature. These findings help to explain the patchy distribution of CRISPR–Cas immune systems within and between bacterial species, and highlight the strong selective benefits of phage-encoded acr genes for both the phage and the host under these circumstances.

Date: 2020
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DOI: 10.1038/s41586-020-1936-2

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