Anti-CRISPR Phages Cooperate to Overcome CRISPR-Cas Immunity

Landsberger, Mariann; Gandon, Sylvain; Meaden, Sean; Rollie, Clare; Chevallereau, Anne; Chabas, Hélène; Buckling, Angus; Westra, Edze R.; Houte, Stineke van

doi:10.1016/j.cell.2018.05.058

Cited by 199 publications

(165 citation statements)

References 70 publications

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“…Anti-CRISPRs, the next innovation in counter adaption between phages and bacteria encoding CRISPR-Cas systems targeting those phages, were shown to work in a phage-concentration dependent manner. In short, anti-CRISPRs from a single phage may not necessarily be enough to overcome host defenses, however, if the environment is full of free phages, subsequent phages benefit from the anti-CRISPRs expended in the attempts at infection by previous phages (65,66). In a similar measurement of microbial populations in an environment, it was recently uncovered that phages can 'listen in' on host quorum sensing to influence the decision between lysogeny and lysis depending on the density of host bacteria (67).…”

Section: Discussionmentioning

confidence: 99%

DominantVibrio choleraephage exhibits lysis inhibition sensitive to disruption by a defensive phage satellite

Hays

Seed

2019

Preprint

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AbstractBacteriophages and their bacterial hosts are locked in a dynamic evolutionary arms race. Phage satellites, selfish genomic islands which exploit both host bacterium and target phage, further complicate the evolutionary fray. One such tripartite system involves the etiological agent of the diarrheal disease cholera – Vibrio cholerae, the predominant phage isolated from cholera patients – ICP1, and a phage satellite – PLE. When ICP1 infects V. cholerae harboring the integrated PLE genome, PLE accelerates host lysis, spreading the PLE while completely blocking phage production protecting V. cholerae at the population level. Here we identify a single PLE gene, lidI, sufficient to mediate accelerated lysis during ICP1 infection and demonstrate that LidI functions through disrupting lysis inhibition – an understudied outcome of phage infection when phages vastly outnumber their hosts. This work identifies ICP1-encoded holin and antiholin genes teaA and arrA respectively, that mediate this first example of lysis inhibition outside the T-even coliphages. Through lysis inhibition disruption, LidI is sufficient to limit the number of progeny phage produced from an infection. Consequently, this disruption bottlenecks ICP1 evolution as probed by recombination and CRISPR-Cas targeting assays. These studies link novel characterization of the classic phenomenon of lysis inhibition with a conserved protein in a dominant phage satellite, highlighting the importance of lysis timing during infection and parasitization, as well as providing insight into the populations, relationships, and evolution of bacteria, phages, and phage satellites in nature.ImportanceWith increasing awareness of microbiota impacting human health comes intensified examination of, not only bacteria and the bacteriophages that prey upon them, but also the mobile genetic elements (MGEs) that mediate interactions between them. Research is unveiling evolutionary strategies dependent on sensing the milieu: quorum sensing impacts phage infection, phage teamwork overcomes bacterial defenses, and abortive infections sacrifice single cells protecting populations. Yet, the first discovered environmental sensing by phages, known as lysis inhibition (LIN), has only been studied in the limited context of T-even coliphages. Here we characterize LIN in the etiological agent of the diarrheal disease cholera, Vibrio cholerae, infected by a phage ubiquitous in clinical samples. Further, we show that a specific MGE, the phage satellite PLE, collapses LIN with a conserved protein during its anti-phage program. The insights gleaned from this work add to our expanding understanding of microbial fitness in natural contexts beyond the canonical bacterial genome and into the realm of antagonistic evolution driven by phages and satellites.

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Section: Discussionmentioning

confidence: 99%

DominantVibrio choleraephage exhibits lysis inhibition sensitive to disruption by a defensive phage satellite

Hays

Seed

2019

Preprint

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“…Bacteriophages (phages) have evolved numerous mechanisms to subvert CRISPR defense [49][50][51] . Several temperate phages of P. aeruginosa encode small proteins that bind and neutralize type I-F Cas proteins 22,24,[51][52][53][54][55][56][57][58] . One of these anti-CRISPR proteins (AcrIF3) binds Cas2/3 and prevents its recruitment to the Csy complex 20,52,54,55 .…”

Section: Anti-crispr Acrif3 Is a Molecular Mimicmentioning

confidence: 99%

Structure reveals mechanism of CRISPR RNA-guided nuclease recruitment and anti-CRISPR viral mimicry

Rollins

Chowdhury

Golden

et al. 2018

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“…Recent studies show that viruses maintain anti-CRISPR proteins that target (sometimes incompletely) CRISPR activity [58,59]. At the virus population level, viruses can "cooperate" in a way that initial infections block the hosts' CRISPR systems, facilitating subsequent infections, which can result in phage epidemics [60]. The demonstration of significant weighted nestedness in the empirical networks suggests that coevolution involving CRISPR-induced immunity is at play in natural microbial populations.…”

Section: Discussionmentioning

confidence: 99%

The network structure and eco-evolutionary dynamics of CRISPR-induced immune diversification

Pilosof

Alcalá-Corona

Wang

et al. 2019

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As a heritable sequence-specific adaptive immune system, CRISPR-Cas is a powerful force shaping strain diversity in host-virus systems. While the diversity of CRISPR alleles has been explored, the associated structure and dynamics of host-virus interactions has not. We develop theory on the role of CRISPR immunity in mediating the interplay between host-virus interaction structure and eco-evolutionary dynamics in a computational model and three natural systems. We show that the structures of networks describing who infects whom and who is protected from whom are modular and weighted-nested, respectively. The dynamic interplay between these networks influences transitions between dynamical regimes of virus diversification and host control,leading to eventual virus extinction. The three empirical systems exhibit weighted nestedness, a pattern our theory shows is indicative of viral control by hosts. Previously missing from studies of microbial host-pathogen systems, the protection network plays a key role in the coevolutionary dynamics. IntroductionThe structure of complex ecological communities is clearly non-random. It is generally argued that interaction structure affects the stability of communities to perturbations [1-3] and arises from coevolutionary dynamics between interacting partners [4][5][6][7], yet the structure-dynamics nexus remains a long-standing central question in community and network ecology. Host-parasite infection networks, in which interaction structure represents 'who infects whom', have been typically described as modular, nested, or both [8,9]. Modularity concerns patterns of specificity, in which the network is partitioned into modules of hosts and parasites that interact densely with each other but sparsely with those outside the group. Nestedness concerns instead patterns of specialization, and describes a network structure in which specialist hosts are infected by subsets of parasites that in turn also infect the more generalist hosts [8,9].Common to all host-parasite network studies is a dominant focus on patterns of infection. Infection structure should critically depend however on the genetic basis of resistance of hosts to pathogens [10]. The emergence of network structure from immune selection has been shown in pathogens of humans such as Plasmodium falciparum [11, 12]. In particular, strain theory developed for pathogens with multilocus encoding of antigens posits that negative frequency dependent selection, mediated by competition for hosts through cross-immunity, can structure pathogen populations into clusters of strains with limited overlap of antigenic repertoires [11][12][13][14][15]. Parasites with 2 . CC-BY-NC-ND 4.0 International license is made available under a resistance by surface mutation can arise quickly to take over CRISPR or restriction-modification systems in providing immunity. This experimental and theoretical evidence for advantages of surface modification may entail strong fitness costs under natural conditions because mutations in surface receptors such a...

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Anti-CRISPR Phages Cooperate to Overcome CRISPR-Cas Immunity

Cited by 199 publications

References 70 publications

DominantVibrio choleraephage exhibits lysis inhibition sensitive to disruption by a defensive phage satellite

DominantVibrio choleraephage exhibits lysis inhibition sensitive to disruption by a defensive phage satellite

Structure reveals mechanism of CRISPR RNA-guided nuclease recruitment and anti-CRISPR viral mimicry

The network structure and eco-evolutionary dynamics of CRISPR-induced immune diversification

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