The highly diverse antiphage defence systems of bacteria

Georjon, Héloïse; Bernheim, Aude

doi:10.1038/s41579-023-00934-x

Cited by 131 publications

(94 citation statements)

References 142 publications

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“…Although we were able to characterize the molecular underpinnings of major features of the interaction network, we also note that more phenotypic and genomic variation exists which we have yet to explain, further highlighting the complexity that can evolve rapidly (i.e., within 100 to 200 generations). Although the molecular mechanisms identified in our flasks will differ across vastly different taxa and ecological communities ( 24 , 34 ), our work demonstrates how inherent coevolutionary processes can give rise to complex patterns that abound in natural ecosystems.…”

Section: Discussionmentioning

confidence: 93%

Rapid bacteria-phage coevolution drives the emergence of multiscale networks

Borin,

Lee,

Lucia-Sanz

et al. 2023

Science

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Interactions between species catalyze the evolution of multiscale ecological networks, including both nested and modular elements that regulate the function of diverse communities. One common assumption is that such complex pattern formation requires spatial isolation or long evolutionary timescales. We show that multiscale network structure can evolve rapidly under simple ecological conditions without spatial structure. In just 21 days of laboratory coevolution, Escherichia coli and bacteriophage Φ21 coevolve and diversify to form elaborate cross-infection networks. By measuring ~10,000 phage-bacteria infections and testing the genetic basis of interactions, we identify the mechanisms that create each component of the multiscale pattern. Our results demonstrate how multiscale networks evolve in parasite-host systems, illustrating Darwin’s idea that simple adaptive processes can generate entangled banks of ecological interactions.

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Section: Discussionmentioning

confidence: 93%

Rapid bacteria-phage coevolution drives the emergence of multiscale networks

Borin,

Lee,

Lucia-Sanz

et al. 2023

Science

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“…Phage and bacteria are engaged in a constant arms race leading to the evolution of a multitude of non-mutually exclusive antiphage defence mechanisms, including the well-understood phage receptor alteration, restriction-modification, abortive infection, CRISPR-Cas systems, as well as new defence systems 45,46 . It is well established that increased phage virulence selects for the evolution of host resistance if the costs associated with resistance are outweighed by the benefits of the capability to avoid infection 47,48 .…”

Section: Discussionmentioning

confidence: 99%

Phage-induced efflux down-regulation boosts antibiotic efficacy

Kraus,

Łapińska,

Chawla

et al. 2023

Preprint

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The interactions between a virus and its host vary in space and time and are affected by the presence of molecules that alter the physiology of either the host or the virus. Determining the dynamics of these interactions is paramount for predicting the fate of bacterial and phage populations and for designing rational phage-antibiotic therapies. We study the interactions between stationary phase Burkholderia thailandensis and the phage phi Bp-AMP1. Although heterogeneous genetic resistance to phage rapidly emerges in B. thailandensis, the presence of phage enhances the efficacy of three major antibiotic classes, the quinolones, the beta-lactams and the tetracyclines, but antagonizes tetrahydrofolate synthesis inhibitors. Enhanced antibiotic efficacy is underpinned by reduced antibiotic efflux in the presence of phage. This new phage-antibiotic therapy allows for eradication of stationary phase bacteria, whilst requiring reduced antibiotic concentrations, which is crucial for treating infections in sites where it is difficult to achieve high antibiotic concentrations.

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“…They regularly attack and predate on bacterial populations across different ecological settings with an estimated rate of infection per second in oceans alone on the order of 10 23 (Mushegian, 2020;Suttle, 2007). To counteract phages and other parasitic mobile elements, bacteria evolved a wide range of defence systems with various molecular mechanisms of action (Bernheim et al, 2021;Doron et al, 2018;Gao et al, 2020;Georjon & Bernheim, 2023;Millman et al, 2022). These include CRISPR-Cas systems, which provide adaptive immunity by storing information about past encounters with MGE (Makarova et al, 2020), restriction-modification (RM) systems that degrade foreign genetic material based on specific molecular patterns (Wilson, 1991), abortive infection mechanisms that limit the spread of phages in the bacterial population by inducing the suicide of infected cells (Lopatina et al, 2020), and multiple others.…”

Section: Introductionmentioning

confidence: 99%

Defence systems and horizontal gene transfer in bacteria

Kogay,

Wolf,

Koonin

2024

Environmental Microbiology

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Horizontal gene transfer (HGT) is a fundamental process in prokaryotic evolution, contributing significantly to diversification and adaptation. HGT is typically facilitated by mobile genetic elements (MGEs), such as conjugative plasmids and phages, which often impose fitness costs on their hosts. However, a considerable number of bacterial genes are involved in defence mechanisms that limit the propagation of MGEs, suggesting they may actively restrict HGT. In our study, we investigated whether defence systems limit HGT by examining the relationship between the HGT rate and the presence of 73 defence systems across 12 bacterial species. We discovered that only six defence systems, three of which were different CRISPR‐Cas subtypes, were associated with a reduced gene gain rate at the species evolution scale. Hosts of these defence systems tend to have a smaller pangenome size and fewer phage‐related genes compared to genomes without these systems. This suggests that these defence mechanisms inhibit HGT by limiting prophage integration. We hypothesize that the restriction of HGT by defence systems is species‐specific and depends on various ecological and genetic factors, including the burden of MGEs and the fitness effect of HGT in bacterial populations.

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The highly diverse antiphage defence systems of bacteria

Cited by 131 publications

References 142 publications

Rapid bacteria-phage coevolution drives the emergence of multiscale networks

Rapid bacteria-phage coevolution drives the emergence of multiscale networks

Phage-induced efflux down-regulation boosts antibiotic efficacy

Defence systems and horizontal gene transfer in bacteria

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