Chapter 3-1 Microbial Arms Race

Bacteriophages (referred to hereafter as phages) and their bacterial hosts coexist in natural and man-made environments, seemingly working towards an endless state of co-evolutionary equilibrium. It has been esti- mated that in most environments, phages outnumber their bacterial hosts by approximately tenfold 1 . Thus, bacteria have either evolved or acquired through lateral transfer a remarkable array of mechanisms to protect themselves against many phage invaders 2 . Bacterial antiphag e systems include the inhibition of phage attach- ment to cell surface receptors, cleavage of the invading phage genome and even the induction of an altruistic cell suicide to abort phage infection. However , despite this arsenal, a large proportion of bacteria succumb to phage infection. Owing to their genomic plasticity and rapid multiplication rates, phages have evolved equally diver- sified strategies to thrive in apparently well-protected bacterial cells. These strategies include mechanisms such as point mutations in specific genes, genome rearrange- ments, and genomic exchange with other viral or microbial genomes to acquire new traits (TABLE 1). Understanding the complex dynamics of phage–host interactions is of interest for several reasons. In the food and biotechnology industries, which rely on phage- resistan t bacteria to manufacture specialized products, it is necessary to monitor the emerging phage population to maximize product yield and quality. Furthermore, renewed interest in phage therapy and the use of phages as biocontrol agents requires a b etter understanding of phage–bacterium co-evolution in order to predict and thereby limit the undesired selection of phage- resistant bacteria. Because phages have crucial roles in environmental processes, such as in the structuring of microbial communities involved in biogeochemical cycling 3 , research on the interactions of phages with their bacterial hosts is necessary to understand their environmental impact. In the past few years, our appreciation of the remarkable ability of phages to adapt to bacterial defence systems has grown enormously. This adaptability has manifested in several active forms, such as the e vasion of bacterial CRISPR–Cas (clustered regularly interspaced short palindromic repeats–CRISPR-associated proteins) immunity using anti-CRISPR proteins, and the hijacking of host antitoxins to prevent abortive infection (TABLE 1). In this Review, we discuss the passive and active strategies used by phages to overcome bacterial resistance mechanisms, and we consider how these strategies are influenced by co-evolution. Access to host receptors To efficiently attach to the surface of its bacterial host (a process known as adsorption), a phage targets cell surface receptors. Given that adsorption is often intricately coupled to the ejection of phage DNA, and that both of these interdependent steps must be achieved to enable intracellular phage replication, the specific interaction between the phage receptor-binding protein (RBP) and its bacterial cell surface receptor is one of the primary parameters defining phage infection kinetics 4,5 . Bacterial receptors belong to various biochemical families and are mainly represented by surface proteins, polysaccharides and lipopolysaccharides (LPSs) 6 . In addition to the presence of these receptors, their Phage therapy The use of phages as therapeutic agents to treat or prevent bacterial infection. Receptor-binding protein A phage protein that is located at the tip of the phage tail and specifically recognizes its cognate receptor on the bacterial surface. Rev enge of the phages: defeating bacterial defences Julie E. Samson, Alf onso H. Magadán, Mour ad Sabri and Sylvain Moineau Abstract | Bacteria and their viral predators (bacteriophages) are locked in a constant battle. In order to proliferate in phage-rich environments, bacteria have an impressive arsenal of defence mechanisms, and in response, phages have evolved counter-strategies to evade these antiviral systems. In this Review, we describe the various tactics that are used by phages to overcome bacterial resistance mechanisms, including adsorption inhibition, restriction–modification, CRISPR–Cas (clustered regularly interspaced short palindromic repeats–CRISPR-associated proteins) systems and abortive infection. Furthermore, we consider how these observations have enhanced our knowledge of phage biology, evolution and phage–host interactions. Département de Biochimie, Microbiologie et Bio-informatique, Faculté des Sciences et de Génie, Groupe de Recherche en Écologie Buccale, Faculté de Médecine Dentaire, Félix d’Hérelle Reference Center for Bacterial Viruses, Université Laval, Québec City, Québec G1V 0A6, Canada. Corresponden ce to S.M. e-mail: Sylvain.Moineau@ bcm.ulaval.ca doi:10.1038/nrmicro3096 Published online 27 August 2013 REVIEWS NATURE REVIEWS | MICROBIOLOGY VOLUME 11 | OCTOBER 2013 | 675 © 2013 Macmillan Publishers Limited. All rights reserved

Chapter 3-1 Microbial Arms Race

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