Review
Special Issue: Microbial Endurance
Why Be Temperate: Lessons from Bacteriophage λ

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Bacteriophage λ is the archetypal temperate phage. The study of the genetic switch between lysis and lysogeny in λ led to a deep understanding of the molecular mechanisms underlying gene regulation in other organisms.

An understanding of the regulation of viral latency in λ offers unique opportunities to explore experimentally and theoretically the adaptive nature of fixed and plastic latency in different environments.

Understanding the evolution of lysogeny in λ can help to build up a comprehensive framework to study the evolution of latency in other infectious diseases, including many life-threatening human pathogens.

Many pathogens have evolved the ability to induce latent infections of their hosts. The bacteriophage λ is a classical model for exploring the regulation and the evolution of latency. Here, I review recent experimental studies on phage λ that identify specific conditions promoting the evolution of lysogenic life cycles. In addition, I present specific adaptations of phage λ that allow this virus to react plastically to variations in the environment and to reactivate its lytic life cycle. All of these different examples are discussed in the light of evolutionary epidemiology theory to disentangle the different evolutionary forces acting on temperate phages. Understanding phage λ adaptations yield important insights into the evolution of latency in other microbes, including several life-threatening human pathogens.

Section snippets

Phage Life Cycles

Some pathogens exploit their host for a very limited amount of time. In humans, for instance, most influenza virus infections last for less than 10 days [1]. The duration of the infection is generally limited by host immunity but it can also be reduced by the death of the infected host. In contrast, other pathogens can remain in their host for a very long time in a latent state. Many human viruses have adopted this alternative life history strategy. For instance, infections by herpes simplex

Latency as a Fixed Strategy

An understanding of the regulation of lysogeny in λ provides invaluable information on the evolution of latency in pathogens. When should pathogens adopt such latent life-history strategies? To answer this question, Berngruber et al. 18, 19 studied the competition between two λ variants with distinct life history strategies. The wild-type temperate λ has a high lysogenisation rate (ϕ  0.5) and a low induction rate (α  10−4). In contrast, the virulent λcI857 is a thermosensitive mutant with a low

Latency as a Plastic Strategy

In the above section, latency is assumed to be a fixed strategy. Bacteriophage λ, however, is also known to exhibit plastic life-history strategies. For instance, the efficacy of lysogenisation and the induction rate of the prophage can vary with the environment. These conditional strategies are well studied on a molecular level but the adaptive nature of this plasticity is often overlooked.

Concluding Remarks

The discovery and the characterization of bacteriophage λ has led to major discoveries in molecular biology [14]. In particular, the regulation of the lysis–lysogeny decision remains a very fruitful topic that stimulated a broad range of research studies 26, 37. The molecular details of the genetic switch of λ have been scrutinized for decades and led to a deep understanding of gene regulation that shed light on many other biological regulatory processes. The lysis–lysogeny decision has

Acknowledgments

This work benefited a lot from discussions with Thomas Berngruber, Marc Choisy, Troy Day, Bryan Grenfell, Quentin Legros, Bruce Levin, Sébastien Lion, Ana Rivero, and Joshua Weitz.

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