Abstract

The canonical lytic-lysogenic binary has been challenged in recent years, as more evidence has emerged on alternative bacteriophage infection strategies. These infection modes are little studied, and yet they appear to be more abundant and ubiquitous in nature than previously recognized, and can play a significant role in the ecology and evolution of their bacterial hosts. In this review, we discuss the extent, causes and consequences of alternative phage lifestyles, and clarify conceptual and terminological confusion to facilitate research progress. We propose distinct definitions for the terms 'pseudolysogeny' and 'productive or non-productive chronic infection', and distinguish them from the carrier state life cycle, which describes a population-level phenomenon. Our review also finds that phages may change their infection modes in response to environmental conditions or the physiological state of the host cell. We outline known molecular mechanisms underlying the alternative phage-host interactions, including specific genetic pathways and their considerable biotechnological potential. Moreover, we discuss potential implications of the alternative phage lifestyles for microbial biology and ecosystem functioning, as well as applied topics such as phage therapy.

Highlights

  • Viruses infecting bacteria are the most abundant biological entities on Earth and play a critical role in the ecology and evolution of their bacterial hosts

  • The canonical lytic–lysogenic binary has been challenged in recent years, as more evidence has emerged on alternative bacteriophage infection strategies

  • Pseudolysogeny, carrier state and chronic infection are the most documented alternative infection types and have been observed among different phage groups. Such phage infections have been identified in divergent environments and in a relatively broad range of bacterial hosts representing gram-negative [1,2,3,4], grampositive [5] and cell wall-less bacteria [6], showing that alternative infection strategies are not limited to a particular group of bacteria or phages

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Summary

Introduction

Viruses infecting bacteria (bacteriophages or phages) are the most abundant biological entities on Earth and play a critical role in the ecology and evolution of their bacterial hosts. Pseudolysogeny, carrier state and chronic infection are the most documented alternative infection types and have been observed among different phage groups. Such phage infections have been identified in divergent environments and in a relatively broad range of bacterial hosts representing gram-negative [1,2,3,4], grampositive [5] and cell wall-less bacteria [6], showing that alternative infection strategies are not limited to a particular group of bacteria or phages. Growing evidence indicates that some phages may establish different alternative infection modes; the ‘selection’ of a particular infection strategy at any given time may be determined by, for example, the bacterial strain [7], host physiological state and/or environmental conditions [1,8,9,10].

A brief history of research on alternative phage infection strategies
Lytic and lysogenic life cycles
Pseudolysogeny
Carrier state life cycle—a populationlevel phenomenon
Technical challenges in studying alternative phage infection strategies
Evolutionary and ecological consequences
Frequency and dynamics in nature
Replication strategies differ between filamentous phages
Genetic programs maintaining the pseudolysogeny
Pseudolysogeny arising from starvation-induced entry arrest
Carrier state-induced changes in host phenotype
Biotechnological and therapeutic considerations
10. Conclusion and future perspectives
61. Secor PR et al 2020 Pf bacteriophage and
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