Black box of phage–bacterium interactions: exploring alternative phage infection strategies

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.

New Microviridae isolated from Sulfitobacter reveals two cosmopolitan subfamilies of ssDNA phages infecting marine and terrestrial Alphaproteobacteria

“…Phage infections are usually described in terms of lytic, lysogenic, or chronic lifestyles. Alternative lifestyles, such as pseudolysogeny or carrier state have been observed among different phage groups, although their definition is not always consistent and the two terms have been used interchangeably (reviewed in (Mäntynen et al 2021)). The same phage can exhibit different lifestyles on the same host.…”

Deploying Viruses against Phytobacteria: Potential Use of Phage Cocktails as a Multifaceted Approach to Combat Resistant Bacterial Plant Pathogens

“…Plant pathogenic bacteria undergo enormous evolutionary pressure from phages. To cope with this pressure, bacteria have evolved with diversified immune mechanisms, including innate and adaptive, which evade the phage infection through a variety of phage resistance actions (Figure 3) [96,142,196,[223][224][225][226][227][228]. For the identification and characterization of the anti-phage underlying mechanisms, newly discovered CRISPR-Cas and RM systems have been established.…”

“…Plant phage cocktails have been explored as promising biocontrol therapeutics for the management of overwhelming bacterial diseases in plants without intimidating fauna and flora, and for the investigation of evolutionary interactions between phage and resistant phytobacteria, as highlighted in this communication. There are diversified mechanisms of phage resistance in bacterial pathogens and emerging strategies that phages employ to evade these systems for successful infections [59,196,227,229]. This knowledge is facilitating synthetic biology in the development of multidimensional phage-mediated therapeutics and novel biotechnological platforms.…”

PhageLeads: Rapid Assessment of Phage Therapeutic Suitability Using an Ensemble Machine Learning Approach

“…For condition (i), the determination of the presence of temperate markers in the phages ensures the exclusion of non-strictly lytic phages from being used in phage therapy. The mechanism of action of phage on a bacterial host depends on the life cycle of the phage, which can be classified into lytic, temperate, chronic, and pseudolysogenic cycles [14,15]. Out of these four lifestyles, lytic phages are considered as the most suitable candidates for phage therapy due to their rapid bactericidal effect.…”