The Life Cycle Transitions of Temperate Phages: Regulating Factors and Potential Ecological Implications

Abstract

Phages are viruses that infect bacteria. They affect various microbe-mediated processes that drive biogeochemical cycling on a global scale. Their influence depends on whether the infection is lysogenic or lytic. Temperate phages have the potential to execute both infection types and thus frequently switch their infection modes in nature, potentially causing substantial impacts on the host-phage community and relevant biogeochemical cycling. Understanding the regulating factors and outcomes of temperate phage life cycle transition is thus fundamental for evaluating their ecological impacts. This review thus systematically summarizes the effects of various factors affecting temperate phage life cycle decisions in both culturable phage-host systems and natural environments. The review further elucidates the ecological implications of the life cycle transition of temperate phages with an emphasis on phage/host fitness, host-phage dynamics, microbe diversity and evolution, and biogeochemical cycles.

Keywords: ecological implication; life cycle transition; lysogeny; prophage induction; regulating factors; temperate phage.

Figure 1

The potential effects of various factors on temperate phage life cycle transition. In the initials of infection, the phage adsorbs to the host cell surface through interacting with host receptors and then injects its genome into the host. Thereafter, the temperate phage enters either the lytic production process or forms a stable coexistence with the host in the lysogenic cycle that is maintained by the repressor protein. Colored arrows indicate factors affecting phage life cycle transition and their potential targets of action. The green solid arrows indicate factors that possibly act on the repressor either directly or indirectly through activation of the host’s SOS response. The pink dashed arrows indicate factors, which are suggested to affect the physiological state of the hosts and thus influence phage life cycle transition, although their effects and underlying mechanisms remain largely unknown. The dark blue solid arrows indicate that salinity may influence the phage life cycle by affecting the phage’s adsorption and genome injection.

Figure 2

Potential ecological implications of lysogenic/lytic transition. (a) Potential ecological implications of lytic to lysogenic cycle transition. The transition protects free phages from various stresses such as solar radiation, grazing, and sinking by attaching to marine aggregates. Lysogeny also enhances bacterial fitness through lysogeny conversion, which averts immediate mortality and facilitates host adaptation to extreme environments. Moreover, lysogeny regulates the host’s genome arrangement and expression pattern through integration and excision of prophages. The red cross symbol represents that hosts are exempted from immediate phage-mediated lysis, while the ray and skull symbols represent the harsh environmental conditions. (b) Potential ecological implications of lysogenic to lytic cycle transition. Prophages entering the lytic cycle reprogram the host’s metabolism to favor phage replication, influence the bacterial community structure through phage-mediated host mortality, facilitate horizontal gene transfer, and drive the biogeochemical cycle.