Host physiology-dependent lysis timing shapes bacteriophage competition under nutrient fluctuations

When bacteriophages infect starved host bacteria, the restrictive host physiology may lead to prolonged latent periods and/or reduced burst sizes, compared to infection of a fast-growing bacterium. Using a mathematical model, we explore a system of two types of virulent phages that have distinct host physiology dependencies and are infecting a shared bacterial host population. We consider different environmental regimes to test whether they can compete and coexist under fluctuating conditions, putting emphasis on phases with limited resources for bacterial growth. We find that the fitness of a phage that can modulate lysis timing in response to changes in the host physiology is elevated in fluctuating feast-famine environments compared to more stable environments, which favor rapid lysis with a reduced burst size. This effect is closely coupled to the increased mortality of free phages due to abortive adsorption to already infected host bacteria during starvation phases. We identify specific system dynamics that either support or suppress the propagation of the delayed lysis phage. This theoretical analysis highlights the competitive benefits and limitations of lysis delay as a phage propagation strategy. Our results underscore the importance of considering the bacterial physiology dependence of bacteriophage replication in order to correctly predict phage fitness and population dynamics in complex environments.IMPORTANCEBacteriophage replication depends strongly on the physiological state of the host, yet most ecological and theoretical studies treat phage life histories as fixed traits. This overlooks how nutrient limitation, starvation, and fluctuating growth conditions reshape infection outcomes. By examining competition between phages with different responses to host physiology, our work shows how environmentally driven changes in the latent period can alter which phages persist, spread, or are lost. These insights clarify when delayed lysis is a beneficial strategy and when it becomes a liability. More broadly, our results highlight the need to integrate host physiology into models of phage-host dynamics to better understand microbial ecosystems and to guide applications such as rational phage therapy design.