Evolutionarily Stable Coevolution Between a Plastic Lytic Virus and Its Microbial Host

Abstract

Hosts influence and are influenced by viral replication. Cell size, for example, is a fundamental trait for microbial hosts that can not only alter the probability of viral adsorption, but also constrain the host physiological processes that the virus relies on to replicate. This intrinsic connection can affect the fitness of both host and virus, and therefore their mutual evolution. Here, we study the coevolution of bacterial hosts and their viruses by considering the dependence of viral performance on the host physiological state (viral plasticity). To this end, we modified a standard host-lytic phage model to include viral plasticity, and compared the coevolutionary strategies emerging under different scenarios, including cases in which only the virus or the host evolve. For all cases, we also obtained the evolutionary prediction of the traditional version of the model, which assumes a non-plastic virus. Our results reveal that the presence of the virus leads to an increase in host size and growth rate in the long term, which benefits both interacting populations. Our results also show that viral plasticity and evolution influence the classic host quality-quantity trade-off. Poor nutrient environments lead to abundant low-quality hosts, which tends to increase viral infection time. Conversely, richer nutrient environments lead to fewer but high-quality hosts, which decrease viral infection time. Our results can contribute to advancing our understanding of the microbial response to changing environments. For instance, both cell size and viral-induced mortality are essential factors that determine the structure and dynamics of the marine microbial community, and therefore our study can improve predictions of how marine ecosystems respond to environmental change. Our study can also help devise more reliable strategies to use phage to, for example, fight bacterial infections.

Unconstrained coevolution of bacterial size and the latent period of plastic phage

“…The population of uninfected hosts increases thanks to the uptake of the most limiting nutrient (here, glucose; first term, Eq (1) ), declines due to infection (second term) or dilution from the chemostat (last term). Similarly to [ 14 ], we consider here potential competition for space, light, or other resources not explicitly modeled that can affect negatively the growth of the focal population (third term), a plausible scenario as the framework introduces in ecological time new host mutants (see below); here, C all represents all hosts from all phenotypes in the system. The population of infected individuals increases due to infection (first term, Eq (2) ), and declines when infected cells are diluted (third term) or lysed (second term).…”

“…Cells lysed at time t produce the new batch of viruses (first term of Eq (3) ), and the population declines as viruses infect new hosts (second term), decay (become non-infective after a period of time, fourth term), or are diluted from the chemostat (last term). We expanded the model from [ 14 ] to include also the possibility for phage to avoid superinfection, thus accounting for the battery of mechanisms that a phage that has entered the host can deploy to prevent any other virus from using the same host for replication [ 29 ]; this mechanism, here implemented with a density-dependent term (third term, where V all represents the sum of all viral density across phenotypes), is not only more realistic but also reduces the mathematical instability reported in [ 13 , 14 ]. Finally, the dynamics of the most limiting nutrient (glucose) include the inflow and dilution of nutrient that characterize the chemostat environment (first and second terms), and the uptake of the nutrient by the uninfected hosts (last term).…”

“…Here, we set a threshold of 1 ind ⋅ l −1 for either population. Differently from [ 14 ], we consider that the threshold for the virus includes not only free viruses but also replicating viruses (i.e. viruses that are currently infecting a host), which prevents the elimination of viral mutant populations that entered the system recently and are still inside infected cells as part of their first lytic cycle.…”

“…In spite of the importance of viral plasticity, only recently have theories started to take it into account when exploring host-virus dynamics from an ecological [ 11 – 13 ] or an evolutionary perspective [ 11 , 14 , 15 ].…”

“…From an ecological point of view, considering viral plasticity leads to the counterintuitive result that lower nutrient conditions are somewhat beneficial for the host, as the consequent deterioration in physiological state is compensated by the associated decrease in viral performance and reduced viral pressure [ 11 ]. From an evolutionary point of view, we recently explored how viral plasticity affects the coevolution of host size and viral latent period [ 14 ]. Our results, restricted to evolutionarily stable states in which both host and virus coexist, showed that such coevolution leads to a negative correlation between host size and viral latent period.…”