The influence of prokaryotic physiology and environmental factors on viral replication cycles (lytic and lysogeny) was investigated using seasonal in situ and experimental approaches, based on samples collected in the mixolimnion of the oligotrophic Lake Pavin, France. In natural prokaryotic communities, the seasonal dynamics of the physiology of prokaryotic communities, inferred from nucleic acid cell content, was strongly governed by the availability of resources (nutrients). The ratio of abundance between cells with high (HNA) and with low (LNA) nucleic acid contents shifted significantly from 1.2 in spring to 0.4 in summer. In contrast, the fraction of inducible lysogenic prokaryotes increased in summer, when a strong nutrients limitation occurred. In accordance, we performed microcosm experiments from samples collected during clear-water phase when nutrients were at their lowest levels in Lake Pavin. By manipulating nutrient concentrations and temperature, we reached the conclusions that (i) the variability of the physiological states of prokaryotic hosts was crucial for the establishment of lysogeny in viral communities, and (ii) lysogeny was favored when the community of prokaryotes faced strong “adaptative physiological transition phases” between survival and exponential growth states, in responses to abiotic changes. These results have raised questions and concerns about intrinsic metabolic effectors in prokaryotes that would be behind those physiological events observed at the community level. Metabolomic analyses allowed distinguishing characteristic métabolomes according to the “physiological” composition of prokaryotic host communities (i.e. HNA-cells dominant, same proportions of HNA- and LNA-cells, and LNA-cells dominant). Discriminant metabolites within metabolomic profiles characteristics of contrasted cell physiological states are discussed, in relation to putative metabolic signals for lysogeny promotion. Overall, we defend the idea that changes in prokaryote physiology are critical for the promotion and establishment of lysogeny within phage community in aquatic ecosystems, which are prone to environmental fluctuations.