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Summary

The current consensus concerning the prevalence of lytic and lysogenic phage life cycles in aquatic systems is that the host physiological state may influence viral strategies, lysogeny being favoured when hosts have reduced metabolic rates. We explored this hypothesis, by following phage cycle dynamics, host physiological state and metabolic activity over an annual cycle in three lakes subjected to strong seasonal fluctuations, including 4–5 months of ice cover. We observed marked seasonal dynamics of viral and bacterial communities, with low bulk and cell-specific bacterial metabolism in winter, and a dramatic increase in injured bacteria under the ice cover in all lakes. This period was accompanied by contrasting patterns in the proportion of lysogenic cells. In the eutrophic lake, times of low bacterial metabolic rates and high proportion of damaged cells corresponded to highest levels of lysogeny, supporting the notion that hosts are a ‘refuge’ for viruses. In the two unproductive lakes, peaks of injured cells corresponded to a minimum of lysogeny, suggesting an ‘abandon the sinking ship’ response, where the prophage replicates before the loss of genome. We suggest that these diverging responses to the host physiological state are not contradictory, but rather that there may be thresholds of cell stress and metabolic activity leading to one or the other response.