Frequency of mispackaging of Prochlorococcus DNA by cyanophage

Prochlorococcus cells are the numerically dominant phototrophs in the open ocean. Cyanophages that infect them are a notable fraction of the total viral population in the euphotic zone, and, as vehicles of horizontal gene transfer, appear to drive their evolution. Here we examine the propensity of three cyanophages—a podovirus, a siphovirus, and a myovirus—to mispackage host DNA in their capsids while infecting Prochlorococcus, the first step in phage-mediated horizontal gene transfer. We find the mispackaging frequencies are distinctly different among the three phages. Myoviruses mispackage host DNA at low and seemingly fixed frequencies, while podo- and siphoviruses vary in their mispackaging frequencies by orders of magnitude depending on growth light intensity. We link this difference to the concentration of intracellular reactive oxygen species and protein synthesis rates, both parameters increasing in response to higher light intensity. Based on our findings, we propose a model of mispackaging frequency determined by the imbalance between the production of capsids and the number of phage genome copies during infection: when protein synthesis rate increase to levels that the phage cannot regulate, they lead to an accumulation of empty capsids, in turn triggering more frequent host DNA mispackaging errors.