Do plasmid-dependent phages enable the survival of costly plasmids?

Plasmids benefit bacterial communities by storing auxiliary genes that address environmental challenges such as antibiotics. Subsequent plasmid loss can also be advantageous if plasmid benefits are temporary but costs are permanent. However, unless positive selection is sustained, plasmid loss can proceed to extinction, with access to plasmid-derived benefits permanently lost. In principle, horizontal transmission can maintain a plasmid in a population, but if the plasmid cost is too high, the host can become uncompetitive. We examine how survival of costly but occasionally beneficial plasmids is possible in a bacterial population. Using population models, we demonstrate that plasmid-dependent phages can, counterintuitively, solve this plasmid survival problem for their bacterial hosts. Phage predation pins the plasmid at low but nonzero abundance, such that the plasmid cost is effectively neutralized at the population level, dramatically lengthening the persistence time of the plasmid. When conditions change and the costly plasmid becomes beneficial, it spreads across the host population and switches to a vertical-transmission lifestyle until benefits again subside.