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

Abstract

Plasmids store auxiliary genes that address environmental challenges such as antibiotics. In the short term, plasmid loss can be advantageous to hosts if plasmid benefits are temporary but costs are permanent. However, this loss can proceed to plasmid extinction, with access to plasmid-derived benefits permanently lost. We consider a worst-case scenario: a plasmid that yields benefits only infrequently, imposes heavy costs that cannot be alleviated, and whose host population faces a competitor that cannot acquire the costly plasmid. Thus, horizontal transmission of this plasmid is detrimental to the host population when the plasmid does not provide benefits. Using population models, we demonstrate that -- counterintuitively -- plasmid-dependent phages can enable high-cost plasmid survival. Phage predation pins the plasmid at low abundance, effectively neutralizing the plasmid cost at the population level and boosting persistence time. When the costly plasmid becomes beneficial, it spreads and survives by vertical transmission until benefits subside.