Ecological Constraints Restrict the Benefits of Horizontally Acquired CRISPR-Cas Systems

Acquiring a new defence system that can offer adaptive immunity against invading genetic elements (such as bacteriophage/phage) would be intuitively assumed to offer an evolutionary advantage to the host. Indeed, the ‘pan-immune model’ has proposed that possession of particular defence systems may be in a continual state of flux in microbial populations: allowing a reservoir of immune potential to be available without any single cell or strain having to carry them and bear the associated fitness costs. Furthermore, phage defence systems have been frequently associated with the hallmarks of horizontal gene transfer. Studies into adaptive-immunity-like CRISPR-Cas systems have supported the pan-immune model, with bioinformatic and experimental evidence for the frequent gain and loss of these systems. However, what is less well understood is the strength and potential conditional requirements to the evolutionary advantages offered to a host by a recently horizontally acquired CRISPR-Cas system. We experimentally modelled this ecological scenario by transferring the type I-F CRISPR-Cas system which is native to Pseudomonas aeruginosa to the naïve host Pseudomonas fluorescens. Although the CRISPR-Cas system is fully functional in the new host, protection against phage lysis is highly dependent on phage species and environment, and spacer acquisition against phage occurs at low frequency. This work shows that the ecological reality of successful selection after horizontal gene transfer events is nuanced. Therefore the limiting factor to successful sharing of defence systems in microbial populations might not only be rates of horizontal gene transfer, but also encountering ‘sweet spots’ of environmental conditions to produce robust selective benefits for hosts with the new defence system.