Long-term genomic coevolution of host-parasite interaction in the natural environment

Abstract

The antagonistic coevolution of parasite infectivity and host resistance alters the biological functionality of species, with effects spanning to communities and ecosystems. Still, studies describing long-term host-parasite coevolutionary dynamics in nature are largely missing. Furthermore, the role of host resistance mechanisms for parasite evolution is poorly understood, necessitating for the molecular and phenotypic characterization of both coevolving parasites and their hosts. We combined long-term field sampling (2007-2014), in vitro cross-infections and time-shift experiments with bacteriophage whole genome sequencing and bacterial (Flavobacterium columnare) CRISPR (Clustered Regularly Interspaced Short Palindromic Repeats) profiling to show the molecular details of the phage-bacterium arms race in the environment. Bacteria were generally resistant to phages from the past and susceptible to phages in the future. The bacterial resistance selected for increased phage infectivity and host range, correlating directly with the expansion of phage genome size by 2656 bp. In the bacterial host, two CRISPR loci were identified: a type II-C locus and an RNA-targeting type VI-B locus. While maintaining a core set of conserved spacers, phage-matching spacers appeared in the variable end of both CRISPR loci over time. The appearance of these CRISPR spacers in the bacterial host often corresponded with arms race -manner molecular changes in the protospacers of the coevolving phage population. However, the phenotypic data indicated that the relative role of constitutive defence may be more important in high phage pressure, highlighting the importance of our findings for understanding microbial community ecology and in the development of phage therapy applications.