Long-run bacteria-phage coexistence dynamics under natural habitat conditions in an environmental biotechnology system

Bacterial viruses are widespread and abundant across natural and engineered habitats. They influence ecosystem functioning through interactions with their hosts. Laboratory studies of phage-host pairs have advanced our understanding of phenotypic and genetic diversification in bacteria and phages. However, the dynamics of phage-host interactions have been seldom recorded in complex natural environments. We conducted an observational metagenomic study of the dynamics of interaction betweenGordoniaand their phages using a three-year data series of samples collected from a full-scale wastewater treatment plant. The aim was to obtain a comprehensive picture of the coevolution dynamics in naturally evolving populations at relatively high time resolution. Coevolution was followed by monitoring changes over time in the CRISPR loci ofGordoniametagenome-assembled genome, and reciprocal changes in the viral genome. Genome-wide analysis indicated low strain variability ofGordonia, and almost clonal conservation of the trailer end of the CRISPR loci. Incorporation of newer spacers gave rise to multiple coexisting bacterial populations. The host population carrying a shorter CRISPR locus that contain only ancestral spacers, which has not acquired newer spacers against the coexisting phages, accounted for more than half of the total host abundance in the majority of samples. Phages genome co-evolved by introducing directional changes, with no preference for mutations within the protospacer and PAM regions. Metagenomic reconstruction of time-resolved variants of host and viral genomes revealed how the complexity at the population level has important consequences for bacteria-phage coexistence.

Automated summary

This study investigated the dynamics of interaction between Gordonia and their phages in a full-scale wastewater treatment plant over a three-year period, revealing the coevolution processes at a relatively high time resolution. Analyzing genomic data showed low strain variability in Gordonia and almost clonal conservation of the CRISPR loci. Phages co-evolved by introducing directional changes, with no preference for mutations within specific regions. The complexity at the population level had important consequences for bacteria-phage coexistence, with certain host populations not acquiring newer spacers to combat coexisting phages.