Bacteriophages carry auxiliary metabolic genes related to energy, sulfur and phosphorus metabolism during a harmful algal bloom in a freshwater lake

Cyanophages play an important role in nutrient cycling in lakes since they can modulate the metabolism of cyanobacteria. A proper understanding of the impact of cyanophage infection on the metabolism and ecology of cyanobacteria is critical during a complete cycle of harmful algal bloom (HAB). The ecology of cyanophages in marine environments has been well-delineated, but cyanophages in freshwater lakes remain less studied. Here, we studied the diversity of cyanophages and their impact on host ecology and metabolism through the succession of HAB in Utah Lake, which is a shallow eutrophic freshwater lake, in 2019. We collected water samples at three different periods from two locations in freshwater Utah Lake. The three sampling periods represented the pre-bloom, peak-bloom, and post-bloom events. We observed that the Utah Lake virome was dominated by families Myoviridae, Siphoviridae, and Podoviridae under the order Caudovirales. We detected photosystem-related genes, sulfur assimilation genes, and pho regulon (phosphorus metabolism) genes in genomes of predicted cyanophages. We were able to capture the changes in relative abundance and expression of functional genes in genomes of cyanophage at different stages of the bloom. We observed higher relative abundance and expression of cyanophage-encoded pho-regulon genes in the “pre-bloom” period. The higher expression of pho-regulon genes in P-limited ecosystem of Utah Lake indicated the possible contribution of cyanophage to enhance the fitness of the host cyanobacteria. Our study provides some insightful findings on the role of cyanophages in controlling the ecology and relative abundance of host cyanobacteria in freshwater lakes.