Marine picocyanobacteria are abundant photosynthetic organisms of global importance. They coexist in the ocean with cyanophages—viruses that infect cyanobacteria. Cyanophages carry many auxiliary metabolic genes acquired from their hosts that are thought to redirect host metabolism for the phage’s benefit1–5. One such gene is nblA, which is present in multiple cyanophage families2,6–8. Under nutrient deprivation cyanobacterial NblA is responsible for inducing proteolytic degradation of the phycobilisome9–11, the large cyanobacterial photosynthetic light-harvesting complex. This increases the pool of amino acids available for essential tasks11, serving as a survival mechanism12. Ectopic expression of different cyanophage nblA genes results in host pigment protein degradation6,8,13. However, the benefit of the virus-encoded NblA for cyanophages and the broader impact on the host are unclear. Here, using a recently developed genetic manipulation system for marine cyanophages14, we reveal that viral NblA significantly accelerates the cyanophage infection cycle, directs degradation of the host phycobilisome and other proteins, and reduces host photosynthetic light-harvesting efficiency. Metagenomic analysis revealed that cyanophages carrying nblA are widespread in the oceans and comprise 35% and 65% of oceanic T7-like cyanophages in surface and deep photic zones, respectively. Our results show a large benefit of NblA to the cyanophage, while it exerts a negative effect on the host photosynthetic apparatus and host photosynthesis. These findings suggest that cyanophage NblA has an adverse global impact on light harvesting by oceanic picocyanobacteria.
