Viral NblA proteins negatively affect oceanic cyanobacterial photosynthesis

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 benefit^1-5. One such gene is nblA, which is present in multiple cyanophage families^2,6-8. Under nutrient deprivation cyanobacterial NblA is responsible for inducing proteolytic degradation of the phycobilisome^9-11, 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 degradation^6,8,13. 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.