Title: Degradation of photosynthetic antennae by viral auxiliary metabolic proteins
Abstract: Cyabophage auxiliary metabolic genes have a direct and substantial effect on oceanic photosynthesis and primary productivity Cyanophages often carry auxiliary metabolic genes (AMGs) acquired from their cyanobacterial hosts, believed to redirect host cell metabolism for the phage’s benefit. Building on our previous work, which suggested that some uncultured marine cyanophages encode active NblA proteins responsible for phycobilisome (PBS) degradation in cyanobacteria, we knocked out the nblA gene in a marine cyanophage, and also constructed a marine cyanobacterial strain overexpressing the viral nblA gene, to investigate the role of NblA in viral fitness. Our study revealed that during infection, cyanophages utilize NblA for targeted PBS degradation. When comparing the infection courses of the wildtype (WT) cyanophage and the nblA deletion mutant in the host cells, we observed faster propagation in the WT, suggesting that the nblA gene significantly enhances infection progression. Infections by the WT cyanophage led to more than 50% reduction in cyanobacterial photosynthesis, compared to those infected by the nblA deletion mutant. Based on metagenomic data, we conclude that cyanophages carrying such nblA genes are widespread and compose between 35% (in surface waters) to 65% (in Deep Chlorophyll Maximum depths) of oceanic T7-like cyanophages. Our data suggest that cyanophage-encoded AMGs such as nblA have a direct and substantial effect on oceanic photosynthesis and primary productivity.