Cyanophage abundance and infection of picocyanobacteria are defined by environmental gradients in the North Pacific Ocean

Viruses infect and kill marine microbes and thus are thought to control population abundances and mediate organic matter cycling in the ocean. Yet how viral infection changes with abiotic conditions and which viruses are responsible for infection are poorly constrained. We used a new solid phase PCR, the polony method, to measure the abundances of 3 major cyanophage families and to quantify virally infected Prochlorocococcus and Synechococcus along environmental gradients in the North Pacific Ocean from the oligotrophic subtropical to the high-nutrient low-chlorophyll subpolar gyres. In both gyres, T4-like cyanomyophages were the most abundant family followed by T7-like cyanopodophages, which together comprised over 80% of total cyanophages. Less than 1% of picocyanobacteria were infected despite cyanophages being 4-16x more abundant than their hosts in oligotrophic waters. However, the transition zone between the gyres was a hotspot of viral activity where abundances and infection by all cyanophage families peaked 2-10x relative to the subtropics. On one transect, viruses infected 8% of picocyanobacteria in the transition zone, killing an estimated 25% of cyanobacteria daily. The increase in viral infection was mirrored by a crash in Prochlorococcus which occurred well before Prochlorococcus’ thermal growth limit. This suggests that viruses may episodically restrict Prochlorococcus’ geographic range. The high percent infection at this time could not be explained solely by host-virus contact rates as similar contact rates were observed on other transects where infection levels were significantly lower. Therefore, cyanobacteria in the transition zone appear to fluctuate in susceptibility to viral infection. Organic matter produced from lysis was calculated to sustain up to 10% of measured heterotrophic bacterial production in the subtropics and the transition zone. Furthermore, virus-mediated organic matter turnover in the mixed layer of the geographically narrow transition zone was similar to that in the entire subtropical gyre mixed layer highlighting the importance of this region to biogeochemical estimates. Thus, viruses may, at times, dramatically shape picocyanobacterial populations and mediate the turnover of primary production which sustains the greater microbial community.