Dynamic marine viral infections and major contribution to photosynthetic processes shown by regional and seasonal picoplankton metatranscriptomes

Viruses are an important top-down control on microbial communities, yet their direct study in natural environments has been hindered by culture limitations1-3. The advance of sequencing and bioinformatics over the last decade enabled the cultivation independent study of viruses. Many studies focus on assembling new viral genomes4-6 and studying viral diversity using marker genes amplified from free viruses7,8. We used cellular metatranscriptomics to study community-wide viral infections at three coastal California sites throughout a year. Generation of and recruitment to viral contigs (> 5kbp, N=66) allowed tracking of infection dynamics over time and space. Here we show that while these assemblies represent viral populations, they are likely biased towards clonal or low diversity assemblages. Furthermore, we demonstrate that published T4-like cyanophages (N=50) and pelagiphages (N=4), having genomic continuity between close relatives, are better tracked using marker genes. Additionally, we demonstrate determination of potential hosts by matching infection dynamics with microbial community composition. Finally, we quantify the relative contribution of various cyanobacteria and viruses to photosystem-II psbA expression in our study sites. We show sometimes >50% of all cyanobacterial+viral psbA expression we observed is of viral origin, which highlights the proportion of infected cells and makes viruses a remarkable contributor to photosynthesis and oxygen production.