Cyanobacterial viruses exhibit diurnal rhythms during infection

Significance To adapt to the daily light–dark cycle, diurnal rhythms are used by the photosynthetic cyanobacteria Prochlorococcus and Synechococcus, which are the most abundant photosynthetic organisms on earth. Field studies revealed that cyanobacterial virus (cyanophage) populations in the oceans showed transcriptional rhythms. To explore the underlying mechanism, we used cyanophage laboratory cultures to find that some showed adsorption rhythms and all showed transcriptional rhythms. We discovered that the cyanophage transcriptional rhythm is partially caused by the photosynthetic activity of host cells, explaining transcriptional rhythms of field cyanophage populations. Our study shows that cultured viruses have diurnal infection rhythms which are critical for understanding how light–dark cycles shape the interaction of cyanophages and their hosts in the oceans.
As an adaptation to the daily light–dark (diel) cycle, cyanobacteria exhibit diurnal rhythms of gene expression and cell cycle. The light–dark cycle also affects the life cycle of viruses (cyanophages) that infect the unicellular picocyanobacteria Prochlorococcus and Synechococcus, which are the major primary producers in the oceans. For example, the adsorption of some cyanophages to the host cells depends on light, and the burst sizes of cyanophages are positively correlated to the length of light exposure during infection. Recent metatranscriptomic studies revealed transcriptional rhythms of field cyanophage populations. However, the underlying mechanism remains to be determined, as cyanophage laboratory cultures have not been shown to exhibit diurnal transcriptional rhythms. Here, we studied variation in infection patterns and gene expression of Prochlorococcus phages in laboratory culture conditions as a function of light. We found three distinct diel-dependent life history traits in dark conditions (diel traits): no adsorption (cyanophage P-HM2), adsorption but no replication (cyanophage P-SSM2), and replication (cyanophage P-SSP7). Under light–dark cycles, each cyanophage exhibited rhythmic transcript abundance, and cyanophages P-HM2 and P-SSM2 also exhibited rhythmic adsorption patterns. Finally, we show evidence to link the diurnal transcriptional rhythm of cyanophages to the photosynthetic activity of the host, thus providing a mechanistic explanation for the field observations of cyanophage transcriptional rhythms. Our study identifies that cultured viruses can exhibit diurnal rhythms during infection, which might impact cyanophage population-level dynamics in the oceans.