The marine cyanobacterium Prochlorococcus is one of the most abundant unicellular photosynthetic organisms in the oceans, being a major contributor to carbon fixation in aquatic environments. Cyanophages are viruses that infect cyanobacteria and release cellular components into the marine ecosystem, contributing greatly to global biogeochemical cycles. 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 cyanophages. 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 transcri...[ Read more ]

The marine cyanobacterium Prochlorococcus is one of the most abundant unicellular photosynthetic organisms in the oceans, being a major contributor to carbon fixation in aquatic environments. Cyanophages are viruses that infect cyanobacteria and release cellular components into the marine ecosystem, contributing greatly to global biogeochemical cycles. 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 cyanophages. 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, before studying cyanophage infection under light-dark cycles, I first characterized synchronized Prochlorococcus, and showed a three-dimensional (3D) organization dynamics of the cell division protein FtsZ during the cell cycle. Then, I studied variation in infection patterns and gene expression of Prochlorococcus phages in laboratory culture conditions as a function of light. I 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 the cyanophages P-HM2 and P-SSM2 also exhibited rhythmic adsorption patterns. I further showed 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. Finally, I compared the relative fitness of cyanophages that showed different life history traits; I allowed laboratory-cultured cyanophages that showed different life history traits to compete and measured the relative abundance of cyanophages with different life history traits that were isolated from the South China Sea. I found that with limited bench culture, P-HM2 had a fitness advantage over P-SSP7 under light-dark cycles and that P-SSM2 outcompeted P-HM2 under continuous light and under light-dark cycles. However, among the field-isolated cyanophages, P-SSP7–like cyanophages had the highest relative fitness. The results suggested a potential coexistence mechanism for the three life history traits. My study identifies that cultured viruses can exhibit diurnal rhythms during infection, which might impact cyanophage population-level dynamics in the oceans.