Daily turnover of active giant virus infection during algal blooms revealed by single-cell transcriptomics

Viruses are the most abundant biological entity in the ocean and play a significant role in shaping the marine ecosystem. The past two decades have revealed an outstanding diversity of giant viruses infecting protists across the tree of life and, in particular, algae that form massive blooms in the ocean. Virus-induced bloom demise significantly impacts marine ecology and biogeochemistry, as well as the associated microbial community. Nevertheless, little is known about the infection dynamics of these giant viruses in the natural environment and their role in regulating algal blooms. Here, we provide evidence for a daily life cycle of giant viral infection in algal blooms by processing the transcriptome of over 12,000 single algal cells during different phases of interaction with their giant viruses. We revealed that viral infection occurs already at the exponential phase of the bloom and that the timing of infection can determine the magnitude of the bloom but not the fraction of infected cells. We further revealed that the same proportion of infected cells are in the early phase of the viral replication program (13.5%) throughout several consecutive days of the bloom, suggesting that a daily turnover of infection is at play during the bloom and demise phases of the algal population. This may imply that a continuous source of virocell-associated metabolites diffuses throughout the bloom succession and could fuel the microbial food webs. Finally, we link single cell infection state to host physiology and show that infected cells remained calcified even in the late stage of infection, contradicting common observation of bulk population in which viral infection is directly linked with decalcification. Together, these results highlight the importance of studying host-virus dynamics in natural populations at a single-cell resolution, which can provide a fresh view of the dynamics and propagation of viral infection. This approach will enable quantification of the impact of marine viruses on microbial food webs.