Host-Virus Interactions Under Turbulent Flow Regimes

Viral infection is a microscale process requiring a virus to encounter, adsorb, and enter its host within an environment that is fundamentally turbulent. While the hydrodynamic environment plays a critical, first-order role in microscale host-virus interactions and their propagation across meso- and global- scales, current research has overlooked how physics impacts infection. Emiliania huxleyi, a cosmopolitan globally-distributed coccolithophore, forms massive blooms frequently terminated by Coccolithovirus (EhV) infection, a process that can impact the fate of fixed carbon and drive elemental cycling. We present a theoretical framework based on encounter rates, adsorption, and infectivity on how physical fluid regimes drive microscale interactions and the dynamics of infection. At natural E. huxleyi bloom densities (10³ ml^-1), the calculated maximum encounter rate between a virus and a calcified host is once every 10 days in highly turbulent, stormy regimes, rendering mesoscale bloom termination highly unlikely over observed weekly bloom-and-bust time scales. We found that high turbulence advanced lytic infection of dense lab cultures (10⁵ ml^-1), for which encounter rates are predicted to be as high as 10 times per day, even though it decreased virus infectivity compared to still conditions. Free coccoliths routinely shed by E. huxleyi cells can act as adsorptive barriers, further lowering host encounter probability. At the same time, we calculated that coccoliths contact viruses 5-100 times more often than host cells, depending on the turbulence regime. These virus-containing coccoliths (i.e., viroliths) potentially catalyze infection across spatial and temporal scales, given our observations that viroliths are infective and contact hosts 100-1000 times more than viruses. Our work highlights fundamental barriers to lytic infection in natural systems and explores how microscale biophysics shapes interactive dynamics and the outcome of infection.