Synergistic impacts of viral infection and iron limitation on diatom-mediated biogeochemical cycling

Diatoms, crucial players in the biological pump, contribute ~40% of marine primary productivity with diatom biogenic silica ballasting substantial vertical flux of particulate organic carbon out of the mixed layer. Iron (Fe) limitation of primary production is associated with regions characterized by high vertical flux and burial of biogenic silica, processes that impact silicon cycling and diatom production globally. Although marine viruses are considered drivers of ocean biogeochemical cycles, little is known about how viruses impact the fate of diatom organic matter. In this study, we explored the interplay between diatoms, viruses and Fe availability. Using metatranscriptomic analysis of natural populations in the California Current Ecosystem, we observed that cell-associated diatom viruses were notably low in Fe-limited diatom populations. We also found reduced viral replication in deck-board incubations of induced Fe-limited diatoms. In laboratory cultures of the bloom forming, centric diatom, Chaetoceros tenuissimus, and its associated virus, CtenDNAV, we found viral infection was impaired during Fe limitation, with delayed host mortality and reduced viral replication. These observations appear to be related to the oxidative state of the cell, as measurements of intracellular reactive oxygen species and cellular antioxidant capacity suggest that host-induced cellular regulation of oxidative stress during Fe limitation impairs viral infection. Our findings were recapitulated in dynamic models of virus infection setting the stage for incorporating these parameters in coupled ecosystem and biogeochemical models. Intriguingly, we also found that infected diatoms exhibit higher cellular biogenic silica, implying the potential for increased mineral ballast during infection that, combined with prolonged infection dynamics, may serve as a conduit for export in Fe-limited regions of the ocean