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

Kimberlee Thamatrakoln1, Chana Kranzler2, Mark A Brzezinski3, Michael A. Maniscalco4, Natalie Cohen5, Robert H Lampe6, James Mack7, Jason R Latham7, David Talmy8, Benjamin S Twining9 and Adrian Marchetti10, (1)Rutgers University, Marine and Coastal Sciences, New Brunswick, United States, (2)Rutgers University, Marine and Coastal Sciences, New Brunswick, NJ, United States, (3)University of California, Marine Science Institute, Santa Barbara, CA, United States, (4)University of California Santa Barbara, Ecology Evolution and Marine Biology, Santa Barbara, CA, United States, (5)Woods Hole Oceanographic Institution, Falmouth, MA, United States, (6)Scripps Institution of Oceanography, La Jolla, United States, (7)Rutgers University, New Brunswick, NJ, United States, (8)The University of Tennessee, Microbiology, Knoxville, United States, (9)Bigelow Lab for Ocean Sciences, East Boothbay, ME, United States, (10)University of North Carolina at Chapel Hill, Earth, Marine, and Environmental Sciences, Chapel Hill, United States
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