Enhanced viral activity and dark CO2 fixation rates under oxygen depletion: the case study of the marine Lake Rogoznica

Global change is determining the expansion of marine oxygen-depleted zones, which are hot spots of microbial-driven biogeochemical processes. However, information on the functioning of the microbial assemblages and the role of viruses in such low-oxygen systems remains largely unknown. Here, we used the marine Rogoznica Lake as a natural model to investigate the possible consequences of oxygen depletion on virus-prokaryote interactions and prokaryotic metabolism in pelagic and benthic ecosystems. We found higher bacterial and archaeal abundances in oxygen-depleted than in oxic conditions, associated with higher heterotrophic carbon production, enzymatic activities and dark inorganic carbon fixation ( DCF) rates. The oxygen-depleted systems were also characterized by higher viral abundance, production and virus-induced prokaryotic mortality. The highest DCF relative contribution to the whole total C production (>30%) was found in oxygen-depleted systems, at the highest virus-induced prokaryotic mortality values (>90%). Our results suggest that the higher rates of viral lysis in oxygen-depleted conditions can significantly enhance DCF by accelerating heterotrophic processes, organic matter cycling, and hence the supply of inorganic reduced compounds fuelling chemosynthesis. These findings suggest that the expansion of low-oxygen zones can trigger higher viral impacts on prokaryotic heterotrophic and chemoautotrophic metabolism, with cascading effects, neglected so far, on biogeochemical processes.