Depth-discrete eco-genomics of Lake Tanganyika reveals roles of diverse microbes, including candidate phyla, in tropical freshwater nutrient cycling

Abstract Lake Tanganyika, the largest tropical freshwater lake and the second largest by volume on Earth is characterized by strong oxygen and redox gradients. In spite of the majority of its water column being anoxic, Tanganyika hosts some of the most diverse and prolific fisheries and ecosystems on Earth. Yet, little is known about microorganisms inhabiting this lake, and their impacts on biogeochemistry and nutrient cycling underlying ecosystem structure and productivity. Here, we apply depth-discrete metagenomics, single-cell genomics, and environmental analyses to reconstruct and characterize 3996 microbial genomes representing 802 non-redundant organisms from 81 bacterial and archaeal phyla, including two novel bacterial candidate phyla, Tanganyikabacteria and Ziwabacteria. We found sharp contrasts in community composition and metabolism between the oxygenated mixed upper layer compared to deep anoxic waters, with core freshwater taxa in the former, and Archaea and uncultured Candidate Phyla in the latter. Microbially-driven nitrogen cycling increased in the anoxic zone, highlighting microbial contribution to the productive surface layers, via production of upwelled nutrients, and greenhouse gases such as nitrous oxide. Overall, we provide a window into how oxygen gradients shape microbial community metabolism in widespread anoxic tropical freshwaters, and advocate for the importance of anoxic freshwater habitats in the context of global biogeochemical cycles and nutrient cycling.