Depth-discrete metagenomics reveals the roles of microbes in biogeochemical cycling in the tropical freshwater Lake Tanganyika

Abstract

19 Lake Tanganyika, the largest tropical freshwater lake and the second largest by volume 20 on Earth is characterized by strong oxygen and redox gradients. In spite of the majority of its 21 water column being anoxic, Tanganyika hosts some of the most diverse and prolific fisheries and 22 ecosystems on Earth. Yet, little is known about microorganisms inhabiting this lake, and their 23 impacts on biogeochemistry and nutrient cycling underlying ecosystem structure and 24 productivity. Here, we apply depth-discrete metagenomics, single-cell genomics, and 25 environmental analyses to reconstruct and characterize 3996 microbial genomes representing 802 26 non-redundant organisms from 81 bacterial and archaeal phyla, including two novel bacterial 27 candidate phyla, Tanganyikabacteria and Ziwabacteria. We found sharp contrasts in community 28 composition and metabolism between the oxygenated mixed upper layer compared to deep 29 anoxic waters, with core freshwater taxa in the former, and Archaea and uncultured Candidate 30Phyla in the latter. Microbially-driven nitrogen cycling increased in the anoxic zone, highlighting 31 microbial contribution to the productive surface layers, via production of upwelled nutrients, and 32 greenhouse gases such as nitrous oxide. Overall, we provide a window into how oxygen 33 gradients shape microbial community metabolism in widespread anoxic tropical freshwaters, and 34 advocate for the importance of anoxic freshwater habitats in the context of global 35 biogeochemical cycles and nutrient cycling. 36Tran et al.

Expanded Phylogenetic Diversity and Metabolic Flexibility of Mercury-Methylating Microorganisms

“…Trout Bog Lake is a small, dimictic humic lake in a rural area near Minocqua, WI, that is surrounded by sphagnum moss, which leaches large amounts of organic carbon. Lake Tanganyika is a meromictic lake with an anoxic monimolimnion in the East African Rift Valley and is the second largest lake in the world both by volume and depth, from which we recently reconstructed nearly 4,000 MAGs ( 34 ). Lake Mendota is a large, dimictic eutrophic lake in an urban setting in Madison, WI, with a sulfidic anoxic hypolimnion.…”

“…We collected depth-discrete samples along the northern basin of Lake Tanganyika at two stations (Kigoma and Mahale). DNA extraction, metagenomic sequencing of 24 samples from Lake Tanganyika, and subsequent genome assembly and refinement were performed as described by Tran et al ( 34 ). Briefly, 24 samples were passed through a 0.2-μm-pore-size fraction filter and used for shotgun metagenomic sequencing on the Illumina HiSeq 2500 platform at the Department of Energy Joint Genome Institute.…”

METABOLIC: High-throughput Profiling of Microbial Genomes for Functional Traits, Biogeochemistry, and Community-scale Metabolic Networks

“…To benchmark and test the performance of METABOLIC in different environments, eight datasets of metagenomes and metagenomic reads from marine, terrestrial, and human environments were used. These included marine subsurface sediments [45] (Deep biosphere beneath Hydrate Ridge offshore Oregon), freshwater lake [46] (Lake Tanganyika, eastern Africa), colorectal cancer (CRC) patient gut [47], healthy human gut [47], deep-sea hydrothermal vent (Guaymas Basin, Gulf of California) [43], terrestrial subsurface sediments and water (Ri e, CO, USA) [2], meadow soils [48] (Angelo Coastal Range Reserve, CA, USA), and advanced water treatment facility [49] (Groundwater Replenishment System, Orange County, CA, USA). Default settings were used for running METABOLIC-C.…”

“…To compare the metabolic pro le of two environments at the community scale, MN-score was used as the benchmarker. Two sets of environment pairs were compared, including marine subsurface sediments [45] and terrestrial subsurface sediments and water [2], and freshwater lake [46] and deep-sea hydrothermal vent [43]. To demonstrate differences between these environments to speci c biogeochemical processes, we focused on the biogeochemical cycling of sulfur.…”

“…We also reconstructed the metabolism for Nitrospirae bacteria M_DeepCast_50m_m2_151, a member of the Nitrospirae phylum reconstructed from Lake Tanganyika [46] (Fig. 9B), it contains the full pathway for the TCA cycle and gluconeogenesis/glycolysis.…”