Vertical niche occupation and potential metabolic interplay of microbial consortia in a deeply stratified meromictic model lake

Abstract

AbstractThe microbial ecology of meromictic lakes assessed with “omics” is still poorly studied compared to other aquatic systems. Here, a combination of metagenomics, high resolution sampling and detailed physical–chemical data gathering allowed to study the planktonic prokaryotic assemblages and metabolic capabilities in the crenogenic meromictic Lake El Tobar (Spain), a model lake for such purposes. This system presents a specific stratification comprising a freshwater layer and a halocline linked to the oxycline, driving to the euxinic hypersaline waters of the deep monimolimnion. The different strata showed a highly diverse and vertically distributed microbiome with their metabolic capacities fitting/influencing the physical–chemical environment. Overall, up to 338 novel genomes were found from metagenome assembled genomes. Picocyanobacteria and methanotrophs were abundant in the upper part of the oxycline. Anoxygenic phototrophs (Chlorobium, Thiohalocapsa, Chromatiaceae, Rhodospirillum, and Rhodobacteraceae spp.) dominated the 12.5–14 m anoxic waters with dim light availability. Sulfate reducers (Desulfobacterota and Firmicutes) inhabited low redox horizons from 13.5 to the bottom (18 m). The potential microbial synergistic performance increases toward the monimolimnion. Among these, a microbial assemblage mostly composed of Spirochaetota, Cloacimonadota, Omitrophota, Firmicutes, Marinisomatota, Nanoarchaeota, and Patescibacteria in hypersaline waters of 14–18 m (conductivities of 118–213 mS cm−1), is potentially capable of performing mixed‐acid fermentations, even including hydrogen and butanol biosynthesis of biotechnological interest. This metagenomics study shows how microbial lifestyles may be determinant in the interplay of environmental gradients, and exemplifies the potential interactions between the microbial guilds thereby.