Ecology and biogeochemistry of the microbial underworld in two sister soda lakes

Abstract

Abstract Approximately 3.7 billion years ago, microbial life may have emerged in phosphate-rich salty ponds. Surprisingly, analogs of these environments are present in alkaline lake systems, recognized as highly productive biological ecosystems. Investigating the microbial ecology of two Canadian soda lake sediment systems characterized by naturally high phosphate levels. Using a comprehensive approach involving geochemistry, metagenomics, and amplicon sequencing, we discovered that groundwater infiltration into Lake Goodenough sediments supported stratified layers of microbial metabolisms fueled by decaying mats. Effective degradation of microbial mats resulted in unexpectedly low net productivity. Evaporation of water from Last Chance Lake and its sediments led to saturation of brines and a habitat dominated by inorganic precipitation reactions, with low productivity, low organic matter turnover and little biological uptake of phosphorus, leading to high phosphate concentrations. Our research highlights that modern analogs for origin-of-life conditions might be better represented by soda lakes with low phosphate concentrations. Highly alkaline brines were found to be dominated by potentially dormant spore-forming bacteria. These saturated brines also hosted potential symbioses between Halobacteria and Nanoarchaeaota, as well as Lokiarchaea and bacterial sulfate reducers. Metagenome-assembled genomes of Nanoarchaeaota lacked strategies for coping with salty brines and were minimal for Lokiarchaea. Thus, highly alkaline brine environments could be too extreme to support origin of life scenarios. These findings shed light on the complex interplay of microbial life in extreme environments and contribute to our understanding of early Earth environments.