Metabolic potential and survival strategies of microbial communities across extreme temperature gradients on Deception Island volcano, Antarctica

Abstract

AbstractActive volcanoes in Antarctica, in contrast to the rest of the icy landscape, have remarkable temperature and geochemical gradients that could select for a wide variety of microbial adaptive mechanisms and metabolic pathways. Deception Island is a stratovolcano flooded by the sea, resulting in contrasting ecosystems such as permanent glaciers (<0 °C) and active fumaroles (up to 100 °C). Steep gradients in temperature, salinity and geochemistry over very short distances have been reported for Deception Island, and have been shown to effect microbial community structure and diversity. However, little is known regarding how these gradients affect ecosystem functioning, for example due to inhibition of key metabolic enzymes or pathways. In this study, we used shotgun metagenomics and metagenome-assembled genomes to explore how microbial functional diversity is shaped by extreme geochemical, salinity and temperature gradients in fumarole and glacier sediments. We observed that microbial communities from a 98 °C fumarole harbor specific hyperthermophilic molecular strategies, as well as reductive and autotrophic pathways, while those from <80 °C fumaroles possess more diverse metabolic and survival strategies capable of responding to fluctuating redox and temperature conditions. In contrast, glacier communities showed less diverse metabolic potentials, comprising mainly heterotrophic and carbon pathways. Through the reconstruction of genomes, we were able to clarify putative novel lifestyles of underrepresented taxonomic groups, especially those related to Nanoarchaeota and thermophilic ammonia-oxidizing archaeal lineages. Our results enhance understanding of the metabolic and survival capabilities of different extremophilic lineages of Bacteria and Archaea.