Microbial assemblages and associated biogeochemical processes in Lake Bonney, a permanently ice-covered lake in the McMurdo Dry Valleys, Antarctica

Abstract

Abstract Background Lake Bonney, which is divided into a west lobe (WLB) and an east lobe (ELB), is a perennially ice-covered lake located in the McMurdo Dry Valleys of Antarctica. Several studies have reported the microbial community dynamics of ice-covered lakes in these ecosystems, yet little is known about genomic diversity and microbe-driven nutrient cycling. Here, we applied gene- and genome-centric approaches to investigate the microbial ecology and reconstruct microbial metabolic potential along the depth gradient in Lake Bonney. Results Lake Bonney is strongly chemically stratified, yielding three distinct redox zones based on oxygen and geochemistry, which provide distinct microbial niches. In the upper relatively freshwater zone with the highest level of sunlight, oxygenic photosynthetic production by the cyanobacterium Pseudanabaena and a diversity of protist microalgae provides new organic carbon to the environment. Carboxydotrophs, such as Acidimicrobiales, Nanopelagicales, and Burkholderiaceae were also prominent in the upper zone and their ability to oxidize carbon monoxide to carbon dioxide can serve as a supplemental energy source during organic carbon starvation and provide carbon dioxide to photoautotrophs. In the deeper saline chemocline zone of ELB, an accumulation of inorganic nitrogen and phosphorus supports photosynthesis despite relatively low light levels. Conversely, in WLB the release of organic rich subglacial discharge from Taylor Glacier in WLB appeared to fuel the growth of heterotrophs with increased potentials for glycolysis, beta-oxidation, and glycoside hydrolase. The suboxic and subzero temperature zones beneath the chemoclines in ELB and WLB supported microorganisms that can utilize hydrogen, nitrogen, and sulfur as metabolic energy sources. Heterotrophs and hydrogen-oxidizing denitrifying bacteria dominated the bottom of the WLB, whereas the conditions at the bottom of the ELB inhibited microbial growth, except for halophile Halomonas and endospore-forming Virgibacillus. Conclusions The niche-dependent distribution of microbially driven C, N and S cycling genes/pathways in this unique lake reveals that microorganisms have their own survival strategies for nutrient and energy acquisition and stress responses through the water column, which are closely linked to biogeochemical cycling in the lake.