Multiple energy sources and metabolic strategies sustain microbial diversity in Antarctic desert soils

Abstract

Numerous diverse microorganisms reside in the cold desert soils of continental Antarctica, though we lack a holistic understanding of the metabolic processes that sustain them. Here, we profile the composition, capabilities, and activities of the microbial communities in 16 physicochemically diverse mountainous and glacial soils. We assembled 451 metagenome-assembled genomes from 18 microbial phyla and inferred through Bayesian divergence analysis that the dominant lineages present are likely native to Antarctica. In support of earlier findings, metagenomic analysis revealed that the most abundant and prevalent microorganisms are metabolically versatile aerobes that use atmospheric hydrogen to support aerobic respiration and sometimes carbon fixation. Surprisingly, however, hydrogen oxidation in this region was catalyzed primarily by a phylogenetically and structurally distinct enzyme, the group 1l [NiFe]-hydrogenase, encoded by nine bacterial phyla. Through gas chromatography, we provide evidence that both Antarctic soil communities and an axenic Bacteroidota isolate (Hymenobacter roseosalivarius) oxidize atmospheric hydrogen using this enzyme. Based on ex situ rates at environmentally representative temperatures, hydrogen oxidation is theoretically sufficient for soil communities to meet energy requirements and, through metabolic water production, sustain hydration. Diverse carbon monoxide oxidizers and abundant methanotrophs were also active in the soils. We also recovered genomes of microorganisms capable of oxidizing edaphic inorganic nitrogen, sulfur, and iron compounds and harvesting solar energy via microbial rhodopsins and conventional photosystems. Obligately symbiotic bacteria, including Patescibacteria, Chlamydiae, and predatory Bdellovibrionota, were also present. We conclude that microbial diversity in Antarctic soils reflects the coexistence of metabolically flexible mixotrophs with metabolically constrained specialists.

Elevational Constraints on the Composition and Genomic Attributes of Microbial Communities in Antarctic Soils

“…Our results build on those reported previously in highlighting that trace gas metabolism is likely an important metabolic strategy used by Antarctic soil microbial taxa ( 19 , 20 ) and support previous work that atmospheric trace gas metabolism, and in particular hydrogen oxidation, is widespread in a variety of soil environments ( 32 , 33 ). These metabolic strategies may be particularly important in Antarctic soils, where biogeochemical studies suggest that the rate at which soil communities oxidize atmospheric trace gases may be sufficient to sustain their energy needs under certain conditions ( 20 ).…”

“…S5 ). This identification of high-elevation-associated metabolic genes supports previous work suggesting that microbial communities use a greater variety of genes coding for metabolic pathways in more challenging Antarctic environments ( 17 – 19 ). Of note, the metabolic pathway with the greatest number of genes overrepresented in the higher-elevation soils was the “methane metabolism” pathway (KEGG pathway KO00680).…”

“…Of note, the metabolic pathway with the greatest number of genes overrepresented in the higher-elevation soils was the “methane metabolism” pathway (KEGG pathway KO00680). Trace gas metabolisms, including methanotrophy, are important metabolic strategies used by microorganisms in Antarctica and other hyperarid environments to generate energy and fix carbon ( 19 , 20 ), yet this evidence suggests that the relative importance of these metabolic strategies may increase under more challenging conditions.…”

“…S6 ). Notably, the most abundant genes related to hydrogen oxidation were those in the recently identified group 1l [NiFe]-hydrogenases (Hyd) (HylL), which have been shown to be the primary catalysts of hydrogen oxidation in cold desert soils in other regions of Antarctica ( 19 ). The higher abundance of genes associated with hydrogen oxidation and methane oxidation suggests that trace gas metabolism may be particularly important for sustaining microbial life in higher-elevation Antarctic soils.…”

“…These adaptations can include those related to osmoregulation and psychrophily that allow microbes to maintain homeostasis and survive Antarctic conditions ( 6 , 13 ). Microbial communities in Antarctica also use a variety of metabolic pathways to survive in the resource-limited environments typical of most Antarctic soils ( 17 – 19 ). For example, there is accumulating evidence that the metabolism of atmospheric trace gases (including CO, H 2 , and CO 2 ) is a key metabolic strategy used by microorganisms in Antarctica and other hyperarid environments to fix carbon and generate energy ( 20 , 21 ).…”