Cold desert soil microbiomes thrive despite severe moisture and nutrient limitations. In Eastern Antarctic soils, bacterial primary production is supported by trace gas oxidation and the light-independent RuBisCO form IE. This study aims to determine if atmospheric chemosynthesis is widespread within Antarctic, Arctic and Tibetan cold deserts, to identify the breadth of trace gas chemosynthetic taxa and to further characterize the genetic determinants of this process. H2 oxidation was ubiquitous, far exceeding rates reported to fulfill the maintenance needs of similarly structured edaphic microbiomes. Atmospheric chemosynthesis occurred globally, contributing significantly (p < 0.05) to carbon fixation in Antarctica and the high Arctic. Taxonomic and functional analyses were performed upon 18 cold desert metagenomes, 230 dereplicated medium-to-high-quality derived metagenome-assembled genomes (MAGs) and an additional 24,080 publicly available genomes. Hydrogenotrophic and carboxydotrophic growth markers were widespread. RuBisCO IE was discovered to co-occur alongside trace gas oxidation enzymes in representative Chloroflexota, Firmicutes, Deinococcota and Verrucomicrobiota genomes. We identify a novel group of high-affinity [NiFe]-hydrogenases, group 1m, through phylogenetics, gene structure analysis and homology modeling, and reveal substantial genetic diversity within RuBisCO form IE (rbcL1E), and high-affinity 1h and 1l [NiFe]-hydrogenase groups. We conclude that atmospheric chemosynthesis is a globally-distributed phenomenon, extending throughout cold deserts, with significant implications for the global carbon cycle and bacterial survival within environmental reservoirs.

Antimicrobial resistance is an escalating health crisis requiring urgent action. Most antimicrobials are natural products (NPs) sourced from Actinomycetota, particularly the Streptomyces. Underexplored and extreme environments are predicted to harbour novel microorganisms with the capacity to synthesise unique metabolites. Herring Island is a barren and rocky cold desert in East Antarctica, remote from anthropogenic impact. We aimed to recover rare and cold-adapted NP-producing bacteria, by employing two culturing methods which mimic the natural environment: direct soil culturing and the soil substrate membrane system. First, we analysed 16S rRNA gene amplicon sequencing data from 18 Herring Island soils and selected the soil sample with the highest Actinomycetota relative abundance (78%) for culturing experiments. We isolated 166 strains across three phyla, including novel and rare strains, with 94% of strains belonging to the Actinomycetota. These strains encompassed thirty-five ‘species’ groups, 18 of which were composed of Streptomyces strains. We screened representative strains for genes which encode polyketide synthases and non-ribosomal peptide synthetases, indicating that 69% have the capacity to synthesise polyketide and non-ribosomal peptide NPs. Fourteen Streptomyces strains displayed antimicrobial activity against selected bacterial and yeast pathogens using an in situ assay. Our results confirm that the cold-adapted bacteria of the harsh East Antarctic deserts are worthy targets in the search for bioactive compounds.

Microorganisms are key to sustaining core ecosystem processes across terrestrial Antarctica but they are rarely considered in conservation frameworks. Whilst greater advocacy has been made towards the inclusion of microbial data in this context, there is still a need for better tools to quantify multispecies responses to environmental change. Here, we extend the scope of Gradient Forest modelling beyond macroorganisms and small datasets to the comprehensive polar soil microbiome encompassing >17, 000 sequence variants for bacteria, micro-eukarya and archaea throughout the hyperarid Vestfold Hills of Eastern Antarctica. Quantification of microbial diversity against 79 physiochemical variables revealed that whilst rank-order importance differed, predictors were broadly consistent between domains, with greatest sharing occurring between bacteria and micro-eukarya. Moisture was identified as the most robust predictor for shaping the regional soil microbiome, with highest compositional turnover or splits occurring within the 10 to 12 % moisture content range. Often the most responsive taxa were rarer lineages of bacteria and micro-eukarya with phototrophic and nutrient-cycling capacities such as Cyanobacteria (up to 61.81 % predictive capacity), Chlorophyta (62.17 %) and Ochrophyta (57.81 %). These taxa groups are thus at greater risk of biodiversity loss or gain to projected climate trajectories, which will inevitably disturb current ecosystem dynamics. Better understanding of these threshold tipping points will positively aid conservation efforts across Eastern Antarctica. Furthermore, the successful implementation of an improved Gradient Forest model also presents an exciting opportunity to broaden its use on microbial systems globally.