The prevalent taxa in oligotrophic Antarctic soils are metabolically versatile aerobes that use atmospheric trace gases for energy, carbon and hydration needs – a process recently termed aerotrophy. Although the widespread aerotrophy genes play a prominent role in microbial adaptation and survival, their dissemination and selective pressures across Antarctic soils remain largely unexplored. Here, we profiled 676 metagenome-assembled genomes from 16 glacial and mountainous soils, from a combination of short- and long-read datasets. Through phylogenetic reconciliation and mobile genetic element analysis, we provide evidence thathorizontal gene transfer events occur frequently among these bacteria. Surprisingly, someaerotrophy genes are horizontally acquired at multiple taxonomic levels and closely associated with various mobile genetic elements, including 12 CO dehydrogenase and 57 [NiFe]-hydrogenase genes. Hydrogenases responsible for atmospheric hydrogen oxidationare encoded by 12 bacterial phyla, and six Group 1l [NiFe]-hydrogenase genes are horizontally transferred among up to eight phyla. To reveal fine-scale evolutionary dynamicsof aerotrophy genes, we further investigate their genetic diversity and selection signature. Metabolic genes associated with horizontal gene transfer or in proximity to mobile genetic elements exhibit significantly higher nucleotide diversity compared to other genes without such associations. The polymorphism rates indicate most aerotrophy genes are under strong purifying selection that preserves functionality, demonstrated by a predominance of synonymous mutations. Moreover, evolutionary metrics in some energy and carbon acquisition genes, including CO dehydrogenase, are significantly related to atmospheric gasoxidation rates. Overall, these findings uncover unique eco-evolutionary trends of microbial aerotrophy in cold desert ecosystems and provide insights into microbial adaptation in the extreme polar biosphere.