Shifts in Genome Size and Energy Utilization Strategies Sustain Microbial Functions Along an Aridity Gradient

Abstract

Microbes acquire energy to sustain their survival and function through the decomposition of organic carbon (C) or by oxidizing atmospheric trace gases (e.g., H₂, CO, CH₄). However, how these two microbial energy-acquisition strategies change along environmental gradients and the underlying mechanisms are unclear. This study investigated the energy strategies and genomic traits of soil microbiomes along a natural aridity gradient, ranging from semi-humid forests to arid deserts. By analyzing 374 metagenome-assembled genomes from 13 microbial phyla, we found that the most prevalent microbes are metabolically versatile aerobes that use atmospheric trace gases to support aerobic respiration, C fixation, and N, P, and S cycling. Soil microbes adapt genomic traits associated with reduced energy expenditure in more arid soils, including smaller genome sizes, lower GC content, and fewer 16S rRNA gene copies. Microbial communities in diverse arid habitats are capable of utilizing organic compounds and the oxidation of trace gases (e.g., H₂, CO, CH₄, and H₂S) as energy sources. However, the utilization of organic energy decreased while reliance on trace gas oxidation increased with increasing aridity. Higher consumption rates of H₂, CO, and CH₄ in desert soils from ex situ culture experiments confirmed that increased aridity stimulates microbial oxidation of atmospheric trace gases. This shift in energy utilization was strongly correlated with declining soil organic C levels. As organic C decreased along the aridity gradient, the abundance of trace gas oxidizers (both specialized and multi-gas oxidizers) increased significantly, while that of non-oxidizers declined. Trace gas oxidizers exhibited smaller genomes, lower 16S rRNA operon copy numbers, and slower predicted growth rates, indicative of oligotrophic lifestyles. In contrast, copiotrophic non-oxidizers had larger genomes and faster growth rates. These findings reveal that microbial communities adapt their genomic traits and energy-acquisition strategies to sustain functionality across aridity gradients, enhancing our understanding of soil microbiome responses to climate change.