Soil, ocean, hot spring, and host-associated environments reveal unique selection pressures on genomic features of bacteria in microbial communities

Abstract

ABSTRACTFree-living bacteria in nutrient limited environments often exhibit small genomes which curb the cost of reproduction – a phenomenon known as genomic streamlining. Streamlining has been associated with a suite of traits such as reduced GC content, fewer 16S rRNA copies, and a lower abundance of regulatory genes, such as sigma (σ) factors. Here, we analyzed these traits from 116 publicly available metagenomes derived from marine, soil, host associated, and thermophilic communities. In marine and thermophilic communities, genome size and GC content declined in parallel, but GC content was higher in thermophilic communities. In soils, the relationship between genome size and GC content was negative, suggesting a different selection pressure on genome size and GC content in soil bacteria. The abundance of σ-factors varied with average genome size, ecosystem type, and the specific functions regulated by the sigma factor. In marine environments, housekeeping and heat-shock σ-factor genes (rpoD and rpoH respectively) increased as genome size declined, and σ-factor responsible for flagella biosynthesis (fliA) decreased, suggesting a trade-off between nutrient conservation and chemotaxis. In soils, a high abundance of fliA and the stress response σ-factor gene (rpoS) was associated with smaller average genome size and often located in harsh and/or carbon-limited environments such as deserts or agricultural fields – suggesting an increased capacity for stress response and mobility in nutrient-poor soils. This work showcases how ecosystem-specific environmental constraints force trade-offs which are then embedded in the genomic features of bacteria in microbial communities, specifically genome size, GC content, and regulatory genes, and further highlights the importance of considering these features in microbial community analysis.