Microbial lifestyles adapted to distinct soil fertility

Abstract

Microbial life-history strategies determine how microbial communities prioritize resource allocation toward growth, resource acquisition, or stress tolerance. However, how soil microbial communities adjust their life-history strategies in response to distinct soil fertility remains poorly understood. In this study, metatranscriptomic sequencing was performed to investigate shifts in microbial life-history strategies in soils with different fertility, developed by 37 year diverse fertilization regimes: no fertilization, mineral fertilization, manure fertilization, and combined mineral/manure fertilization. Organic amendments increased the transcript abundance of genes (normalized by transcripts per million [TPM]) related to biogeochemical cycles by 13%-246% relative to unfertilized soils. We quantified the relative transcript abundance of each functional pathway within individual biogeochemical cycles to compare transcriptional allocation across treatments. Within each cycle, organic amendments increased the relative transcript abundance of genes involved in organic matter degradation by 9%-12% and dissimilatory nitrate reduction by 24%-37% relative to unfertilized soils. Although TPM-normalized transcript abundance of growth-associated genes increased 1.8- to 2.2-fold in fertilized soils, their relative abundance among all life-history transcripts remained stable at approximately 77%. Organic inputs altered microbial resource allocation by favoring resource acquisition over stress tolerance. This shift was associated with increased nutrient availability and soil pH neutralization. Taxonomic analysis revealed growth yield as the dominant strategy across most phyla. Within each strategy, Desulfobacterota showed a strong association with growth yield, Verrucomicrobiota with resource acquisition, and Pseudomonadota and Actinomycetota with stress tolerance. Notably, while strategy preferences were broadly conserved across phyla, fertilization modulated the intensity of strategy-specific gene expression, indicating functional plasticity of microbial communities in response to environmental change. Collectively, our findings suggest that differences in soil fertility resulting from long-term fertilization alter microbial resource allocation among life-history strategies by changing the functional expression of transcripts assigned to different taxa, reflecting the functional plasticity of soil microbial communities under intensified agriculture.