Trade-off between microbial ecophysiological features regulated by soil fertility governs plant residue decomposition

Soil fertility influences microbial-driven plant residue decomposition, thus further affecting soil organic carbon (C) formation. Both ecological and physiological features of microbial communities change with soil fertilities, however, the mechanism of how soil fertility influences microbial ecophysiological features (both the taxonomic and functional profiles) driving plant residue decomposition is unclear. Here, four series of microcosms were set up, inoculated with two distinct soils, each with low and high fertility levels as a result of contrasting long-term fertilization regimes, and incubated with 13C-labeled rice straw amendments. DNA stable-isotope probing (DNA-SIP) based amplicon sequencing and shotgun metagenomic sequencing were conducted. We found that both bacterial community composition (including the relative abundance, α- and β-diversities, and taxonomic composition) and carbohydrate metabolic efficiency were significantly changed under different soil fertilities. High fertile soils gave rise to greater increases in bacterial populations and straw decomposition than low fertile soils, yet DNA-SIP-based shotgun metagenomic sequencing showed that the bacterial average carbohydrate metabolic efficiency, characterized by the average carbohydrate-active enzyme (CAZyme) abundance within each bacterial phylum was significantly lower. Linear regressions between bacterial ribosomal RNA operon (rrn) copy number and bacterial carbohydrate metabolic efficiency under contrasting soil fertilities suggested that high fertile soils select for fast-but-inefficient bacteria to degrade rice straw while low fertile soils select for slow-but-efficient ones. Collectively, the data demonstrate a fundamental trade-off between the ecological and physiological attributes of straw-degrading microbial communities. The trade-off is regulated by soil fertility and in turn governs plant residue decomposition. This work provides novel insights for better understanding the ecological and physiological roles of microbes in organic matter decomposition and global terrestrial C cycling, especially in the context of crop straw degradation under contrasting soil fertilities.