Reduced legacy precipitation decreases microbial community growth efficiency and alters soil organic carbon in a California grassland

Abstract

Changes in global patterns can leave a lasting legacy in semi-arid grasslands by reshaping microbial growth dynamics and carbon cycling during the first wet-up in the autumn--a period known for intense microbial activity and significant carbon emissions. To study the lasting impacts of decreased winter rain, we implemented two precipitation regimes (100% vs. 50% mean annual precipitation) in California Mediterranean-climate grassland field plots. After the dry season, soils were rewetted in the laboratory with H218O, and sampled at 0 h, 3 h, 24 h, 48 h, 72 h, and 168 h post rewet. We quantified CO2 efflux; measured microbial growth and mortality via quantitative 18O stable isotope probing and 16S rRNA gene amplicon sequencing; and characterized the soil organic carbon chemical composition, metagenomes, and metatranscriptomes. We found that reduced winter precipitation imposed a strong legacy effect on microbial turnover; despite maintaining similar respiration rates, microbial growth declined by [~]1 order of magnitude, yielding decreased community growth efficiency (CGE = gross community growth/net respiration), and microbial mortality declined by [~]2 orders of magnitude. Soil organic carbon also shifted from lipid-like, amino-sugar-like, and protein-like compounds (indicative of microbial necromass) to more oxidized lignin-like and tannin-like compounds (indicative of decomposing plant-derived compounds). Meta-omics revealed distinct metabolic strategies linked to CGE. At high-CGE, microbes appeared to consume more energetically favorable N-rich necromass (released via high microbial turnover), this allowed for increased amino acids and peptidoglycan biosynthesis and greater aromatic compound degradation, fueling further energy production and growth efficiency. At low-CGE, communities had elevated carbohydrate metabolism and lipid turnover, consistent with increased investment in plant detritus degradation and membrane repair and maintenance rather than growth. Together, our findings demonstrate that reduced winter rainfall decreases microbial turnover following rewetting. Persistent decreases in CGE due to reduced winter rainfall result in consistent carbon loss as CO2, which, if sustained over multiple years, could ultimately lead to a net decline in total soil organic carbon.