Divergence of microbial carbon use efficiency and soil organic carbon along a tidal flooding gradient in a subtropical coastal wetland

Abstract

Microbial carbon use efficiency (CUE) typically promotes soil organic carbon (SOC) storage in terrestrial ecosystems. However, this relationship remains poorly understood in coastal wetlands, where tidal flooding creates unique environmental conditions, facilitates lateral transfer and SOC loss, and mediates organic matter exchange between terrestrial and marine systems. Here we examined the CUE-SOC relationship across a tidal flooding gradient (4–25% frequency) in a subtropical coastal wetland. Along this gradient, SOC decreased by 65% while microbial CUE increased from 0.24 to 0.32. This inverse relationship coincided with marked compositional shifts: plant debris declined from 57% to 18%, while microbial necromass increased from 21% to 35%. The enhanced CUE was accompanied by increased turnover times alongside decreased metabolic quotient (qCO₂), C-acquiring enzyme activities, soil basal respiration, and microbial biomass carbon (MBC). This enhanced efficiency stemmed from substrate-microbe interactions rather than environmental stresses, as communities transitioned from oligotrophic taxa (α-proteobacteria, Basidiomycota) specializing in recalcitrant terrestrial substrates to copiotrophic microorganisms (γ-proteobacteria, Bacteroidota, Ascomycota) efficiently metabolizing labile marine compounds. Contrary to terrestrial patterns, enhanced CUE did not promote SOC storage due to three key mechanisms: (i) enhanced CUE from marine substrates could not compensate for declining plant debris accumulation; (ii) reduced microbial biomass limited necromass formation despite higher CUE; and (iii) metabolic benefits from high CUE (reduced enzyme activities and respiration rates) could not offset the substantial decrease in SOC inputs. Our findings reveal distinct CUE-SOC relationships in coastal wetlands compared to terrestrial ecosystems, highlighting the importance of considering both terrestrial and marine processes in understanding carbon cycling in these transitional environments.