Plant-microbe interactions underpin the contrasting enzymatic responses to wetland drainage

The tremendous carbon storage of wetlands is closely related to the inhibited enzyme (especially phenol oxidase) activity under oxygen-deprived conditions, which is a rate-limiting step in carbon decomposition. However, phenol oxidase response to field drainage is highly uncertain, constraining our ability to predict wetland carbon-climate feedbacks. Here, using literature data, laboratory simulations, and a pair-wise survey of 30 diverse wetlands experiencing long-term (15–55 years) drainage across China, we show that in contrast to short-term drainage where oxygen exposure generally increases phenol oxidative activity, its response to long-term drainage diverges in Sphagnum vs. non-Sphagnum wetlands. By employing soil metagenomic and plant metabolic analyses, we further demonstrate that long-term drainage increases plant secondary metabolites in non-Sphagnum wetlands, thereby decreasing phenol oxidase-producing microbes and phenol oxidative activity. In contrast, phenol oxidative activity increases in drained Sphagnum wetlands due to replacement of Sphagnum rich in phenolic, antimicrobial metabolites by vascular plants. Therefore, plant-microbe interactions underpin the divergent responses of phenol oxidase to field drainage in Sphagnum vs. non-Sphagnum wetlands, with cascading effects on hydrolytic enzyme activity and decomposition processes. Our findings highlight that trait-based plant dynamics are pivotal to decipher wetland carbon dynamics and feedback to climate change under shifting hydrological regimes.