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The Puzzle: Enzymatic Response to Wetland Drainage
Wetlands store approximately one third of soil carbon globally and are a key player in mediating climate change as an important sink of atmospheric CO2. The tremendous carbon storage in wetlands is often attributed to the inhibited enzyme (particularly phenol oxidase) activity under oxygen-deprived conditions, which acts as an ‘enzyme latch’ on organic carbon degradation. Wetland drainage is hence expected to induce a surge of phenol oxidative activity and carbon decomposition via increasing oxygen availability. However, studies have reported no changes and even decreases of phenol oxidative activity following drainage in different wetlands. These contrasting reports intrigue us to investigate the divergent enzymatic responses to drainage and the underlying mechanisms.
Our preliminary literature review indicates that increased phenol oxidase activity following drainage is mainly observed in high-latitude, carbon-rich wetlands, in particular Sphagnum-dominated peatlands in Europe and North America. In contrast, non-Sphagnum wetlands, dominated by herbaceous and/or woody species such as Carex, often show no change or even a decrease in phenol oxidase activity after drainage. The latter wetlands are widespread globally, especially in mid- and low-latitude regions, including the largest wetland areas in China—the Sanjiang Plain and Zoige wetlands. Our previous studies have shown that Sphagnum wetlands differ greatly from non-Sphagnum wetlands in soil properties, microbial activities and even organo-mineral interactions due to acidic, antimicrobial metabolites exudated by Sphagnum. Therefore, we hypothesize that the contrasting responses of phenol oxidase to drainage are associated with the different plant species in wetlands.
Sphagnum and non-Sphagnum wetlands in China (by Yunpeng Zhao)
The Journal: A Nationwide, Pairwise Survey of Typical Wetlands Across China
To test our hypothesis, we initially surveyed three Sphagnum wetlands and three non-Sphagnum wetlands in China that had experienced drainage by ditching in the past few decades. As expected, we observed significant differences in phenol oxidase responses to drainage between the Sphagnum and non-Sphagnum wetlands. While the preliminary result was promising, my supervisor, Professor Xiaojuan Feng, argued that we still could not prove the prevalence and robustness of the contrasts. The limited number of sites may not adequately represent wetland types in China and the underlying mechanisms remained unclear. We needed more wetlands and samples to comprehensively evaluate what caused the divergent enzymatic responses.
Therefore, from 2020 to 2023, we conducted a nationwide, pairwise survey of enzymatic activity in the drained vs. waterlogged areas of typical wetlands across China. The task was challenging, as we targeted at representative wetlands in China that had experienced long-term drainage yet with minimal human disturbances otherwise. We carried out extensive surveys, a thorough review of the literature, consultation with local government departments as well as on-site field trip to obtain the required information. Through these efforts, we identified 30 wetlands spanning diverse climatic zones and landscapes (including 14 Sphagnum and 16 non-Sphagnum wetlands). Most sites were located within natural reserves, where human disturbance was minimal after drainage (by ditching for 15–55 years). Long-term drainage has significantly altered plant communities so that we could select drained vs. waterlogged sites based on differences in water-table levels and plant community composition (including xerophytes or mesophytes). To minimize environmental variations other than hydrology, we controlled the distance to 100–800 meters between the drained and waterlogged sites at each wetland. These efforts yielded a unique sample set for our study.
Sampling sites and experimental design
During the wetland survey and sampling, we had to deal with challenging field conditions (summer heat, heavy rainfall, and mosquitoes) as well as unexpected restrictions. We often had to change our travelling plan due to a sudden outbreak of COVID locally. Nonetheless, the three-year investigation was immensely valuable, not only for advancing our study but also for witnessing the diversity and characteristics of wetlands in China. The diversity of wetlands, natural landscapes and phenomena was impressive, including the people, culture, plants, animals and sceneries. This field work answered lots of our prior questions and curiosities, including the one that had puzzled us for so long.
The first day: We are equipped! This will be simple. We are going to collect samples!
The next few days: Things are not so simple…
The Discovery: Plant-Microbe Interactions in Wetlands
The central conclusion from our field survey and metagenomic analyses is that microbes rather than oxygen content control phenol oxidative activity after long-term wetland drainage. This conclusion does not seem surprising, as microbes produce and regulate extracellular enzymes in the long term. However, importantly, we provide evidence that the response of phenol oxidase-producing microbes to drainage is linked to plant communities and their secondary metabolites. Specifically, 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.
Pathways regulating enzymatic response to long-term drainage
Implications and Challenges
Our findings reconcile the discrepancy of phenol oxidase responses to drainage across different timescales and wetland types. We also suggest divergent vulnerability to drainage for carbon stocks in Sphagnum vs. non-Sphagnum wetlands, given that phenol oxidase plays a central role in carbon degradation and regulating hydrolase activity in these organics-rich environments. “Our study highlights that trait-based plant dynamics are pivotal to decipher wetland carbon dynamics and feedback to climate change under shifting hydrological regimes”, said Prof. Xiaojuan Feng.
Nonetheless, some challenges remain. Although our surveyed sites included typical wetlands in China, wetlands with thick peat layers and dominated by woody species were not included. The latter is widespread in boreal North America and Europe. As woody species may possess a different spectrum of secondary metabolites compared with herbaceous plants, plant-microbe interactions and effects on carbon decomposition in these wetlands deserve further investigation following drainage.
The Research Group
We are “Carbon Cycling and Organic Geochemistry Research Group” from the Institute of Botany, Chinese Academy of Sciences, led by Prof. Xiaojuan Feng (https://www.researchgate.net/profile/Xiaojuan-Feng-4). Our research focuses on investigating the transformation and transport of terrestrial organic matter under global changes and on assessing biogeochemical processes that affect terrestrial carbon cycling. In particular, we combine molecular-level techniques (including biomarkers, compound-specific 13C and 14C analysis) with landscape-scale experiments and sampling to examine environmental controls on the distribution and transformation of organic carbon in soils and aquatic systems.
Carbon Cycling and Organic Geochemistry Research Group
Contributors: Yunpeng Zhao and Prof. Xiaojuan Feng