Nutrient loading decreases blue carbon by mediating fungi activities within seagrass meadows

Coastal pollution, including nutrient loading, can negatively impact seagrass health and cover and may consequently alter soil organic carbon (SOC) accumulation and preservation. Key to understanding how eutrophication impacts SOC cycling in seagrass ecosystems is how nutrient loading changes the sources of carbon being deposited and how these changes in resources, both nutrients and carbon availability, influence soil microbiota community and activity. Currently, the direction and magnitude of nutrient loading impacts on seagrass SOC dynamics are poorly understood at a meadow scale, limiting our ability to reveal the driving mechanisms of SOC remineralisation. The purpose of this study was to assess the response of surface SOC and soil microbiomes to nutrient loading within tropical seagrass meadows. To achieve this, we quantified both total SOC and recalcitrant soil organic carbon (RSOC) concentrations and sources, in addition to the composition of bacterial and fungal communities and soil extracellular enzyme activities. We found that nutrient loading elevated SOC and RSOC content, mainly facilitated by enhanced algal growth. There was no nutrient effect on the soil prokaryotic communities, however, saprotrophic fungi groups (i.e. Trapeliales, Sordaridales, Saccharomycetales and Polyporales) and fungal activities were elevated under high nutrient conditions, including extracellular enzyme activities linked to seagrass-based cellulose and lignin decomposition. This relative increase in RSOC transformation may decrease the relative contribution of seagrass carbon to RSOC pools. Additionally, significantly different fungal communities were observed between adjacent T. hemprichii and E. acoroides areas, which coincided with elevated RSOC-decomposing enzyme activity in T. hemprichii meadows, even though the mixed seagrass meadow received allochthonous SOC and RSOC from the same sources. These results suggest that nutrient loading stimulated fungal activity and community shifts specific to the local seagrass species, thereby causing fine-scale (within-meadow) variability in SOC cycling in response to nutrient loading. This study provides evidence that fungal composition and activity, mediated by human activities (e.g. nutrient loading), can be an important influence on seagrass blue carbon accumulation and remineralisation.