Benthic macrofauna and microbiota mediate bottom trawling impacts on long-term carbon storage in marine sediments

The seafloor is the largest carbon sink on Earth and plays a pivotal role in the carbon cycle. Benthic fauna and microbiota influence sedimentary organic matter (SOM) through various processes, resulting in partial remineralization to carbon dioxide and its release into the atmosphere. Bottom trawling, a widespread fishing practice, threatens long-term OM storage in the seafloor by physically remixing surface sediments and remobilizing OM. Additionally, trawling alters faunal and microbial communities and their diversity, yet the consequences of these biotic changes for SOM dynamics are only poorly understood. We generated a regional-scale dataset of paired macrofaunal and microbial communities in the North Sea and used structural equation modeling to assess how bottom trawling and the benthic biota jointly influence SOM. Bottom trawling impacted SOM directly through mechanical disturbance of the sediment but also indirectly by disturbing ecological interactions among benthic fauna and microbiota. The indirect impacts of trawling are complex and their combined effect on SOM is negative, explaining about one third of the overall trawling-induced SOM loss. While SOM loss was associated with increased microbial aerobic respiration potential, SOM increased with microbial assimilation processes, including dark carbon fixation. Benthic microbial community structure shaped SOM directly while macrofaunal impacts on SOM were indirect and mediated by microbiota as the macrofaunal communities strongly influenced benthic microbiota. Several traits related to bioturbation and faunal diversity promoted shifts in benthic microbiota that favor SOM. Our findings underscore the importance of ecological mechanisms in carbon sequestration and call for better integration of benthic biodiversity and ecological processes into assessments of seafloor carbon storage under anthropogenic pressures. SIGNIFICANCE STATEMENTThe seafloor stores large quantities of organic carbon, thereby essentially contributing to the regulation of Earths climate. However, human activities, such as bottom trawling, can compromise this function. Our study demonstrates that the impacts of bottom trawling on carbon storage extend beyond physical sediment disturbance. By altering benthic faunal and microbial communities, trawling disrupts ecological interactions that favor carbon storage. Using a regional-scale dataset from the North Sea and structural equation modeling, we demonstrate that microbial communities directly influence sedimentary organic matter dynamics, whereas faunal impacts are largely indirect through the effects of macrofaunal biodiversity and bioturbation on microbiota. These findings highlight that biodiversity and ecological mechanisms are central to maintaining ocean carbon sinks and should be considered for the assessment of trawling impacts on seafloor carbon storage.