Crab bioturbation alters nitrogen cycling and promotes nitrous oxide emission in intertidal wetlands: Influence and microbial mechanism

Highlights: • Nitrogen cycling in intertidal wetlands was accelerated by crab bioturbation. • Crab bioturbation promoted the N₂O emission in intertidal wetlands. • Crab activity caused a disproportionate increase in N₂O production over consumption. • The source of N₂O was altered by crab bioturbation in intertidal sediments. • Crab bioturbation increased the contribution of NH₂OH oxidation to N₂O production. Intertidal wetlands provide important ecosystem functions by acting as nitrogen (N) cycling hotspots, which can reduce anthropogenic N loading from land to coastal waters. Benthic bioturbations are thought to play an important role in mediating N cycling in intertidal marshes. However, how the burrowing activity of benthos and their microbial symbionts affect N transformation and greenhouse gas nitrous oxide (N₂O) emission remains unclear in these environments. Here, we show that bioturbation of crabs reshaped the structure of intertidal microbial communities and their N cycling function. Molecular analyses suggested that the microbially-driven N cycling might be accelerated by crab bioturbation, as the abundances of most of the N related functional genes were higher on the burrow wall than those in the surrounding bulk sediments, except for genes involved in N fixation, dissimilatory nitrate reduction to ammonium (DNRA), and N₂O reduction, which were further confirmed by isotope-tracing experiments. Especially, the potential rates of the main N₂O production pathways, nitrification and denitrification, were 2-3 times higher in the burrow wall sediments. However, even higher N₂O emission rates (approximately 6 times higher) were observed in this unique microhabitat, which was due to a disproportionate increase in N₂O production over N₂O consumption driven by burrowing activity. In addition, the sources of N₂O were also significantly affected by crab bioturbation, which increased the contribution of hydroxylamine oxidation pathway. This study reveals the mechanism through which benthic bioturbations mediate N cycling and highlights the importance of considering burrowing activity when evaluating the ecological function of intertidal wetlands.