The Interplay of Macrofauna Functional Groups Shapes Nitrogen Cycling in Oligotrophic Estuarine Sediments

Abstract

The effects of single macrofauna species on benthic nitrogen (N) cycling has been extensively studied, whereas the effect of macrofauna communities on N-related processes remains poorly explored. In this study, we characterized benthic N-cycling in bioturbated sediments of an oligotrophic northern Baltic waters (Öre estuary). Solute fluxes and N transformations (N2 fixation, denitrification and DNRA) were measured in sediments and in macrofauna-bacteria holobionts to partition the role of three dominant macrofauna taxa (Limnecola balthica, Marenzelleria sp. and Monoporeia affinis) in shaping N-cycling, and to disentangle the contribution of different functional groups within the community. In the studied area, benthic macrofauna comprised a low diversity community with extremely high local dominance of three macrofauna taxa, which are widespread and dominant in the Baltic. The biomass of these three taxa in the benthic community explained up to 30% of variation in measured biogeochemical processes, confirming their role in ecosystem functioning. The results also show that these taxa significantly contributed to the benthic metabolism and N-cycling (direct effect) as well as reworked sediments with positive feedback to dissimilative nitrate reduction (indirect effect). Taken together, these functions promoted a re-use of nutrient at the benthic level, limiting net losses (e.g. denitrification) and effluxes to bottom water. Finally, the detection of multiple N transformations in dominating macrofauna holobionts suggested a community-associated active and versatile microbiome, which alternatively contributes to the biogeochemical processes. The present study highlights hidden and interactive effects among microbes and macrofauna, which should be considered in analysing benthic functioning.