Abstract
The effects of single macrofauna taxa on benthic nitrogen (N) cycling have been extensively studied, whereas how macrofaunal communities affect N-related processes remains poorly explored. In this study, we characterized benthic N-cycling in bioturbated sediments of the oligotrophic Öre Estuary (northern Baltic Sea). Solute fluxes and N transformations (N2 fixation, denitrification and dissimilative nitrate reduction to ammonium [DNRA]) were measured in sediments and macrofauna-associated microbes (holobionts) to partition the role of three dominant taxa (the filter feeder Limecola balthica, the deep deposit feeder Marenzelleria spp., and the surface deposit feeder Monoporeia affinis) in shaping N-cycling. In the studied area, benthic macrofauna comprised a low diversity community with dominance of the three taxa, which are widespread and dominant in the Baltic. The biomass of these taxa in macrofaunal community explained up to 30% of variation in measured biogeochemical processes, confirming their important 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 to sediments bioturbation with positive feedback to dissimilative nitrate reduction (indirect effect). Taken together, these functions promoted a reuse of nutrients at the benthic level, limiting net losses (e.g. denitrification) and effluxes to bottom water. Finally, the detection of multiple N transformations in macrofauna holobionts suggested a community-associated versatile microbiome, however, its role was of minor importance as compared to the activity of sediment-associated microbial communities. The present study highlights hidden and interactive effects among microbes and macrofauna, which should be considered analysing benthic functioning.
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Acknowledgements
We gratefully thank the staff at Umeå Marine Science Center (UMF) for hosting the INBALANCE Team, and for providing lab facilities and sampling boat. We kindly thank Jan Albertsson for precious suggestions while selecting sampling sites, Irma Vybernaitė-Lubienė, Saulė Medelytė, and Rūta Barisevičiūtė for laboratory analysis, Tobia Politi for data handling, and Bo Thamdrup for making mass spectrometry instrumentation available at University of Southern Denmark.
Funding
The study was supported by the “Invertebrate–Bacterial Associations as Hotpots of Benthic Nitrogen Cycling in Estuarine Ecosystems (INBALANCE)” project funded by the European Social Fund (Project No. 09.3.3-LMT-K-712-01-0069) under grant agreement with the Research Council of Lithuania (LMTLT). Additional support to S.B. was provided by the Swedish Research Council Formas (Project No. 2017-01513) and U.M. was supported by Grundfos Foundation.
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MZ, MB, UC and SB conceived the ideas and designed methodology; MZ, MB, DD, UM and UC carried out sampling and the incubation experiments; SB, GC and UM carried out the mass spectrometry analyses and animal measurements; UC, UM and SB led the data analysis; MZ and MB wrote the first draft of the manuscript. All authors contributed to the discussion and interpretation of data, and revised and approved the manuscript for submission.
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Zilius, M., Daunys, D., Bartoli, M. et al. Partitioning benthic nitrogen cycle processes among three common macrofauna holobionts. Biogeochemistry 157, 193–213 (2022). https://doi.org/10.1007/s10533-021-00867-8
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DOI: https://doi.org/10.1007/s10533-021-00867-8