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Dissolved organic carbon (DOC) is essential to balance the metabolicdemands of four dominant North-Atlantic deep-sea sponges

Bart, Martijn C; Mueller, Benjamin; Rombouts, Titus; van de Ven, Clea; Tompkins, Gabrielle J; Osinga, Ronald; Brussaard, Corina PD; MacDonald, Barry; Engel, Anja; Rapp, Hans Tore; de Goeij, Jasper M

ABSTRACT

Sponges are ubiquitous components of various deep-sea habitats, including cold water coral reefs and deep-sea sponge grounds. Despite being surrounded by oligotrophic waters, these ecosystems are known to be hotspots of biodiversity and carbon cycling. To assess the role of sponges in the carbon cycling of deep-sea ecosystems, we studied the energy budgets of six dominant deep-sea sponges (the hexactinellid species Vazella pourtalesi, and demosponge species Geodia barrettiGeodia atlanticaCraniella zetlandicaHymedesmia paupertas and Acantheurypon spinispinosum) in an ex situ aquarium setup. Additionally, we determined morphological metrics for all species (volume, dry weight (DW), wet weight (WW), carbon (C) content, and ash-free dry weight (AFDW)) and provide species-specific conversion factors. Oxygen (O2) removal rates averaged 3.3 ± 2.8 µmol O2 DWsponge h−1 (all values mean ± SD), live particulate (bacterial and phytoplankton) organic carbon (LPOC) removal rates averaged 0.30 ± 0.39 µmol C DWsponge h−1 and dissolved organic carbon (DOC) removal rates averaged 18.70 ± 25.02 µmol C DWsponge h−1. Carbon mass balances were calculated for four species (V. pourtalesiG. barrettiG. atlantica and H. paupertas) and revealed that the sponges acquired 1.3–6.6 times the amount of carbon needed to sustain their minimal respiratory demands. These results indicate that irrespective of taxonomic class, growth form, and abundance of microbial symbionts, DOC is responsible for over 90 % of the total net organic carbon removal of deep-sea sponges and allows them to sustain in otherwise food-limited environments on the ocean floor.

ACKNOWLEDGEMENTS We want to dedicate this publication to our EU Horizon 2020 SponGES project coordinator and co‐author Prof. Hans Tore Rapp, who sadly, and too soon, passed on March 7, 2020. We want to thank all our collaborators within the EU Horizon 2020 SponGES project. Dr. Ellen Kenchington at the Bedford Institute of Oceanography (BIO), Nova Scotia, Canada, and the Department of Biological Sciences at the University of Bergen, Norway, for the use of facilities and equipment. Many thanks to the ROV crews of both the ÆGIR 6000 in Norway and the Deep Sea Systems International Oceaneering in Canadian waters, for their careful collection of the sponges. DFO provided the ship time on the CCGS Hudson for the collection of the V. pourtalesii individuals and we thank Dr. Ellen Kenchington for collecting the sponges at sea under less than ideal conditions. We further thank Dr. L. Woodall, NEKTON, for providing the ROV for the collection of the V. pourtalesii. Thanks to Erik Wurz for his help maintaining the onboard aquaria. We also thank Jorien Schoorl and Rutger van Hall for their technical assistance at the University of Amsterdam, Niklas Kornder and Dr. Emiel van Loon for their advice on the statistical analysis, Heikki Savolainen for his technical support at the University of Bergen, Dr. Alice Ortmann (BIO), Anna Noordeloos (NIOZ) and Santiago Gonzalez (NIOZ) for their help with the flow cytometry analysis, and Jon Roa at GEOMAR for the analysis of the DOC samples. This project has received funding from the European Research Council under the European Union's Horizon 2020 research and innovation programme (SponGES grant agreement n° 679849 and ERC starting grant agreement n° 715513 to J.M. de Goeij). Additionally, this project has received funding from the KNAW Academy Ecology fund in 2017 and 2018 (personal grant to M.C. Bart). Salary for Gabrielle Tompkins was funded through the Canadian Department of Fisheries and Oceans (DFO) International Governance Strategy internal funding awarded to Dr. Ellen Kenchington (DFO, BIO). This document reflects only the authors' views and the Executive Agency for Small and Medium‐sized Enterprises (EASME) is not responsible for any use that may be made of the information it contains.
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