10.3389/fmars.2020.596251
https://zenodo.org/records/4478428
oai:zenodo.org:4478428
de Kluijver, Anna
Anna
de Kluijver
Department of Earth Sciences, Faculty of Geosciences, Utrecht University, Utrecht, Netherlands
Bart, Martijn C
Martijn C
Bart
Department of Freshwater and Marine Ecology, Institute for Biodiversity and Ecosystem Dynamics, University of Amsterdam, Amsterdam, Netherlands
van Oevelen, Dick
Dick
van Oevelen
Department of Estuarine and Delta Systems, Royal Netherlands Institute for Sea Research (NIOZ) and Utrecht University, Yerseke, Netherlands
de Goeij, Jasper M
Jasper M
de Goeij
Department of Freshwater and Marine Ecology, Institute for Biodiversity and Ecosystem Dynamics, University of Amsterdam, Amsterdam, Netherlands
Leys, Sally P
Sally P
Leys
Department of Biological Sciences, University of Alberta, Edmonton, AB, Canada
Maier, Sandra R
Sandra R
Maier
Department of Estuarine and Delta Systems, Royal Netherlands Institute for Sea Research (NIOZ) and Utrecht University, Yerseke, Netherlands
Maldonado, Manuel
Manuel
Maldonado
Center for Advanced Studies of Blanes (CEAB), Spanish National Research Council (CSIC), Girona, Spain
Soetaert, Karline
Karline
Soetaert
Department of Earth Sciences, Faculty of Geosciences, Utrecht University, Utrecht, Netherlands; Department of Estuarine and Delta Systems, Royal Netherlands Institute for Sea Research (NIOZ) and Utrecht University, Yerseke, Netherlands
Verbiest, Sander
Sander
Verbiest
Department of Earth Sciences, Faculty of Geosciences, Utrecht University, Utrecht, Netherlands
Middelburg, Jack J
Jack J
Middelburg
Department of Earth Sciences, Faculty of Geosciences, Utrecht University, Utrecht, Netherlands
An Integrative Model of Carbon and Nitrogen Metabolism in a Common Deep-Sea Sponge (Geodia barretti)
Zenodo
2021
allometry
metabolic network model
sponge holobiont metabolism
production
biogeochemistry
chemoautotrophy
sponge ground
LIM
European Union (EU)
Horizon 2020
Grant Agreement No 679849
Deep-sea Sponge Grounds Ecosystems of the North Atlantic: an integrated approach towards their preservation and sustainable exploitation
SponGES
2021-01-18
https://www.frontiersin.org/articles/10.3389/fmars.2020.596251/full#fun1
https://www.frontiersin.org/articles/10.3389/fmars.2020.596251/full#supplementary-material
https://zenodo.org/communities/sponges
https://zenodo.org/communities/eu
Creative Commons Attribution 4.0 International
ABSTRACT
Deep-sea sponges and their microbial symbionts transform various forms of carbon (C) and nitrogen (N) via several metabolic pathways, which, for a large part, are poorly quantified. Previous flux studies on the common deep-sea sponge Geodia barretti consistently revealed net consumption of dissolved organic carbon (DOC) and oxygen (O2) and net release of nitrate (NO−3). Here we present a biogeochemical metabolic network model that, for the first time, quantifies C and N fluxes within the sponge holobiont in a consistent manner, including many poorly constrained metabolic conversions. Using two datasets covering a range of individual G. barretti sizes (10–3,500 ml), we found that the variability in metabolic rates partially resulted from body size as O2 uptake allometrically scales with sponge volume. Our model analysis confirmed that dissolved organic matter (DOM), with an estimated C:N ratio of 7.7 ± 1.4, is the main energy source of G. barretti. DOM is primarily used for aerobic respiration, then for dissimilatory NO−3 reduction to ammonium (NH+4) (DNRA), and, lastly, for denitrification. Dissolved organic carbon (DOC) production efficiencies (production/assimilation) were estimated as 24 ± 8% (larger individuals) and 31 ± 9% (smaller individuals), so most DOC was respired to carbon dioxide (CO2), which was released in a net ratio of 0.77–0.81 to O2 consumption. Internally produced NH+4 from cellular excretion and DNRA fueled nitrification. Nitrification-associated chemoautotrophic production contributed 5.1–6.7 ± 3.0% to total sponge production. While overall metabolic patterns were rather independent of sponge size, (volume-)specific rates were lower in larger sponges compared to smaller individuals. Specific biomass production rates were 0.16% day–1 in smaller compared to 0.067% day–1 in larger G. barretti as expected for slow-growing deep-sea organisms. Collectively, our approach shows that metabolic modeling of hard-to-reach, deep-water sponges can be used to predict community-based biogeochemical fluxes and sponge production that will facilitate further investigations on the functional integration and the ecological significance of sponge aggregations in deep-sea ecosystems.
ACKNOWLEDGEMENTS
Titus Rombouts and Pieter Slot (UvA) and Sharyn Ossebaar (NIOZ) are acknowledged for their analytical assistance with the nutrient measurements of the incubation experiments. We thank Asimenia Gavriilidou and Detmer Sipkema (WUR, SponGES) for their input on the microbial genome in G. barretti. We thank last Hans Tore Rapp (UiB) for the excellent project coordination. We would like to thank CF and CR for their valuable and constructive reviews.
AUTHOR CONTRIBUTIONS
AK developed the model, performed the data analyses and model analyses, prepared the figures, and wrote the manuscript. MB and JG designed and conducted the incubation experiments, performed nutrient analyses, and contributed to the writing of the manuscript. SV contributed to model conceptualization and development. JM acquired funding and contributed to the conceptualization of the model, interpretation, and writing of the manuscript. MM contributed to the conceptualization of the model, interpretation, and writing. SL and SM contributed data for model development. KS contributed technically with model implementation and analyses. DO designed the model, contributed to model development and interpretation, and writing of the manuscript. All authors contributed to the article and approved the submitted version.
SUPPLEMENTARY MATERIAL
The Supplementary Material for this article can be found online at: https://www.frontiersin.org/articles/10.3389/fmars.2020.596251/full#supplementary-material
CONFLICT OF INTEREST
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
DATA AVAILABILITY STATEMENT
The dataset of Leys et al. (2018) is available at University of Alberta Education and Research Archive: doi: 10.7939/R3057D48V. The dataset of Bart et al. (2020b) will be made available at Pangaea. The model input files and R scripts are available on Zenodo: doi: 10.5281/zenodo.4139792.
FUNDING
This research has been performed in the scope of the EU SponGES project, which received funding from the European Union's Horizon 2020 Research and Innovation Program under grant agreement no. 679849. Further support included ERC starting grant agreement no. 715513 to JG and the Netherlands Earth System Science Center to JM. 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.
European Commission
10.13039/501100000780
679849
Deep-sea Sponge Grounds Ecosystems of the North Atlantic: an integrated approach towards their preservation and sustainable exploitation