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 ((Formula presented.)). 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 (Formula presented.) reduction to ammonium ((Formula presented.) (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 (Formula presented.) 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.

Original languageEnglish
Article number596251
Pages (from-to)1-18
Number of pages18
JournalFrontiers in Marine Science
Volume7
DOIs
Publication statusPublished - 18 Jan 2021

Bibliographical note

Funding Information:
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.

Funding Information:
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. 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.

Publisher Copyright:
© Copyright © 2021 de Kluijver, Bart, van Oevelen, de Goeij, Leys, Maier, Maldonado, Soetaert, Verbiest and Middelburg.

Keywords

  • LIM
  • allometry
  • biogeochemistry
  • chemoautotrophy
  • metabolic network model
  • production
  • sponge ground
  • sponge holobiont metabolism

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