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An integrative model of carbon and nitrogen metabolism in a common deep-sea sponge (Geodia barretti)
de Kluijver, A.; Bart, M.C.; van Oevelen, D.; de Goeij, J.M.; Leys, S.P.; Maier, S.R.; Maldonado, M.; Soetaert, K.; Verbiest, S.; Middelburg, J.J. (2021). An integrative model of carbon and nitrogen metabolism in a common deep-sea sponge (Geodia barretti). Front. Mar. Sci. 7: 596251. https://hdl.handle.net/10.3389/fmars.2020.596251

Bijhorende data:
In: Frontiers in Marine Science. Frontiers Media: Lausanne. ISSN 2296-7745, meer
Peer reviewed article  

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Author keywords
    allometry; metabolic network model; sponge holobiont metabolism; production; biogeochemistry; chemoautotrophy; sponge ground; LIM

Auteurs  Top 
  • de Kluijver, A., meer
  • Bart, M.C.
  • van Oevelen, D., meer
  • de Goeij, J.M.
  • Leys, S.P.
  • Maier, S.R., meer
  • Maldonado, M.
  • Soetaert, K., meer
  • Verbiest, S.
  • Middelburg, J.J., meer

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−3NO3-). 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 thevariability in metabolic rates partially resulted from body size as O 2 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−3NO3- reduction to ammonium (NH+4)NH4+) (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+4NH4+ 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 comparedto 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.


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