An Integrative Model of Carbon and Nitrogen Metabolism in a Common Deep-Sea Sponge (Geodia barretti)

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 (O 2 ) and net release of nitrate ( <mml:math xmlns:mml="http://www.w3.org/1998/Math/MathML" id="INEQ1"><mml:msubsup><mml:mtext>NO</mml:mtext><mml:mn>3</mml:mn><mml:mo>-</mml:mo></mml:msubsup></mml:math> ). 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 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 <mml:math xmlns:mml="http://www.w3.org/1998/Math/MathML" id="INEQ2"><mml:msubsup><mml:mtext>NO</mml:mtext><mml:mn>3</mml:mn><mml:mo>-</mml:mo></mml:msubsup></mml:math> reduction to ammonium ( <mml:math xmlns:mml="http://www.w3.org/1998/Math/MathML" id="INEQ3"><mml:mrow><mml:msubsup><mml:mtext>NH</mml:mtext><mml:mn>4</mml:mn><mml:mo>+</mml:mo></mml:msubsup><mml:mo stretchy="false">)</mml:mo></mml:mrow></mml:math> (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 (CO 2 ), which was released in a net ratio of 0.77–0.81 to O 2 consumption. Internally produced <mml:math xmlns:mml="http://www.w3.org/1998/Math/MathML" id="INEQ4"><mml:msubsup><mml:mtext>NH</mml:mtext><mml:mn>4</mml:mn><mml:mo>+</mml:mo></mml:msubsup></mml:math> 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.

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