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

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 (NO3- ). 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 NO3- reduction to ammonium (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 O-2 consumption. Internally produced NH4+ 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.