Dissolved organic carbon (DOC) is essential to balance the metabolic demands of North-Atlantic deep-sea sponges

Abstract

Sponges are ubiquitous components of various deep-sea habitats, including cold water coral reefs and deep-sea sponge grounds. Despite being surrounded by oligotrophic waters, these ecosystems are known to be hotspots of biodiversity and carbon cycling. To assess the role of sponges in the carbon cycling of deep-sea ecosystems, we studied the energy budgets of six dominant deep-sea sponges (the hexactinellid species Vazella pourtalesi, and demosponge species Geodia barretti, Geodia atlantica, Craniella zetlandica, Hymedesmia paupertas and Acantheurypon spinispinosum) in an ex situ aquarium setup. Additionally, we determined morphological metrics for all species (volume, dry weight (DW), wet weight (WW), carbon (C) content, and ash-free dry weight (AFDW)) and provide species-specific conversion factors. Oxygen (O2) removal rates averaged 3.3 ± 2.8 µmol O2 DWsponge h−1 (all values mean ± SD), live particulate (bacterial and phytoplankton) organic carbon (LPOC) removal rates averaged 0.30 ± 0.39 µmol C DWsponge h−1 and dissolved organic carbon (DOC) removal rates averaged 18.70 ± 25.02 µmol C DWsponge h−1. Carbon mass balances were calculated for four species (V. pourtalesi, G. barretti, G. atlantica and H. paupertas) and revealed that the sponges acquired 1.3–6.6 times the amount of carbon needed to sustain their minimal respiratory demands. These results indicate that irrespective of taxonomic class, growth form, and abundance of microbial symbionts, DOC is responsible for over 90 % of the total net organic carbon removal of deep-sea sponges and allows them to sustain in otherwise food-limited environments on the ocean floor.

Differential processing of dissolved and particulate organic matter by deep-sea sponges and their microbial symbionts

“…assimilation and respiration) of a dissolved (DOM) and a particulate (bacteria) food source for a selection of three dominant deep-sea sponges from two different phylogenetic classes that differ in functional traits, such as the abundance of microbial symbionts and morphology. Our results corroborate recent and increasing evidence 28,30,49 that DOM-processing is not restricted to high microbial (HMA) sponges as is commonly suggested 40,41,50 , but that low microbial abundance (LMA) sponges are capable of processing DOM at even higher rates than HMA species. However, the HMA sponge in this study, Geodia barretti, did show the highest assimilation-to-respiration efficiency of DOM, i.e.…”

“…This corroborates earlier findings that sponges, and hexactinellids in particular, are very efficient in filter-feeding and assimilating (tracer) bacteria 18,42 . Still, DOM potentially constitutes a much larger proportion of their daily diet than bacteria 28 , mainly due to the order of magnitude higher ambient concentration of DOM-derived C and N in seawater 35 . The different assimilation-to-respiration efficiencies of DOM versus bacteria suggest that food sources may serve different purposes for sponge nutrition as was previously hypothesized by Refs.…”

“…In general, sponges are efficient filter-feeders that utilize a wide variety of particulate food sources ranging from bacterio-and phytoplankton to detrital particles, and even zooplankton 18,26,27 . Moreover, in recent years it has become increasingly evident that many sponges, including dominant North Atlantic deep-sea species 28,29 , use dissolved organic matter (DOM) as main food source 30 . DOM constitutes the largest pool of reduced carbon in the ocean, and is therefore the largest potential marine organic food source 31 .…”

“…Sponges with high abundances of associated microbes (HMA; species-specific microbial communities with up to four orders of magnitude higher bacterial concentrations than the surrounding sea water) were suggested to be better equipped to utilize DOM, than those with low microbial abundances (LMA; community composition and abundances of microbes similar to surrounding sea water) [39][40][41] . However, recent evidence from complementary studies using different approaches suggests that microbial abundance may not determine the capacity of sponges to feed on DOM, since many LMA sponges were found to take up DOM 29,35,36,42 and some even at higher uptake rates than HMA sponges 28,43,44 . Furthermore, DOM has been shown to be assimilated by both sponge host and bacterial symbiont cells 42,44 , ultimately visualized at a (sub) cellular level 45,46 .…”

“…Indeed, first evidence of four dominant North-Atlantic sponge species, including one massive vase-shaped LMA hexactinellid, one encrusting sheet-shaped LMA and two massive ball-shaped HMA demosponges, showed that none of these species could acquire sufficient carbon from particulate organic matter (POM) food sources alone to meet their respiratory demand. Instead, all tested species relied on DOM to balance their metabolic requirements 28 . However, no information is yet available on the role of the animal host versus its symbionts in the processing of particulate and dissolved organic food sources, which hampers our understanding of different strategies these deep-sea sponges may have to acquire food.…”