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

Abstract

Deep-sea sponges create hotspots of biodiversity and biological activity in the otherwise barren deep-sea. However, it remains elusive how sponge hosts and their microbial symbionts acquire and process food in these food-limited environments. Therefore, we traced the processing (i.e. assimilation and respiration) of 13C- and 15N-enriched dissolved organic matter (DOM) and bacteria by three dominant North Atlantic deep-sea sponges: the high microbial abundance (HMA) demosponge Geodia barretti, the low microbial abundance (LMA) demosponge Hymedesmia paupertas, and the LMA hexactinellid Vazella pourtalesii. We also assessed the assimilation of both food sources into sponge- and bacteria-specific phospholipid-derived fatty acid (PLFA) biomarkers. All sponges were capable of assimilating DOM as well as bacteria. However, processing of the two food sources differed considerably between the tested species: the DOM assimilation-to-respiration efficiency was highest for the HMA sponge, yet uptake rates were 4–5 times lower compared to LMA sponges. In contrast, bacteria were assimilated most efficiently and at the highest rate by the hexactinellid compared to the demosponges. Our results indicate that phylogeny and functional traits (e.g., abundance of microbial symbionts, morphology) influence food preferences and diet composition of sponges, which further helps to understand their role as key ecosystem engineers of deep-sea habitats.

Subcellular view of host–microbiome nutrient exchange in sponges: insights into the ecological success of an early metazoan–microbe symbiosis

“…The role of host and microbiome in organic matter uptake DOM uptake DOM was rapidly incorporated by the HMA species P. angulospiculatus and the LMA species H. caerulea, and bulk rates of incorporation into sponge tissue (1.1-1.5 μmol C tracer /mmol C sponge /h and 0.4-0.6 μmol N tracer / Table S1 mmol N sponge /h; Additional file 2: Table S2) are in the range of rates presented for seven other tropical sponge species (0.3-1.2 μmol C tracer /mmol C sponge /h and 0.3-1.3 μmol N tracer /mmol N sponge /h) [30,37], confirming the viability of our tested sponges. These findings contribute to a growing body of evidence that DOM-feeding by sponges is not related to the abundance of spongeassociated microbes [8,38,49,50]. NanoSIMS analysis revealed that both symbionts and host choanocyte cells were actively involved in DOM uptake.…”

“…4h; Additional file 2: Table S1), indicating preferential utilisation of POMderived N by cells of the mesohyl and the mesohyl matrix, which consists primarily of the polypeptides collagen, galectin, and fibronectin-like molecules [66]. Taken together, our results suggest that POM represents a high-quality food source for host anabolism (which may include predation on microbial symbionts [39,67]), despite representing only a small portion of the natural organic matter pool and sponge diet [2,50].…”

Seasonal Variability in Near-bed Environmental Conditions in the Vazella pourtalesii Glass Sponge Grounds of the Scotian Shelf

“…Bacteria are expected to be an even more important food source than suspended particulate matter for some glass sponges and will be assimilated efficiently (Pile and Young, 2006;Kahn et al, 2015;Bart et al, 2020a). On the Scotian Shelf an important source of bacteria can be the resuspended sediments, which are 100-1000 times enriched in heterotrophic bacteria compared to the overlaying water (Kuwae and Hosokawa, 1999).…”

Bacterial precursors and unsaturated long-chain fatty acids are biomarkers of North-Atlantic deep-sea demosponges

“…barretti ( n = 6) individuals were obtained from the Barents Sea (70°47N 18°03'E) around 300 m water depth on a subsequent G.O. Sars expedition in August 2018 [ 28 ]. Norwegian research expeditions do not require special permits for sample collection in this region.…”