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

Abstract

Sponges are ubiquitous components of various deep-sea habitats, including cold water coral reefs, and form deep-sea sponge grounds. Although the deep sea is generally considered to be a food-limited environment, 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 carbon budgets of six dominant deep-sea sponges of different phylogenetic origin, with various growth forms and hosting distinct associated microbial communities, in an ex situ aquarium setup. Additionally, we determined biomass metrics-planar surface area, volume, wet weight, dry weight (DW), ash-free dry weight, and organic carbon (C) content-and conversion factors for all species. Oxygen (O 2) removal rates averaged 3.3 ± 2.8 μmol O 2 g DW sponge h −1 (mean ± SD), live particulate (bacterio-and phytoplankton) organic carbon removal rates averaged 0.30 ± 0.39 μmol C g DW sponge h −1 and dissolved organic carbon (DOC) removal rates averaged 18.70 ± 25.02 μmol C g DW sponge h −1. Carbon mass balances were calculated for four species 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 themselves in otherwise food-limited environments on the ocean floor.

A Microbial Nitrogen Engine Modulated by Bacteriosyncytia in Hexactinellid Sponges: Ecological Implications for Deep-Sea Communities

“…The detection of prokaryotic glutamine synthetase and glutamate dehydrogenase in the MAGs ( Supplementary Table 4A) suggests that a large part of the microbiota N assimilation occurs through ammonification of ammonia to produce basic amino acids, as already concluded for the SAR3254 symbiont in a previous study of V. pourtalesii (Bayer et al, 2020). The recent finding that V. pourtalesii covers its energetic demands mostly (90%) through uptake of dissolved organic carbon (DOC) rather than through filter feeding (10%) of bacterioplankton and other particulate carbon (Bart et al, 2020) also suggests that a substantial part of the DOC taken up by the sponges could indeed not be used by the sponge cells themselves but running through the assimilation pathway of the microbiota (Figure 6), as it has also been shown for some HMA demosponges (Rix et al, 2020).…”

“…A poor free-living bacterioplankton community in the demersal water mass around the aggregations of V. pourtalesii would decrease the feeding chances for those sponge species that do not farm their bacteria internally but that rather rely on the filter feeding of external bacterioplankton and picophytoplankton. In line with this view, it has recently being found (Bart et al, 2020) that the bulk energy for the aerobic metabolism of V. pourtalesii is not provided by the filter-feeding of the free-living bacterioplankton (only about 10%). Rather, the sponge appears to largely rely on the uptake of dissolved organic matter (about 90%), a carbon source that can be likely processed by both the internal microbiota and the sponge cells (Figure 6), as also demonstrated for demosponges (Rix et al, 2020).…”

The Hexactinellid Deep-Water Sponge Vazella pourtalesii (Schmidt, 1870) (Rossellidae) Copes With Temporarily Elevated Concentrations of Suspended Natural Sediment

“…No deleterious effects of microbubble exposure were evident in the control sponges upon the start of the experiment. We subsequently acquired control data on the respiration and clearance rate from colleagues working on this same species in the same aquaria facilities at another time (Bart et al, 2020) in order to compare these rates with our potentially compromised control sponges.…”

“…Wet mass was measured on a scale after taking the sponge out of the water and allowing the water to drain for 10 s. Volume of individual sponges was measured by water replacement in a graded beaker prior to sampling for microscopy approaches (see section "Recovery Potential and Electron Microscopy"). To make the rates assessed in this study comparable to published datasets, we used the conversion factor (mL:gDM = 5.2) from Bart et al (2020) to calculate dry mass from sponge volume. Water samples were drawn from the chamber at the beginning and the end of the 4 h incubations via tubes inserted through the lid.…”

“…have been compromised in their physiological performance. For this reason, data from the control group evaluated in this study were augmented by a published dataset (Bart et al, 2020) on the physiological rates of V. pourtalesii. Respiration and clearance rates of V. pourtalesii described by Bart et al (2020) (n = 7) were assessed in a similar manner as in this study (chamber-based incubations) and were performed in the same aquaria facilities.…”