Abstract

AbstractSponges 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 (O2) removal rates averaged 3.3 ± 2.8 μmol O2 g DWsponge h−1 (mean ± SD), live particulate (bacterio‐ and phytoplankton) organic carbon removal rates averaged 0.30 ± 0.39 μmol C g DWsponge h−1 and dissolved organic carbon (DOC) removal rates averaged 18.70 ± 25.02 μmol C g DWsponge 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.

Highlights

  • Oxygen removal rates The concentration of O2 in the incubation chambers linearly decreased with time for V. pourtalesii (t = 4.59, df = 7, p < 0.01), G. barretti (t = 3.69, df = 11, p < 0.01), G. atlantica (t = 5.11, df = 5, p < 0.01), C. zetlandica (t = 3.5, df = 3, p < 0.05), H. paupertas (t = 4.38, df = 2, p < 0.05) and A. spinispinosum, (t = 7.96, df = 5, p < 0.001) compared to seawater control incubations

  • For the four assessed species, more than 90% of the average net total organic carbon (TOC) removal was accounted for by dissolved organic carbon (DOC) (V. pourtalesii 92.0 Æ 5.5%, G. barretti 99.5 Æ 0.5%, G. atlantica 93.6 Æ 8.4%, A. spinispinosum 100%) (Table 4)

  • In this study we show, for the first time, that multiple, dominant, North-Atlantic deep-sea sponge species, irrespective of taxonomic class, growth form, and abundance of microbial symbionts, are capable of consuming ambient DOC, and that this consumed DOC—representing more than 90% of the total organic carbon uptake—is essential to satisfy their minimal respiratory demands

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Summary

Introduction

LMA sponges contain microbes with abundances and sizes comparable to ambient seawater (~ 0.5–1 × 106 cells mL−1), while HMA sponges can harbor up to four orders of magnitude more and generally much larger microbes (Vacelet and Donadey 1977; Reiswig 1981; Hentschel et al 2003) These symbionts are involved in various metabolic processes, including carbon (C) and nitrogen (N) metabolism (reviewed by Pita et al 2018). For some species DOM uptake has been suggested (Leys et al 2018), for others it was not found (Yahel et al 2007; Kahn et al 2015) These studies did not directly measure DOC, but derived the dissolved organic carbon fraction from the total organic carbon fraction. Direct DOC measurements are challenging, as they are performed almost within detection limits of current analytical systems

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