Deep-sea sponge grounds as nutrient sinks: denitrification is common in boreo-Arctic sponges

ABSTRACT. Sponges are commonly known as general nutrient providers for the marine ecosystem, recycling organic matter into various forms of bioavailable nutrients such as ammonium and nitrate. In this study we challenge this view. We show that nutrient removal through microbial denitrification is a common feature in six cold-water sponge species from boreal and Arctic sponge grounds. Denitrification rates were quantified by incubating sponge tissue sections with ₁₅NO⁻³ - amended oxygen-saturated seawater, mimicking conditions in pumping sponges, and de-oxygenated seawater, mimicking non-pumping sponges. It was not possible to detect any rates of anaerobic ammonium oxidation (anammox) using incubations with ₁₅NH⁺⁴. Denitrification rates of the different sponge species ranged from below detection to 97 nmol N cm⁻³ sponge d⁻¹ under oxic conditions, and from 24 to 279 nmol N cm⁻³ sponge d⁻¹ under anoxic conditions. A positive relationship between the highest potential rates of denitrification (in the absence of oxygen) and the species-specific abundances of nirS and nirK genes encoding nitrite reductase, a key enzyme for denitrification, suggests that the denitrifying community in these sponge species is active and prepared for denitrification. The lack of a lag phase in the linear accumulation of the ₁₅N-labelled N₂ gas in any of our tissue incubations is another indicator for an active community of denitrifiers in the investigated sponge species. Low rates for coupled nitrification–denitrification indicate that also under oxic conditions, the nitrate used to fuel denitrification rates was derived rather from the ambient seawater than from sponge nitrification. The lack of nifH genes encoding nitrogenase, the key enzyme for nitrogen fixation, shows that the nitrogen cycle is not closed in the sponge grounds. The denitrified nitrogen, no matter its origin, is then no longer available as a nutrient for the marine ecosystem. These results suggest a high potential denitrification capacity of deep-sea sponge grounds based on typical sponge biomass on boreal and Arctic sponge grounds, with areal denitrification rates of 0.6 mmol N m⁻² d⁻¹ assuming non-pumping sponges and still 0.3 mmol N m⁻² d⁻¹ assuming pumping sponges. This is well within the range of denitrification rates of continental shelf sediments. Anthropogenic impact and global change processes affecting the sponge redox state may thus lead to deep-sea sponge grounds changing their role in marine ecosystem from being mainly nutrient sources to becoming mainly nutrient sinks.

DATA AVAILABILITY. The data are available in the data publisher PANGAEA, https://doi.pangaea.de/10.1594/PANGAEA.899821 (Rooks et al., 2019).

SUPPLEMENT. The supplement related to this article is available online at: https://doi.org/10.5194/bg-17-1231-2020-supplement.

ACKNOWLEDGMENTS. This study was performed in the scope of the SponGES project, which received funding from the European Union’s Horizon 2020 research and innovation programme under grant agreement no. 679849. This document reflects only the authors’ views and the Executive Agency for Small and Medium-sized Enterprises (EASME) is not responsible for any use that may be made of the information it contains.

FINANCIAL SUPPORT. This research has been supported by the Eu-ropean Union Horizon 2020 programme (grant no. 679849), the Norwegian Research Council (grant no. 225283), and the Norwegian National Research Infrastructure (grant no. 245907). Joana R. Xavier’s research is further supported by the strategic funding (grant no. UID/Multi/04423/2019) provided by the Portuguese Foundation for Science and Technology (FCT) to CIIMAR.