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 15 NO − 3amended 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 15 NH + 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 speciesspecific 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 15 N-labelled N 2 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 nonpumping 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.

Benthic Communities on the Mohn’s Treasure Mound: Implications for Management of Seabed Mining in the Arctic Mid-Ocean Ridge

“…The potential exploitation of mineral resources in the region may result in harmful effects on the crinoid and sponge communities that we observed and on the ecosystem services they provide, such as nutrient regeneration and habitat provision. For example, close associations between ground-forming sponges and specialized microbes have proven to be key players in the biogeochemical cycling of nutrients along the ridge (Rooks et al, 2020). Stressors such as enhanced sedimentation or release of bioavailable metals caused by commercially exploited seabed minerals may have serious effects on ecosystem function, potentially changing these sponge communities from being nutrient sources to nutrient sinks (Rooks et al, 2020).…”

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

“…Some sponge grounds consisting essentially of an assemblage of deep-water astrophorid demosponges have shown high denitrification activity (i.e., similar in rate values to those of marine sediments). Denitrification in those astrophorid grounds was so intense that the sponges were estimated to incorporate a large part of the nitrate available in the seawater of their habitat (Rooks et al, 2020). From the available results in V. pourtalesii, the conventional coupling of nitrification to denitrification through nitrate does not appear to happen (Figure 6): the nitrifying enzymes for the conversion of nitrite into nitrate are missing.…”

An Integrative Model of Carbon and Nitrogen Metabolism in a Common Deep-Sea Sponge (Geodia barretti)

“…In G. barretti, the microbiome is actively involved in the (re)cycling of C and N compounds and, therefore impacts the holobiont nutrition (Hoffmann et al, 2009;Leys et al, 2018;Bart et al, 2020a). As for many sponge species, anaerobic and aerobic N-transforming processes occur in G. barretti, thereby expanding its metabolic capacity (Hoffmann et al, 2009;Rooks et al, 2020). It has been hypothesized that G. barretti actively controls the oxygenation level of its tissue to maintain aerobic and anaerobic microenvironments that facilitate the co-existence of aerobic and anaerobic symbionts (Hoffmann et al, 2005).…”