Abstract. Sponges are commonly known as general nutrient providers for the marine ecosystem, recycling organic matter into various forms of bio-available 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 15NO3- – amended oxygen saturated seawater, mimicking conditions in pumping sponges, and de-oxygenated seawater, mimicking non-pumping sponges. Rates of anaerobic ammonium oxidation (anammox) using incubations with 15NH4+ could not be detected. Denitrification rates of the different sponge species ranged from 0 to 114 nmol N cm-3 sponge day-1 under oxic conditions, and from 47 to 342 nmol N cm-3 sponge day-1 under anoxic conditions. An exponential 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 both prepared and optimized 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. High rates for coupled nitrification-denitrification (up to 89 % of nitrate reduction in the presence of oxygen) shows that under these conditions, the NO3- reduced in denitrification was primarily derived from nitrification within the sponge, directly coupling organic matter degradation and nitrification to denitrification in sponge tissues. Under anoxic condition when nitrification was not possible, nitrate to fuel the much higher denitrification rates had to be retrieved directly from the seawater. 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 of its origin, is then no longer available as a nutrient for the marine ecosystem. Considering average sponge biomasses on typical boreal and Arctic sponge grounds, our sponge denitrification rates reveal areal denitrification rates of 0.8 mmol N m-2 day-1 assuming non-pumping sponges and still 0.3 mmol N m-2 day-1 assuming pumping sponges. This is well within the range of denitrification rates of continental shelf sediments. For the most densely populated boreal sponge grounds we calculated denitrification rates of up to 2 mmol N m-2 day-1, which is comparable to rates in coastal sediments. Increased future impact of sponge grounds by anthropogenic stressors reducing sponge pumping activity and further stimulating sponge anaerobic processes may thus lead to that deep-sea sponge grounds change their role in the marine ecosystem from nutrient sources to nutrient sinks.
Highly diverse Asgard archaea participate in organic matter degradation in coastal sediments
