Deep-sea sponge grounds as nutrient sinks: denitrification is common in boreo-Arctic sponges
2020
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 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 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 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.
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