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

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 fea...

Full description

Bibliographic Details
Published in:Biogeosciences
Main Authors: Rooks, C, Fang, JKH, Morkyed, PT, Zhao, R, Rapp, HT, Xayier, JR, Hoffmann, F
Format: Article in Journal/Newspaper
Language:English
Published: Copernicus GmbH 2020
Subjects:
Online Access:http://hdl.handle.net/10397/82269
https://doi.org/10.5194/bg-17-1231-2020
id ftpolyuhongkong:oai:ira.lib.polyu.edu.hk:10397/82269
record_format openpolar
spelling ftpolyuhongkong:oai:ira.lib.polyu.edu.hk:10397/82269 2023-05-15T14:59:45+02:00 Deep-sea sponge grounds as nutrient sinks: denitrification is common in boreo-Arctic sponges Rooks, C Fang, JKH Morkyed, PT Zhao, R Rapp, HT Xayier, JR Hoffmann, F 2020 http://hdl.handle.net/10397/82269 https://doi.org/10.5194/bg-17-1231-2020 en eng Copernicus GmbH Biogeosciences Biogeosciences, 6 Mar. 2020, v. 17, no. 5, p. 1231-1245 1726-4170 http://hdl.handle.net/10397/82269 1231 1245 17 5 doi:10.5194/bg-17-1231-2020 WOS:000518835100001 2-s2.0-85081250951 1726-4189 © Author(s) 2020. This work is distributed under the Creative Commons Attribution 4.0 License (https://creativecommons.org/licenses/by/4.0/). The following publication Rooks, C., Fang, J. K. H., Mørkved, P. T., Zhao, R., Rapp, H. T., Xavier, J. R., & Hoffmann, F. (2020). Deep-sea sponge grounds as nutrient sinks: denitrification is common in boreo-Arctic sponges. Biogeosciences, 17(5), 1231-1245 is available at https://dx.doi.org/10.5194/bg-17-1231-2020 CC-BY Journal/Magazine Article 2020 ftpolyuhongkong https://doi.org/10.5194/bg-17-1231-2020 2020-06-19T00:01:22Z 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. Department of Applied Biology and Chemical Technology 202006 bcrc published_final Article in Journal/Newspaper Arctic Hong Kong Polytechnic University: PolyU Institutional Repository (PolyU IR) Arctic Biogeosciences 17 5 1231 1245
institution Open Polar
collection Hong Kong Polytechnic University: PolyU Institutional Repository (PolyU IR)
op_collection_id ftpolyuhongkong
language English
description 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. Department of Applied Biology and Chemical Technology 202006 bcrc published_final
format Article in Journal/Newspaper
author Rooks, C
Fang, JKH
Morkyed, PT
Zhao, R
Rapp, HT
Xayier, JR
Hoffmann, F
spellingShingle Rooks, C
Fang, JKH
Morkyed, PT
Zhao, R
Rapp, HT
Xayier, JR
Hoffmann, F
Deep-sea sponge grounds as nutrient sinks: denitrification is common in boreo-Arctic sponges
author_facet Rooks, C
Fang, JKH
Morkyed, PT
Zhao, R
Rapp, HT
Xayier, JR
Hoffmann, F
author_sort Rooks, C
title Deep-sea sponge grounds as nutrient sinks: denitrification is common in boreo-Arctic sponges
title_short Deep-sea sponge grounds as nutrient sinks: denitrification is common in boreo-Arctic sponges
title_full Deep-sea sponge grounds as nutrient sinks: denitrification is common in boreo-Arctic sponges
title_fullStr Deep-sea sponge grounds as nutrient sinks: denitrification is common in boreo-Arctic sponges
title_full_unstemmed Deep-sea sponge grounds as nutrient sinks: denitrification is common in boreo-Arctic sponges
title_sort deep-sea sponge grounds as nutrient sinks: denitrification is common in boreo-arctic sponges
publisher Copernicus GmbH
publishDate 2020
url http://hdl.handle.net/10397/82269
https://doi.org/10.5194/bg-17-1231-2020
geographic Arctic
geographic_facet Arctic
genre Arctic
genre_facet Arctic
op_relation Biogeosciences
Biogeosciences, 6 Mar. 2020, v. 17, no. 5, p. 1231-1245
1726-4170
http://hdl.handle.net/10397/82269
1231
1245
17
5
doi:10.5194/bg-17-1231-2020
WOS:000518835100001
2-s2.0-85081250951
1726-4189
op_rights © Author(s) 2020. This work is distributed under the Creative Commons Attribution 4.0 License (https://creativecommons.org/licenses/by/4.0/).
The following publication Rooks, C., Fang, J. K. H., Mørkved, P. T., Zhao, R., Rapp, H. T., Xavier, J. R., & Hoffmann, F. (2020). Deep-sea sponge grounds as nutrient sinks: denitrification is common in boreo-Arctic sponges. Biogeosciences, 17(5), 1231-1245 is available at https://dx.doi.org/10.5194/bg-17-1231-2020
op_rightsnorm CC-BY
op_doi https://doi.org/10.5194/bg-17-1231-2020
container_title Biogeosciences
container_volume 17
container_issue 5
container_start_page 1231
op_container_end_page 1245
_version_ 1766331874514305024