Freshwater copepod carcasses as pelagic microsites of dissimilatory nitrate reduction to ammonium

Peter Stief, Ann Sofie Birch Lundgaard, Alexander H Treusch, Bo Thamdrup, Hans-Peter Grossart, Ronnie N Glud

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Abstract

A considerable fraction of freshwater zooplankton was recently found to consist of dead specimens that sink to the lake bottom. Such carcasses host intense microbial activities that may promote oxygen depletion at the microscale. Therefore, we tested the hypothesis that sinking zooplankton carcasses are microsites of anaerobic nitrogen cycling that contribute to pelagic fixed-nitrogen loss even in the presence of ambient oxygen. Incubation experiments were performed with the ubiquitous copepods Eudiaptomus sp. and Megacyclops gigas at different ambient oxygen levels that sinking carcasses encounter during their descent in stratified lakes. 15N-stable-isotope incubations revealed intense carcass-associated anaerobic nitrogen cycling only at low ambient oxygen levels (<25% air saturation). Dissimilatory nitrate reduction to ammonium (DNRA) dominated over denitrification and thus the potential for fixed-nitrogen loss was low. Consistent with this partitioning of anaerobic nitrogen cycling, the relative abundance of the carcass-associated marker gene for DNRA (nrfA) was ∼20-400 times higher than that for denitrification (nirS). Additionally, the relative nrfA and nirS abundances were ∼90-180 times higher on copepod carcasses than in lake water. This functional distinctiveness of carcass-associated bacterial communities was further substantiated by 16S rDNA-based fingerprinting. We conclude that the unique bacterial communities and microenvironments provided by zooplankton carcasses influence pelagic nitrogen cycling in lakes, but mainly at seasonally low ambient O2 levels in the bottom water.

Original languageEnglish
Article numberfiy144
JournalFEMS Microbiology Ecology
Volume94
Issue number10
ISSN0168-6496
DOIs
Publication statusPublished - 1. Oct 2018

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Fresh Water
Ammonium Compounds
Nitrogen
ammonium
Lakes
Zooplankton
nitrate
nitrogen
Oxygen
zooplankton
oxygen
denitrification
lake
incubation
Ribosomal DNA
Isotopes
bottom water
lake water
microbial activity
relative abundance

Cite this

@article{d67d8135e2af4f45b897fe32e92426e9,
title = "Freshwater copepod carcasses as pelagic microsites of dissimilatory nitrate reduction to ammonium",
abstract = "A considerable fraction of freshwater zooplankton was recently found to consist of dead specimens that sink to the lake bottom. Such carcasses host intense microbial activities that may promote oxygen depletion at the microscale. Therefore, we tested the hypothesis that sinking zooplankton carcasses are microsites of anaerobic nitrogen cycling that contribute to pelagic fixed-nitrogen loss even in the presence of ambient oxygen. Incubation experiments were performed with the ubiquitous copepods Eudiaptomus sp. and Megacyclops gigas at different ambient oxygen levels that sinking carcasses encounter during their descent in stratified lakes. 15N-stable-isotope incubations revealed intense carcass-associated anaerobic nitrogen cycling only at low ambient oxygen levels (<25{\%} air saturation). Dissimilatory nitrate reduction to ammonium (DNRA) dominated over denitrification and thus the potential for fixed-nitrogen loss was low. Consistent with this partitioning of anaerobic nitrogen cycling, the relative abundance of the carcass-associated marker gene for DNRA (nrfA) was ∼20-400 times higher than that for denitrification (nirS). Additionally, the relative nrfA and nirS abundances were ∼90-180 times higher on copepod carcasses than in lake water. This functional distinctiveness of carcass-associated bacterial communities was further substantiated by 16S rDNA-based fingerprinting. We conclude that the unique bacterial communities and microenvironments provided by zooplankton carcasses influence pelagic nitrogen cycling in lakes, but mainly at seasonally low ambient O2 levels in the bottom water.",
author = "Peter Stief and Lundgaard, {Ann Sofie Birch} and Treusch, {Alexander H} and Bo Thamdrup and Hans-Peter Grossart and Glud, {Ronnie N}",
year = "2018",
month = "10",
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doi = "10.1093/femsec/fiy144",
language = "English",
volume = "94",
journal = "F E M S Microbiology Ecology",
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Freshwater copepod carcasses as pelagic microsites of dissimilatory nitrate reduction to ammonium. / Stief, Peter; Lundgaard, Ann Sofie Birch; Treusch, Alexander H; Thamdrup, Bo; Grossart, Hans-Peter; Glud, Ronnie N.

In: FEMS Microbiology Ecology, Vol. 94, No. 10, fiy144, 01.10.2018.

Research output: Contribution to journalJournal articleResearchpeer-review

TY - JOUR

T1 - Freshwater copepod carcasses as pelagic microsites of dissimilatory nitrate reduction to ammonium

AU - Stief, Peter

AU - Lundgaard, Ann Sofie Birch

AU - Treusch, Alexander H

AU - Thamdrup, Bo

AU - Grossart, Hans-Peter

AU - Glud, Ronnie N

PY - 2018/10/1

Y1 - 2018/10/1

N2 - A considerable fraction of freshwater zooplankton was recently found to consist of dead specimens that sink to the lake bottom. Such carcasses host intense microbial activities that may promote oxygen depletion at the microscale. Therefore, we tested the hypothesis that sinking zooplankton carcasses are microsites of anaerobic nitrogen cycling that contribute to pelagic fixed-nitrogen loss even in the presence of ambient oxygen. Incubation experiments were performed with the ubiquitous copepods Eudiaptomus sp. and Megacyclops gigas at different ambient oxygen levels that sinking carcasses encounter during their descent in stratified lakes. 15N-stable-isotope incubations revealed intense carcass-associated anaerobic nitrogen cycling only at low ambient oxygen levels (<25% air saturation). Dissimilatory nitrate reduction to ammonium (DNRA) dominated over denitrification and thus the potential for fixed-nitrogen loss was low. Consistent with this partitioning of anaerobic nitrogen cycling, the relative abundance of the carcass-associated marker gene for DNRA (nrfA) was ∼20-400 times higher than that for denitrification (nirS). Additionally, the relative nrfA and nirS abundances were ∼90-180 times higher on copepod carcasses than in lake water. This functional distinctiveness of carcass-associated bacterial communities was further substantiated by 16S rDNA-based fingerprinting. We conclude that the unique bacterial communities and microenvironments provided by zooplankton carcasses influence pelagic nitrogen cycling in lakes, but mainly at seasonally low ambient O2 levels in the bottom water.

AB - A considerable fraction of freshwater zooplankton was recently found to consist of dead specimens that sink to the lake bottom. Such carcasses host intense microbial activities that may promote oxygen depletion at the microscale. Therefore, we tested the hypothesis that sinking zooplankton carcasses are microsites of anaerobic nitrogen cycling that contribute to pelagic fixed-nitrogen loss even in the presence of ambient oxygen. Incubation experiments were performed with the ubiquitous copepods Eudiaptomus sp. and Megacyclops gigas at different ambient oxygen levels that sinking carcasses encounter during their descent in stratified lakes. 15N-stable-isotope incubations revealed intense carcass-associated anaerobic nitrogen cycling only at low ambient oxygen levels (<25% air saturation). Dissimilatory nitrate reduction to ammonium (DNRA) dominated over denitrification and thus the potential for fixed-nitrogen loss was low. Consistent with this partitioning of anaerobic nitrogen cycling, the relative abundance of the carcass-associated marker gene for DNRA (nrfA) was ∼20-400 times higher than that for denitrification (nirS). Additionally, the relative nrfA and nirS abundances were ∼90-180 times higher on copepod carcasses than in lake water. This functional distinctiveness of carcass-associated bacterial communities was further substantiated by 16S rDNA-based fingerprinting. We conclude that the unique bacterial communities and microenvironments provided by zooplankton carcasses influence pelagic nitrogen cycling in lakes, but mainly at seasonally low ambient O2 levels in the bottom water.

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