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Shell biofilm‐associated nitrous oxide production in marine molluscs: processes, precursors and relative importance
Author(s) -
Heisterkamp Ines M.,
Schramm Andreas,
Larsen Lone H.,
Svenningsen Nanna B.,
Lavik Gaute,
de Beer Dirk,
Stief Peter
Publication year - 2013
Publication title -
environmental microbiology
Language(s) - English
Resource type - Journals
SCImago Journal Rank - 1.954
H-Index - 188
eISSN - 1462-2920
pISSN - 1462-2912
DOI - 10.1111/j.1462-2920.2012.02823.x
Subject(s) - biology , biofilm , nitrification , environmental chemistry , mesocosm , denitrification , microcosm , nitrous oxide , nitrite , nitrate , denitrifying bacteria , anoxic waters , ammonium , ecology , nitrogen , nutrient , bacteria , chemistry , genetics , organic chemistry
Summary Emission of the greenhouse gas nitrous oxide (N 2 O) from freshwater and terrestrial invertebrates has exclusively been ascribed to N 2 O production by ingested denitrifying bacteria in the anoxic gut of the animals. Our study of marine molluscs now shows that also microbial biofilms on shell surfaces are important sites of N 2 O production. The shell biofilms of Mytilus edulis , Littorina littorea and Hinia reticulata contributed 18–94% to the total animal‐associated N 2 O emission. Nitrification and denitrification were equally important sources of N 2 O in shell biofilms as revealed by 15 N‐stable isotope experiments with dissected shells. Microsensor measurements confirmed that both nitrification and denitrification can occur in shell biofilms due to a heterogeneous oxygen distribution. Accordingly, ammonium, nitrite and nitrate were important drivers of N 2 O production in the shell biofilm of the three mollusc species. Ammonium excretion by the animals was found to be sufficient to sustain N 2 O production in the shell biofilm. Apparently, the animals provide a nutrient‐enriched microenvironment that stimulates growth and N 2 O production of the shell biofilm. This animal‐induced stimulation was demonstrated in a long‐term microcosm experiment with the snail H. reticulata , where shell biofilms exhibited the highest N 2 O emission rates when the animal was still living inside the shell.