Shell biofilm-associated nitrous oxide production in marine molluscs: processes, precursors and relative importance
Article first published online: 26 JUL 2012
© 2012 John Wiley & Sons Ltd and Society for Applied Microbiology
Thematic Issue: Invertebrate-Microbe Interactions
Volume 15, Issue 7, pages 1943–1955, July 2013
How to Cite
Heisterkamp, I. M., Schramm, A., Larsen, L. H., Svenningsen, N. B., Lavik, G., de Beer, D. and Stief, P. (2013), Shell biofilm-associated nitrous oxide production in marine molluscs: processes, precursors and relative importance. Environmental Microbiology, 15: 1943–1955. doi: 10.1111/j.1462-2920.2012.02823.x
- Issue published online: 4 JUL 2013
- Article first published online: 26 JUL 2012
- Accepted manuscript online: 22 JUN 2012 10:53AM EST
- Received 29 December, 2011; revised 6 June, 2012; accepted 10 June, 2012.
Emission of the greenhouse gas nitrous oxide (N2O) from freshwater and terrestrial invertebrates has exclusively been ascribed to N2O 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 N2O production. The shell biofilms of Mytilus edulis, Littorina littorea and Hinia reticulata contributed 18–94% to the total animal-associated N2O emission. Nitrification and denitrification were equally important sources of N2O in shell biofilms as revealed by 15N-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 N2O production in the shell biofilm of the three mollusc species. Ammonium excretion by the animals was found to be sufficient to sustain N2O production in the shell biofilm. Apparently, the animals provide a nutrient-enriched microenvironment that stimulates growth and N2O 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 N2O emission rates when the animal was still living inside the shell.