Award: OCE-1233327

Oyster reefs are biogeochemical hot spots and prominent estuarine habitats that provide disproportionate ecological services. Oysters are capable of improving water quality and diminishing eutrophication by filtering nutrients and particles from the water column and depositing them in the sediments. Recycling of oyster biodeposits may enhance sedimentary denitrification that facilitates nitrogen removal in estuarine and coastal ecosystems, and there is the potential for this to occur in natural, restored, and cultured oysters. However, the explanation of excess nutrient removal mediated by oysters has been inconsistent in studies in various contexts. In addition, oysters could be a source of nitrous oxide (N2O), a greenhouse gas, in marine habitats due to incomplete denitrification. Our interdisciplinary research team of a microbial ecologist, a biogeochemist, an ecologist and an ecosystem modeler worked to 1) evaluate the effects of oyster mediated denitrification on nitrogen removal efficiency in marine ecosystems, 2) determine the environmental factors controlling oyster mediated denitrification producing N2 and N2O, 3) identify the oyster microbiomes responsible for denitrification, and 4) examine the fate of nitrogen in phytoplankton biomass. Experiments conducted with oysters and sediments collected from three oyster reefs in Virginia and North Carolina as well as oyster aquaculture sites in Connecticut showed higher denitrification activities in the presence of oysters. The sediments impacted by oyster biodeposits also had higher denitrification activities than the sediments without the biodeposit exposure. We found that nitrogen removal through denitrification in sediments in oyster reefs constructed as a component of a living shoreline reached rates similar to natural reefs within several years. In these same reefs N2O fluxes out of the sediments were extremely low and often sediments removed N2O from the atmosphere. Model simulations confirmed the potential for oysters to enhance nitrogen removal in Chesapeake Bay sub-estuaries. The model also predicts the levels of oyster restoration required to enhance nitrogen removal capacity and water quality in these sub-estuaries. Nitrous oxide production mediated by oysters was approximately 1% of total N2 production by denitrification, indicating that oysters are a trivial source of N2O in marine ecosystems. We also found that nitrate, oxygen, and temperature are important environmental factors affecting oyster mediated denitrification. Oyster microbiomes responsible for denitrification were examined using a combined metagenomic and metabolic inference approach. We investigated the gill, gut and shell microbiomes of oysters and their associated denitrifiers in response to spatial and temporal changes. The oyster gill, gut, and shell microbiomes all showed distinct and unique composition of their microbiomes. Higher denitrifier abundance was found in the shell microbiomes than other tissues, indicating the importance of shell biofilm communities in oyster mediated nitrogen removal. We also found niche differentiation of oyster microbiomes, demonstrating different groups of denitrifiers are responsible for performing denitrification in the examined oyster tissues. To date, 18 publications have resulted from this work with multiple additional manuscripts in progress. Data from this project are publically available on the BCO-DMO portal and through Dryad. Substantial educational contributions were made through training two postdoctoral fellows, six graduate students seeking Ph.D. or M.S degrees, 12 undergraduates, and three technicians. Two Ph.D.s were awarded and four other students completed their M.S. degrees in marine science. Information from this study was broadly disseminated to the general public and advanced the science that connects changes in nutrient cycling and oyster ecosystem functioning. This research has also informed efforts to plan and evaluate restoration of oyster reefs which rank among the most degraded estuarine habitats in the world. Last Modified: 01/01/2018 Submitted by: Michael F Piehler