The Microbial Ecology of Nitrous Oxide Cycling in Marine Environments: Linking community dynamics to ecosystem processes




Jameson, Brett Douglas

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Nitrous oxide (N2O) is an increasingly abundant, atmospheric trace-gas that contributes to climate change and stratospheric ozone depletion. Marine environments act as a net source of N2O to the atmosphere at global scales resulting from the combined microbial processes of nitrification and denitrification. Considerable effort has been directed toward understanding the environmental drivers of N2O production and consumption in the ocean over the past few decades. However, comparatively little is known about the ecological mechanisms that facilitate N2O cycling in marine environments and how this relates to environmental variability. This research attempts to resolve some of these knowledge gaps by leveraging modern molecular tools and biogeochemical rate measurements to identify links between microbial community dynamics and N2O production across a wide range of marine environments. The first data chapter considers Saanich Inlet, a seasonally anoxic fjord located on Vancouver Island, Canada, as a model oxygen deficient zone for investigating patterns of microbial community assembly in relation to variable N2O production rates across spatial and temporal redox gradients. Network analysis of prokaryote 16S rRNA amplicon sequences delineated discrete community subnetworks that were structured around several putative keystone taxa and displayed contrasting water column distributions and roles in N2O cycling. Keystone taxa implicated in coupled carbon, nitrogen, and sulfur cycling were prominent in the low-oxygen subnetwork and correlated well with N2O production from denitrification in waters demonstrating net N2O consumption. Conversely, oxycline subnetworks were characterized by keystone aerobic heterotrophs that correlated with nitrification rates and water column N2O accumulation. This work presents a first assessment of the relationships between microbial community interaction networks and N2O cycling rate processes in the ocean. The remainder of this dissertation focuses on N2O cycling in sediment environments, which can act as net sources or sinks of N2O at local scales. The third chapter resolves an important data gap with respect to N2O fluxes from continental margin sediments underlying the northeast subarctic Pacific (NESAP) oxygen deficient zone, a previously unstudied environment with respect to N2O cycling. This work reports the first sub-millimeter resolution porewater N2O profiles in offshore sediments and employs a profile interpretation model to demonstrate that these environments are a considerable source of N2O to the water column. Finally, experimental manipulations provided evidence that upwelling conditions can stimulate N2O production and efflux from continental shelf sediments. Chapter Four builds on this work by adapting this procedure for work at low N2O concentrations to quantify the N2O sink capacity of minimally impacted mangrove sediments. Molecular data collected from both the mangrove and NESAP continental margin sediments was then used to identify relationships between microbial community dynamics and sediment N2O source/sink status. Mangrove N2O sinks had higher abundances and expression levels of ‘atypical’ N2O reductases (nosZII), suggesting that net N2O consumption in nitrogen-limiting systems may be driven by non-denitrifying N2O scavengers. NosZII was associated with taxonomic groups implicated in dissimilatory nitrate reduction to ammonium (DNRA), a prominent nitrogen conservation pathway in nitrogen-limiting systems. N2O source sediments from the NESAP contained higher abundances of putative ammonia oxidizing Archaea and were associated with elevated expression levels of typical nosZI variants, suggesting likely contributions from both nitrification and denitrification.



Nitrous Oxide, Nitrogen, Microsensors, Climate Change, Microbial Ecology, Microbiology, Environmental Microbiology, Sediments, Oxygen Minimum Zones, Biogeochemistry, Nutrient Cycles