Marine waters are often nitrogen (N) limited. Denitrification, the microbial conversion of nitrate to dinitrogen (N 2) gas, is responsible for significant N removal from the coastal ocean. In contrast, nitrogen fixation, the microbial transformation of N 2 to ammonium, is typically regarded as an inconsequential N source. The imbalance between these 2 processes is responsible, at least in part, for N limitation in the coastal ocean. Organic matter quality and quantity has been shown to determine rates of these critical N cycling processes. We hypothesized that the timing of organic matter deposition to the benthos might also be important in determining which process dominates. We tested this hypothesis using a coupled biogeochemical-molecular approach. We report directly measured net sediment denitrification rates and corresponding expression of nirS, a gene in the denitrification pathway, with the simultaneous expression of nifH, a gene associated with nitrogen fixation. The timing of organic matter deposition determined the magnitude of the net sediment N 2 fluxes. Highest rates of denitrification occurred soon after deposition, and the lowest rates occurred over 200 d after the last deposition event concomitant with increased nifH expression. Phylogenetic evidence suggests that sulfur and sulfate reducers are responsible for the nitrogen fixation. Globally, warming water temperatures, changes in light, and reduced nutrient loads through management intervention have been linked to decreases and/or altered phenology of water column productivity. Based on a conceptual model developed here, we suggest that in these systems, heterotrophic sediment nitrogen fixation may become an important component of the nitrogen budget.
Nitrogen (N) cycling microbial communities in marine sediments are extremely diverse, and it is unknown whether this diversity reflects extensive functional redundancy. Sedimentary denitrifiers remove significant amounts of N from the coastal ocean and diazotrophs are typically regarded as inconsequential. Recently, N fixation has been shown to be a potentially important source of N in estuarine and continental shelf sediments. Analysis of expressed genes for nitrite reductase (nirS) and a nitrogenase subunit (nifH) was used to identify the likely active denitrifiers and nitrogen fixers in surface sediments from different seasons in Narragansett Bay (Rhode Island, USA). The overall diversity of diazotrophs expressing nifH decreased along the estuarine gradient from the estuarine head to an offshore continental shelf site. Two groups of sequences related to anaerobic sulphur/iron reducers and sulphate reducers dominated libraries of expressed nifH genes. Quantitative polymerase chain reaction (qPCR) and quantitative reverse transcription polymerase chain reaction (qRT-PCR) data shows the highest abundance of both groups at a mid bay site, and the highest nifH expression at the head of the estuary, regardless of season. Several potential environmental factors, including water temperature, oxygen concentration and metal contamination, may influence the abundance and nifH expression of these two bacterial groups.
Bacteria that carry out many processes of the nitrogen cycle inhabit estuarine sediments. Denitrification is known to be a dominant process causing estuarine sediments to behave as net nitrogen sinks. However, measurements of nitrogen fluxes in the sediments of Narragansett Bay, Rhode Island, USA, have at times revealed high rates of net nitrogen (N 2 ) fixation. Whereas changes in primary production, in magnitude and phenology, within Narragansett Bay have been identified as possible causes for these changes in nitrogen cycling within the benthos, a factor that has not been examined thus far is seasonal hypoxia. Since anaerobic diazotrophs figure so prominently within the sediments of Narragansett Bay, we hypothesized that dissolved oxygen concentrations in the bottom waters affect their activity. In order to explore this relationship, we measured the activity of diazotrophs in the surface sediments of 3 study areas during the summers of 2013 and 2014 using the acetylene reduction assay. We explored the effects of several water quality parameters on nitrogenase activity including, among others, dissolved oxygen and chlorophyll concentrations. Our measurements of nitrogenase activity were generally low, ranging between 2 and 5 nmol ethylene g −1 d −1 but spiked to 16 nmol ethylene g −1 d −1 at an area experiencing severe hypoxia in July 2013. Our data suggest that diazotrophy in estuarine sediments is enhanced when the benthos experiences very low dissolved oxygen in conjunction with recent influxes of autochthonous organic matter. Experiments with sediment core incubations conducted in the laboratory support our hypothesis that low dissolved oxygen and organic matter additions promote N 2 fixation.
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