Diazotroph activity in surface Narragansett Bay sediments in summer is stimulated by hypoxia and organic matter delivery

Abstract

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.

Pelagic N2 fixation dominated by sediment diazotrophic communities in a shallow temperate estuary

“…This may suggest that diazotrophs were associated with chlorophyll‐rich particles that at least partially derive from phytoplankton biomass previously deposited onto the sediments. This is consistent with a previous study in Narragansett Bay sediments showing N 2 fixation stimulated by organic matter inputs (Spinette et al 2019) and the sampling period of the present study coincided with the highest chlorophyll concentrations observed along the year in Narragansett Bay (Oviatt et al 2002). Similar results have been obtained from pelagic tropical and temperate coastal ecosystems, as well as in deep aphotic waters (Moisander et al 2014; Benavides et al 2015; Severin et al 2015).…”

“…Many of the dominant diazotrophs observed in the water column during our sampling were affiliated with nifH Subcluster 1A and Cluster III. These sequence clusters contain putative anaerobic diazotrophs previously observed in the Bay's sediments (Fulweiler et al 2013; Brown and Jenkins 2014; Spinette et al 2019) as well as in other temperate and subtropical estuarine systems (Moisander et al 2007; Bentzon‐Tilia et al 2015 b ). The reports of active non‐cyanobacterial diazotrophs in eutrophic coastal and estuarine environments, coupled with molecular evidence of the genetic basis for how heterotrophic bacterial diazotrophs can maintain N 2 fixation under high nitrogen conditions (reviewed in Bombar et al 2016), suggests that eutrophic environments may be a niche for non‐cyanobacterial diazotrophs.…”

“…However, a recent study reported N 2 fixation activity related to severe hypoxic events coupled with fresh organic matter inputs in the Bay's sediments (Spinette et al 2019). The rationale for this process is that hypoxia reduces oxygen availability for nitrification, eventually reducing nitrate concentrations and inhibiting denitrification, providing a niche for diazotrophs to thrive (Spinette et al 2019). The N 2 fixation activity has been attributed to anaerobic and sulfate‐reducing bacteria, which are the dominant diazotrophs in the bay's sediments (Fulweiler et al 2013; Brown and Jenkins 2014).…”

“…Consequently, the organic matter deposited onto the sediment has progressively decreased in quantity and quality, which has led to a reduction in denitrification rates with reversals to net N 2 fixation activity in the warmest and most nutrient-depleted periods of the year (Fulweiler et al 2007(Fulweiler et al , 2013. However, a recent study reported N 2 fixation activity related to severe hypoxic events coupled with fresh organic matter inputs in the Bay's sediments (Spinette et al 2019). The rationale for this process is that hypoxia reduces oxygen availability for nitrification, eventually reducing nitrate concentrations and inhibiting denitrification, providing a niche for diazotrophs to thrive (Spinette et al 2019).…”

Biological Nitrogen Fixation in Sediments of a Cyanobacterial Bloom‐Occurring Bay in One Eutrophic Shallow Lake: Occurrence and Related Environmental Factors

“…Temperature is another key factor regulating nitrogenase activity (NA) (Sorensen & Michelsen, 2011), and NA has been observed to have a maximum in summer in marine sediments (Bertics et al., 2013). Moreover, other environmental factors, such as the total nitrogen (TN): total phosphorous (TP) molar ratio (Yao et al., 2018), organic matter (Fulweiler et al., 2013; Spinette et al., 2019), and dissolved inorganic nitrogen can also affect BNF (Knapp, 2012).…”