Unravelling the nitrogen cycle in a periodically hypoxic estuary

Abstract

The incidences of hypoxia (O2 10 m) and the Baltic Sea (> 60 m) or oxygen minimum zones (100 - 1000 m). To my knowledge no studies currently exist on the influence of hypoxia on nitrogen cycling in a shallow (3 - 5 m) salt wedge estuary. The Yarra River estuary, Australia, the study site for this research, is a shallow salt wedge estuary prone to periods of hypoxia during low freshwater inflow events. The estuary is a conduit for the transport of nitrogen into Port Phillip Bay; a nitrogen limited system. This research investigated the influence of hypoxia on nitrogen cycling within the Yarra River estuary through two means; 1) an observational survey of in situ nitrogen behaviour in addition to the measurement of nitrate (NO3-) reduction pathways, denitrification and dissimilatory NO3- reduction to ammonium (DNRA) using the 15N isotope pairing technique. 2) an in depth experimental study on the behaviour of denitrification and DNRA under changing oxygen conditions alongside availability of reductants using microelectrodes combined with diffusive equilibrium in thin layer (DET) gels and slurries. The observational survey of the Yarra River estuary was carried out from September 2009 through to March 2011. The estuary was a source of dissolved organic nitrogen (DON) and ammonium (NH4+) during hypoxic conditions using deviations from conservative mixing (Δ). Dissolved inorganic carbon (DIC) was used as a proxy for mineralisation and comparison of the in situ nutrient measurements (whole system) and DIC and NH4+ fluxes from intact core incubations showed that NH4+ was regenerated more efficiently relative to DIC under hypoxic conditions. For the whole system, mean ∆DIC : ∆NH4+ ratios under oxic (85 ± 33) and hypoxic (20 ± 3) conditions were significantly different. The more efficient NH4+ regeneration during hypoxia was due to a disconnect between mineralisation and nitrogen removal via nitrification-denitrification coupling due the cessation of nitrification; DNRA was not a significant contributor. Unexpectedly, DNRA increased in the presence of oxygen in the water column; the mean DNRA rate under oxic conditions (124 ± 31 µmol m-2 h-1) was significantly higher than rates during hypoxia (0.6 ± 0.1 µmol m-2 h-1). High DNRA rates led to a significant decrease in the denitrification : DNRA ratio under oxic (19 ± 18) conditions compared to the ratio during hypoxia (144 ± 48). In contradiction to the current paradigm, the increased DNRA rates can be explained by the presence of Fe2+ in the sediment supported by data from both intact cores and slurries. The coupling of Fe2+ oxidation and NO3- reduction to NH4+ has been observed in a bacterial study Weber et al. (2006) however to our knowledge this is the first study to observe this process in intact estuarine sediments. The absence of DNRA under hypoxic conditions was explained by the presence of high S2- concentrations and the binding of FeS, removing available Fe2+ for DNRA. This study identified the impact of hypoxia on the nitrogen removal capacity of a shallow estuarine system; the nitrogen removal capacity of the Yarra River estuary was low with < 4 % of the dissolved inorganic nitrogen load removed when compared to 20 - 50 % removal presented for other estuarine systems. During hypoxia the removal of NO3- via denitrification was minimal compared with the efflux of NH4+ from the sediment due to the disconnect between NH4+ removal via nitrification-denitrification coupling and mineralisation. Importantly, this study observed DNRA under conditions not considered to be conducive toward this process; Fe2+ oxidation coupled to NO3- reduction to NH4+. The Yarra River estuary is prone to high inputs of iron both filterable and colloidal, and as such has high concentrations of Fe2+ in the porewaters under oxic conditions. In large rivers such as the Amazon and Mississippi, significant amounts of iron may be deposited on the continental shelf, leading to high rates of iron reduction and Fe2+ accumulation within the porewaters. It is therefore possible that Fe-driven DNRA observed in the Yarra River estuary may occur at globally significant rates within these diagenetic hotspots.