Temporal dynamics of dissolved inorganic nitrogen (DIN) in the aphotic layer of a coastal upwelling system with variable dissolved oxygen
Introduction
The accumulation of NH4+ and NO2− in the ocean is rarely observed. This is due to the dynamic balance between the lateral and vertical transport of nutrients and various assimilative and dissimilative microbial processes, which occur over diverse temporal scales ranging from hours to days. These processes result in rapid NH4+ recycling, thus maintaining NH4+ at nanomolar levels (Dickson and Wheeler, 1995; Ward et al., 1989). NO3−, on the other hand, can accumulate and reaches micromolar levels during successive organic matter regeneration/oxidation cycles (Ganachaud and Wunsch, 2002), contributing to the NO3− inventory in the mid and deep ocean (Ward, 2008).
In some cases, NH4+ and NO2− can reach micromolar levels at specific depths, including the nitracline (Ward et al., 1989), the base of the euphotic zone (Lomas and Lipschultz, 2006) and oxygen minimum zones (OMZs) (Ward, 2000). For example, low NH4+, levels are present at the core of the OMZ, with an occasional transient peak at the oxycline (Molina and Farías, 2009), while NO2− accumulates at the so-called secondary NO2− maximum (SNM) throughout OMZs, reaching levels of >5 μM, as is the case in the northeastern Arabian Sea (Naqvi, 1991), and up to 23 μM off the Peruvian coast (Codispoti et al., 1986).
Respiration (aerobic and anaerobic) mediates the regeneration of NH4+ during organic matter (OM) mineralization (Lam et al., 2009). In this way, NH4+ accumulation occurs in areas of high organic matter (OM) mineralization, where NH4+ regeneration exceeds consumption. NH4+ consumption involves both aerobic and anaerobic NH4+ oxidation (i.e., AAO and anammox, respectively) as well as an assimilative consumption by phytoplankton (in the euphotic layer) and bacterioplankton (throughout the entire water column).
In the presence of DO, the oxidation of NH4+ to NO2− and subsequently of NO2− to NO3− is achieved by aerobic nitrification. Both pathways have been the focus of recent studies, following the breakthrough discovery of a clade of Crenarchaeota containing the amoA gene (which encodes for the AMO enzyme), today known as ammonia oxidizing archaea (AOA) (Beman et al., 2008; Könneke et al., 2005; Schleper et al., 2005; Santoro et al., 2010). Research has also been driven by the discovery that nitrification can occur below nanomolar levels of DO (Bristow et al., 2016).
In the absence or near absence of DO, three anaerobic metabolisms can be responsible for NO2− and NH4+ cycling in the aphotic layer: dissimilatory NO3− reduction and denitrification, anaerobic ammonium oxidation (anammox), and the dissimilatory reduction of NO3− to NH4+ (DNRA). The coupling and/or decoupling of these processes may therefore result in the accumulation of NO2− and NH4+. All three processes are regulated, in part, by DO concentrations and by the availability of different substrates (organic matter, NO2−, NO3−, NH4+, HS−), which may determine competitive relationships (Zehr and Kudela, 2011).
NO2− can be produced by dissimilatory NO3− reduction and be consumed during the sequential reduction of NO2− to N2, or denitrification (Naqvi et al., 2008; Ward et al., 2009). Additionally, NO2− can be used to oxidize NH4+ during anammox. NO2− may also become reoxidized to NO3− during aerobic NO2− oxidation (nitrification); during this process, NO2− occurs in a greater variety of environments, including within the OMZ core (Anderson et al., 1982; Bristow et al., 2016). DNRA, on the other hand, produces NH4+ but competes with denitrification for NO3− and NO2−, as DNRA is expected to dominate in environments with high organic matter content (Jensen et al., 2011).
NO3−, NO2− and NH4+ can also be assimilated, yet gaps in knowledge exist surrounding the consequences of DIN assimilation by bacterioplankton. For over four decades, the 15N tracer technique has been applied to estimate NO3− and NH4+ assimilation in seawater for both phytoplankton (Dugdale and Goering, 1967; Eppley and Peterson, 1979) and bacterioplankton (Goldman and Dennett, 2001) in the photic layer. Both planktonic components are known to compete for these substrates in the euphotic zone (Harrison, 1990); however, there is a lack of information regarding the aphotic zone, where bacterioplankton is the primary component determining ecosystem functioning. In general, studies on dissolved inorganic nitrogen (DIN) uptake have been restricted to short term assessments over days or weeks (Dugdale and Wilkerson, 1986; Dugdale et al., 2007; Fernandez et al., 2009). Few studies have focused on N-uptake within microbial communities (Allen et al., 2002; Lipschultz et al., 1990; Rodriguez and Williams, 2002) and fewer still have addressed O2 stress in aphotic waters (Lipschultz et al., 1990).
OMZs occur in coastal upwelling regions where primary production (PP) and export production (Ryther, 1969; Suess, 1980) exceeded advective O2 supply. These processes result in very high O2 utilization rates in subsurface layers, producing extremely low O2 conditions (Feely et al., 2004; Keeling et al., 2010). In coastal upwelling areas experiencing seasonal OMZ in subsurface water, several aerobic and anaerobic microbial processes play a key role in mediating biogeochemical N cycling (Lam et al., 2007; Naqvi et al., 1998; Zafiriou, 1990). In most cases, these mechanisms lead to the production of N2 or N2O and a resulting loss of N (Codispoti and Christensen, 1985; Galán et al., 2014, Galán et al., 2017; Naqvi and Noronha, 1991).
The ocean experiences stress from large scale processes, such as global warming and eutrophication, processes that contribute to deoxygenation (Keeling et al., 2010; Rabalais et al., 2014; Zhang et al., 2010). These changes have implications for the coastal upwelling zone off central Chile, which represents one of the world's most productive marine ecosystems and sustains a significant percentage of global primary production and fishery yields. Evidence indicates that upwelling-favorable winds have increased within the southern boundary of the Humboldt Current System in recent decades (35°–42 °S) (Aguirre et al., 2018). This trend is consistent with a poleward movement of the Southeast Pacific Anticyclone's influence and resembles the spatial pattern projected by Global Circulation Models for warming scenarios (Aguirre et al., 2018). A deepening of the mixed layer has also been observed and is associated with increasing winds, which may partly explain the cooler, more saline, and more productive surface waters (García-Loyola, 2017), with the latter potentially resulting in fluctuations in DO and therefore biogeochemical processes sensitive to changes in oxygenation.
This research is mainly based on a mid-term environmental dataset (spanning 10 years), including monthly measurements of OU and DIN uptake rates in aphotic layer. The way in which microbes can channel O2 and nutrients in assimilative or dissimilative pathways is investigated to elucidate the impact of microbial metabolisms on bio-element reservoirs and their turnovers in an upwelling system of central Chile.
Section snippets
Study area
The study area is located on the continental shelf off central Chile and includes a time-series station, “Station 18” (ST18), located 18 km offshore at 36.5 °S; 73.1 °W and at a depth of 92 m (Fig. 1).
The study area comprises one of the widest continental shelves off the Chilean coast, excepting Patagonia. The study area experiences seasonal OMZ, partially supported by the Peru-Chile undercurrent, which plays an important role in transporting O2-poor Equatorial Subsurface Water (ESSW)
Temporal and vertical distribution of physical-chemical variables
Annual climatology (mean monthly conditions) of temperature, salinity, and DO from 2002 to 2012 is shown in Fig. 2. As expected for Equatorial Subsurface Water (ESSW) upwelling, the 11 °C isotherm (Fig. 2a) and 34.5 halocline (Fig. 2b) rose to 20 m during spring (Sept.–Dec.) and remained at this shallow depth from summer until early autumn (Jan.–April). DO also showed a seasonal pattern (Fig. 2c) provoked by alternations between the upwelling of O2 poor, nitrate-rich ESSW during spring-summer
Oxygen budget on the continental shelf off central Chile
The Peru-Chile countercurrent transports ESSW from 5 °S toward 45 °S and influences DO distribution (Karstensen et al., 2008; Strub et al., 1998). When this current reaches the continental shelf (36 °S), one of the widest off Chile (excluding Patagonia), it covers shelf sediment and creates extreme O2 deficiency in bottom waters. During the coastal upwelling season (phases II and III), southerly winds place stress on the surface layer, driving vertical and lateral transport of the ESSW (Sobarzo
Conclusion
Subsurface waters off central Chile become increasingly oxygen deficient as primary production and associated OM downward flux enhance and accumulate in bottom waters and sediments. The annual cycle has been divided into three phases based on prevailing oceanographic conditions, reflecting observed phases in primary productivity. Suboxic conditions observed during the austral summer favor the accumulation of nitrite and ammonium at levels up to 5.6 and 4.1 μM. Such high concentrations of
Acknowledgements
Financial assistance was provided by the Comisión Nacional de Investigaciones Científicas y Tecnológicas (CONICYT) through, FONDAP N° 15110009, FONDECYT 1161138 (LF, PI) and the Gordon and Betty Moore Foundation (GBMF, 1661). The authors thank Dr. Luis Antonio Cuevas and Paul Harrison for their critical review and language editing. We also thank M. Gallegos, M. Alcaman and G. Garcia for assistance during laboratory analyses, and the crew of the R/V Kay Kay. This study was carried out based on
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