The Eastern Tropical North Pacific (ETNP) is a large, persistent, and intensifying oxygen minimum zone (OMZ) that accounts for almost half of the total area of global OMZs. Within the OMZ core (∼350–700 m depth), dissolved oxygen is typically near or below the analytical detection limit of modern sensors (∼10 nM). Steep oxygen gradients above and below the OMZ core lead to vertical structuring of microbial communities that also vary between particle-associated (PA) and free-living (FL) size fractions. Here, we use 16S amplicon sequencing (iTags) to analyze the diversity and distribution of prokaryotic populations between FL and PA size fractions and among the range of ambient redox conditions. The hydrographic conditions at our study area were distinct from those previously reported in the ETNP and other OMZs, such as the ETSP. Trace oxygen concentrations (∼0.35 μM) were present throughout the OMZ core at our sampling location. Consequently, nitrite accumulations typically reported for OMZ cores were absent as were sequences for anammox bacteria (Brocadiales genus Candidatus Scalindua), which are commonly found across oxic-anoxic boundaries in other systems. However, ammonia-oxidizing bacteria (AOB) and archaea (AOA) distributions and maximal autotrophic carbon assimilation rates (1.4 μM C d–1) coincided with a pronounced ammonium concentration maximum near the top of the OMZ core. In addition, members of the genus Nitrospina, a dominant nitrite-oxidizing bacterial (NOB) clade were present suggesting that both ammonia and nitrite oxidation occur at trace oxygen concentrations. Analysis of similarity test (ANOSIM) and Non-metric Dimensional Scaling (nMDS) revealed that bacterial and archaeal phylogenetic representations were significantly different between size fractions. Based on ANOSIM and iTag profiles, composition of PA assemblages was less influenced by the prevailing depth-dependent biogeochemical regime than the FL fraction. Based on the presence of AOA, NOB and trace oxygen in the OMZ core we suggest that nitrification is an active process in the nitrogen cycle of this region of the ETNP OMZ.
Introduction
In response to ongoing climate change and localized human activities, concentrations of dissolved oxygen have been declining in the open ocean and in coastal marine systems (Breitburg et al., 2018). Estimated oxygen loss from the open ocean during the past 60 years exceeds 2% (Schmidtko et al., 2017), creating concerns about the consequences of oxygen-depleted zone expansion (Paulmier and Ruiz-Pino, 2009). Open ocean OMZs form when high surface primary production fuels biological oxygen demand in subsurface waters that exceeds rates of physical ventilation at depth. Oxygen concentrations in OMZ water columns can have steep gradients (oxycline) above and below the oxygen-depleted core creating hypoxic (typically between 2 and ∼90 μM), suboxic (<2 μM) and anoxic (below detection limit (∼10 nM) layers of varying dimensions (Bertagnolli and Stewart, 2018). Oxygen gradients lead to vertical structuring of metazoan and microbial communities and biogeochemical processes along these extensive oxyclines (Belmar et al., 2011).
Some of the highest rates of nitrogen loss have been recorded in OMZs of the Eastern Tropical North Pacific (ETNP) and South Pacific (ETSP) (Callbeck et al., 2017; Penn et al., 2019), the permanently stratified Cariaco Basin (Montes et al., 2013), the Arabian Sea (Ward et al., 2009), and the OMZ of the Benguela upwelling system (Kuypers et al., 2005). In these systems, the microbial processes of canonical denitrification (heterotrophic reduction of nitrate to nitrogen intermediates and often to dinitrogen gas) and anammox (anaerobic ammonium oxidation) lead to nitrogen losses that can potentially limit primary production (Ward et al., 2007). Moreover, oceanic nitrous oxide emissions (a potent greenhouse gas) from microbial denitrification occurring in OMZs is estimated to account for at least one third of global natural nitrous oxide emissions (Naqvi et al., 2010).
The ETNP OMZ is a large, persistent, and intensifying oxygen minimum zone that accounts for almost half of the total area of global OMZs, is located between 0–25°N latitude and 75 and 180°W longitude (Paulmier and Ruiz-Pino, 2009; Schmidtko et al., 2017). Due to their ecological importance, the biogeochemistry and microbial diversity of different ETNP OMZ regions have been studied intensively (e.g., Beman and Carolan, 2013; Duret et al., 2015; Ganesh et al., 2015; Chronopoulou et al., 2017; Pack et al., 2015; Peng et al., 2015). Previous studies report that dissolved oxygen in this OMZ core (∼250–750 m depth) is typically near or below analytical detection limits (∼10 nM) (Tiano et al., 2014; Garcia-Robledo et al., 2017). However, along the northern margin of the ETNP’s OMZ (study site location ∼22°N) oxygen concentrations at 500 m can reach annual averages between 10 and 20 μM (Paulmier and Ruiz-Pino, 2009; Data from World Ocean Atlas 2013)1. During the field campaign reported herein, we measured oxygen in the OMZ core at sufficient concentrations (0.35 μM) to support aerobic microbial processes, such as ammonium and nitrite oxidation, and partially inhibit important anaerobic microbial processes. Aerobic microbial processes have been detected previously in seemingly suboxic or anoxic layers of the ETNP OMZ (Peng et al., 2015; Garcia-Robledo et al., 2017; Penn et al., 2019). However, factors controlling the distribution and activities of specific functional groups of microorganisms in OMZs are not yet fully understood.
The presence of nitrifiers where oxygen is undetectable in an OMZ can be explained by recent shifts in the vertical position of the oxycline due to episodic vertical oxygen ventilation, which can lead to ephemeral trace oxygen levels within OMZ cores (Muller-Karger et al., 2001; Ulloa et al., 2012; Garcia-Robledo et al., 2017). Such transient conditions can be exploited by aerobic or microaerophilic populations, including nitrifiers. Moreover, sinking particles from the epipelagic (aggregated cells, fecal pellets, and complex organic materials) can contain trace levels of oxygen (Ganesh et al., 2014). Thus, oxygen and aerobic microbes can be transported to otherwise anoxic waters, temporarily allowing aerobic metabolisms to occur in association with particles. Particles are known to be hotspots of microbial biogeochemical cycling (Simon et al., 2002; Ganesh et al., 2014) and can support contrasting anaerobic or aerobic microbial processes that are not observed in the free-living state (Alldredge and Cohen, 1987; Wright et al., 2012; Suter et al., 2018).
In the present study, we investigate prokaryotic communities occupying the northern margin of the ETNP’s OMZ and environmental factors that likely influence their vertical distributions using 16S amplicon sequencing (iTags) coupled with multivariate statistics. We examined two size fractions; the free-living (0.2–2.7 μm) fraction, and the particle-associated fraction (>2.7 μm, capturing particles as well as protistan cells) at multiple depths along the oxycline that correspond to distinct redox conditions.
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Post time: Jul-05-2024