Spatial Heterogeneity in Particle‐Associated, Light‐Independent Superoxide Production Within Productive Coastal Waters

Abstract

In the marine environment, the reactive oxygen species (ROS) superoxide is produced through a diverse array of light-dependent and light-independent reactions, the latter of which is thought to be primarily controlled by microorganisms. Marine superoxide production influences organic matter remineralization, metal redox cycling, and dissolved oxygen concentrations, yet the relative contributions of different sources to total superoxide production remain poorly constrained. Here we investigate the production, steady-state concentration, and particle-associated nature of light-independent superoxide in productive waters off the northeast coast of North America. We find exceptionally high levels of light-independent superoxide in the marine water column, with concentrations ranging from 10 pM to in excess of 2,000 pM. The highest superoxide concentrations were particle associated in surface seawater and in aphotic seawater collected meters off the seafloor. Filtration of seawater overlying the continental shelf lowered the light-independent, steady-state superoxide concentration by an average of 84%. We identify eukaryotic phytoplankton as the dominant particle-associated source of superoxide to these coastal waters. We contrast these measurements with those collected at an off-shelf station, where superoxide concentrations did not exceed 100 pM, and particles account for an average of 40% of the steady-state superoxide concentration. This study demonstrates the primary role of particles in the production of superoxide in seawater overlying the continental shelf and highlights the importance of light-independent, dissolved-phase reactions in marine ROS production. Plain Language Summary Superoxide is a reactive oxygen species (ROS) that forms in seawater as a result of light-dependent and light-independent reactions. This molecule is relatively short lived, and its tendency to react with nutrients including organic carbon and metals makes it an important player in many element cycles essential to life. Although the origin of light-independent superoxide production is thought to primarily result from the extracellular production of superoxide by microorganisms, this notion is largely untested. In this study, we investigated the concentration and production rate of light-independent superoxide in coastal waters off the northeast coast of North America. We found that light-independent superoxide concentrations exhibited significant spatial heterogeneity (10-2,000 pM) and that filtration of particles lowered superoxide concentrations by 84% and 40% in seawater collected on and off the continental shelf, respectively. We found that eukaryotic phytoplankton are most closely associated with light-independent superoxide concentrations in these coastal waters. This work demonstrates that microorganisms can account for a significant fraction light-independent superoxide in the marine environment, but dissolved-phase superoxide production can also contribute significantly to light-independent ROS production, particularly in de...

Dark Reduction Drives Evasion of Mercury From the Ocean

“…2 ) was measured using the chemiluminescence method described by Rose et al (2008a), with minor modifications (Sutherland et al, 2020). Superoxide signals were measured by pumping unfiltered seawater (UFSW) or aged filtered seawater (AFSW) from dark bottles using a high accuracy peristaltic pump directly into a flowthrough FeLume Mini system (Waterville Analytical, Waterville ME).…”

“…2 ) and hydrogen peroxide (H 2 O 2 ) in natural waters has more recently been attributed in large part to light-independent reactions mediated by particles, presumably composed primarily of microbes (Rose et al, 2008b;Hansard et al, 2010;Roe et al, 2016;Zhang et al, 2016;Sutherland et al, 2020). As these ROS may influence the cycling of Hg, some of our amendment experiments either added exogenous ROS or stimulated ROS production by the resident microbial community.…”

Inter-domain Horizontal Gene Transfer of Nickel-binding Superoxide Dismutase

“…In the surface ocean, superoxide and hydrogen peroxide production is wide-spread and results from a combination of light-dependent and light-independent reactions (Diaz et al, 2019; Sutherland et al, 2019; Vermilyea et al, 2010). Surface superoxide concentrations range from low pM to several nM in the open ocean, with higher concentrations typically found in productive surface waters (Sutherland, Grabb, et al, 2020; Sutherland, Wankel, et al, 2020). In some cases, superoxide may approach 100-200 nM in productive coral reef ecosystems (Diaz et al, 2016; Grabb et al, 2019).…”

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“…As noted above, there was no discernible trend in the gross specific rate of Hg(II) reduction in unfiltered samples across our stations. This is interesting because the stations where our experiments were conducted include waters with a range in cell abundance from 0.4•10 6 to 2•10 6 bacterial cells mL −1 in aphotic waters (Sutherland et al, 2020) and perhaps a range in community activity as well. This suggests three possibilities: (1) Hg(II) reduction in the dark is not dependent on heterotrophic bacterial activity at all and whatever the agent responsible for Hg reduction was, had a uniform distribution or was at sufficient excess at all our stations, (2) cells at the lower abundance site had a higher per cell dark reduction rate than cells at the higher abundance sites, or (3) the rate of dark reduction, whatever the mechanism, is set by a slow step other than the reaction itself, for example the rate of release of Hg from a "hard-toreduce" pool.…”

“…The fraction of total Hg as Hg 0 compared to the light-independent, steady-state concentration of superoxide (left) and the rate of light-independent superoxide production in unfiltered water (right) at all stations and depths. For more details on the superoxide dynamics (see Sutherland et al, 2020).…”