Dark biological superoxide production as a significant flux and sink of marine dissolved oxygen

Abstract

The balance between sources and sinks of molecular oxygen in the oceans has greatly impacted the composition of Earth’s atmosphere since the evolution of oxygenic photosynthesis, thereby exerting key influence on Earth’s climate and the redox state of (sub)surface Earth. The canonical source and sink terms of the marine oxygen budget include photosynthesis, respiration, photorespiration, the Mehler reaction, and other smaller terms. However, recent advances in understanding cryptic oxygen cycling, namely the ubiquitous one-electron reduction of O2 to superoxide by microorganisms outside the cell, remains unexplored as a potential player in global oxygen dynamics. Here we show that dark extracellular superoxide production by marine microbes represents a previously unconsidered global oxygen flux and sink comparable in magnitude to other key terms. We estimate that extracellular superoxide production represents a gross oxygen sink comprising about a third of marine gross oxygen production, and a net oxygen sink amounting to 15 to 50% of that. We further demonstrate that this total marine dark extracellular superoxide flux is consistent with concentrations of superoxide in marine environments. These findings underscore prolific marine sources of reactive oxygen species and a complex and dynamic oxygen cycle in which oxygen consumption and corresponding carbon oxidation are not necessarily confined to cell membranes or exclusively related to respiration. This revised model of the marine oxygen cycle will ultimately allow for greater reconciliation among estimates of primary production and respiration and a greater mechanistic understanding of redox cycling in the ocean.

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 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).…”

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).…”

Marine Dissolved Oxygen Prediction With Tree Tuned Deep Neural Network

“…The predictors we choose include temperature and salinity, since warmer water holds less oxygen and salinity also affect oxygen solubility [10]. Other factors, including biological activity [22], longitude and latitude, oceanatmosphere interactions and ocean circulations are considered to influence the concentration of oxygen too. So, we use phosphate, salinity, temperature, depth, silicate, longitude, latitude, and chlorophyll as the predictors in experiments.…”