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

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.

The regulation of oxygen to low concentrations in marine oxygen-minimum zones

The Bay of Bengal hosts persistent, measurable, but sub-micromolar, concentrations of oxygen in its oxygen-minimum zone (OMZ). Such low-oxygen conditions are not necessarily rare in the global ocean and seem also to characterize the OMZ of the Pescadero Basin in the Gulf of California, as well as the outer edges of otherwise anoxic OMZs, such as can be found, for example, in the Eastern Tropical North Pacific. We show here that biological controls on oxygen consumption are required to allow the semistable persistence of low-oxygen conditions in OMZ settings; otherwise, only small changes in physical mixing or rates of primary production would drive the OMZ between anoxic and oxic states with potentially large swings in oxygen concentration. We propose that two controls are active: an oxygen-dependent control on oxygen respiration and an oxygen inhibition of denitrification. These controls, working alone and together, can generate low-oxygen concentrations over a wide variability in ocean mixing parameters. More broadly, we discuss the oxygen regulation of organic matter cycling and N2 production in OMZ settings. Modern biogeochemical models of nitrogen and oxygen cycling in OMZ settings do contain some of the parameterizations that we explore here. However, these models have not been applied to understanding the persistence of low, but measurable, concentrations of oxygen in settings like the Bay of Bengal, nor have they been applied to understanding what biological/physical processes control the transition from a weakly oxygenated state to a “functionally” anoxic state with implications for nitrogen cycling. Therefore, we believe that the approach here illuminates the relationship between oxygen and the biogeochemical cycling of carbon and nitrogen in settings like the Bay of Bengal. Furthermore, we believe that our results could further inform large-scale ocean models seeking to explore how global warming might influence the spread of low-oxygen waters, influencing the cycles of oxygen, carbon, and nitrogen in OMZ settings.

Plankton

Healthy waterways and oceans are essential for our increasingly urbanised world. Yet monitoring water quality in aquatic environments is a challenge, as it varies from hour to hour due to stormwater and currents. Being at the base of the aquatic food web and present in huge numbers, plankton are strongly influenced by changes in environment and provide an indication of water quality integrated over days and weeks. Plankton are the aquatic version of a canary in a coal mine. They are also vital for our existence, providing not only food for fish, seabirds, seals and sharks, but producing oxygen, cycling nutrients, processing pollutants, and removing carbon dioxide from our atmosphere. This Second Edition of Plankton is a fully updated introduction to the biology, ecology and identification of plankton and their use in monitoring water quality. It includes expanded, illustrated descriptions of all major groups of freshwater, coastal and marine phytoplankton and zooplankton and a new chapter on teaching science using plankton. Best practice methods for plankton sampling and monitoring programs are presented using case studies, along with explanations of how to analyse and interpret sampling data. Plankton is an invaluable reference for teachers and students, environmental managers, ecologists, estuary and catchment management committees, and coastal engineers.

The effects of marine eukaryote evolution on phosphorus, carbon and oxygen cycling across the Proterozoic–Phanerozoic transition

A ‘Neoproterozoic oxygenation event’ is widely invoked as a causal factor in animal evolution, and often attributed to abiotic causes such as post-glacial pulses of phosphorus weathering. However, recent evidence suggests a series of transient ocean oxygenation events ∼660–520 Ma, which do not fit the simple model of a monotonic rise in atmospheric oxygen (pO2). Hence, we consider mechanisms by which the evolution of marine eukaryotes, coupled with biogeochemical and ecological feedbacks, potentially between alternate stable states, could have caused changes in ocean carbon cycling and redox state, phosphorus cycling and atmospheric pO2. We argue that the late Tonian ocean ∼750 Ma was dominated by rapid microbial cycling of dissolved organic matter (DOM) with elevated nutrient (P) levels due to inefficient removal of organic matter to sediments. We suggest the abrupt onset of the eukaryotic algal biomarker record ∼660–640 Ma was linked to an escalation of protozoan predation, which created a ‘biological pump’ of sinking particulate organic matter (POM). The resultant transfer of organic carbon (Corg) and phosphorus to sediments was strengthened by subsequent eukaryotic innovations, including the advent of sessile benthic animals and mobile burrowing animals. Thus, each phase of eukaryote evolution tended to lower P levels and oxygenate the ocean on ∼104 year timescales, but by decreasing Corg/P burial ratios, tended to lower atmospheric pO2 and deoxygenate the ocean again on ∼106 year timescales. This can help explain the transient nature and ∼106 year duration of oceanic oxygenation events through the Cryogenian–Ediacaran–Cambrian.

Cryptic oxygen cycling in anoxic marine zones

Oxygen availability drives changes in microbial diversity and biogeochemical cycling between the aerobic surface layer and the anaerobic core in nitrite-rich anoxic marine zones (AMZs), which constitute huge oxygen-depleted regions in the tropical oceans. The current paradigm is that primary production and nitrification within the oxic surface layer fuel anaerobic processes in the anoxic core of AMZs, where 30–50% of global marine nitrogen loss takes place. Here we demonstrate that oxygenic photosynthesis in the secondary chlorophyll maximum (SCM) releases significant amounts of O2to the otherwise anoxic environment. The SCM, commonly found within AMZs, was dominated by the picocyanobacteriaProchlorococcusspp. Free O2levels in this layer were, however, undetectable by conventional techniques, reflecting a tight coupling between O2production and consumption by aerobic processes under apparent anoxic conditions. Transcriptomic analysis of the microbial community in the seemingly anoxic SCM revealed the enhanced expression of genes for aerobic processes, such as nitrite oxidation. The rates of gross O2production and carbon fixation in the SCM were found to be similar to those reported for nitrite oxidation, as well as for anaerobic dissimilatory nitrate reduction and sulfate reduction, suggesting a significant effect of local oxygenic photosynthesis on Pacific AMZ biogeochemical cycling.