Examining the Influence of Reactive Oxygen Species on “Respiration” Isotope Effects

Abstract:

The biogeochemical fluxes that produce and consume O₂ play a critical role in regulating Earth’s climate and habitability. The measurement of the triple oxygen isotope (TOI) composition of O₂ is a valuable tool used to understand the nature of these fluxes in the environment. The TOI composition of O₂ is determined by biogeochemical processes that produce, consume, and physically transport O₂ (e.g. photosynthesis, respiration, and atmospheric circulation) and their respective fractionation factors. TOI measurements of dissolved oxygen in seawater are a particularly powerful tool for quantifying primary productivity in the marine environment. However, recent work has demonstrated that our understanding of the isotope effects of respiration is lacking and may be a source of significant uncertainty in measurements of marine gross primary productivity. In this study, we take a close look at the role of one of the simplest oxyanions, superoxide, and examine its influence on the TOI composition of dissolved oxygen through cryptic recycling of oxygen. There is growing recognition that the production of reactive oxygen species (ROS) of both intracellular and extracellular origin is widespread in the microbial world. Microorganisms degrade these ROS using a suite of enzymes including superoxide dismutases (SODs), catalase, and peroxidases. Several of these enzymes degrade ROS through disproportionation reactions, which recycle oxygen and have considerable leverage on the oxygen isotope composition of dissolved oxygen. We combine an isotope modeling approach and isotopic studies of representative SOD and catalase enzymes to demonstrate that modulation in ROS production is sufficient to reconcile significant disparities in respiration isotope effects. We argue that a more comprehensive consideration of ROS-mediated recycling of O₂ is needed to improve oxygen isotope based estimates of gross primary productivity and our overall understanding of electron flows in the global ocean.