Dynamics of Reactive Oxygen Species and Nitrogen Cycling in Soils as a Mechanism for Volatile Reactive Nitrogen Oxide Production

Abstract

Heterotrophic bacteria and fungi are responsible for the decomposition of organic matter in soil. During this process, reactive oxygen species (ROS) can be produced directly and indirectly as extracellular byproducts of respiration. It is well known that nitrogen (N) cycle processes lead to the formation of volatile reactive nitrogen oxides (NOy), a group of climate-active gases that contribute to atmospheric chemistry and negatively impact human health. Primary microbial sources of NOy include ammonia- oxidising bacteria and denitrifying bacteria and fungi. Despite soil being a significant source of global NOy emissions, studies to date have primarily focused on N emissions from agricultural soils and there remains a large scope for investigating mechanisms of soil NOy production in a wider context in order to better constrain terrestrial and climate process models. Here, we propose a potential microbial mechanism involving ROS that could influence the production of NOy from soil. We utilised metagenomics and metatranscriptomics alongside continuous gas flux measurements and analysis of soil properties to evaluate the connection between microbial ROS and soil-sourced NOy. Our findings suggest that more NOy, particularly nitric oxide (NO), is produced in the presence of increased abundance of ammonia-oxidising and denitrifying taxa. NO can be lost to the environment or reacts with superoxide, an ROS produced via the enzymatic activity of soil organic matter (SOM) decomposers. This reaction produces peroxynitrite (ONOO-), which we have demonstrated to enhance nitrogen dioxide (NO2) emissions from soil. We have shown that the extent of NOy production through this pathway may be dependent on SOM composition, and the associated variability in carbon and nitrogen content.