The environmental fate of nucleic acids (i.e., DNA and RNA) has broad implications for diverse fields, including microbial ecology, ecological risk assessment of emerging RNA-based biopesticides, and biogeochemical cycling of phosphorous. As long polymers, nucleic acids strongly bind to surfaces (e.g., minerals in soil) because, they attach to surfaces at multiple binding sites. Consequently, adsorption at mineral-water interfaces plays an important role in determining the environmental fate of nucleic acids. For example, adsorption to mineral-water interfaces is well-established to retard the enzymatic hydrolysis of DNA and increase the persistence of DNA in the environment. However, similar stabilization effects have not been reported for RNA. To explain this difference, we hypothesized that adsorption of RNA to minerals present in soils mediates RNA degradation by catalyzing the hydrolysis of phosphodiester bonds. To test this hypothesis, we determined that RNA specifically adsorbed to the mineral goethite underwent abiotic hydrolysis with half-lives on the timescale of 6-12 hours at neutral pH. RNA degradation was impeded by adsorption competitors like organic matter and orthophosphate. We determined phosphodiester bond hydrolysis was the dominant degradation mechanism by identifying monophosphate nucleotides as primary reaction products. With these results, we propose that the mechanism of goethite-mediated RNA hydrolysis involves nucleophilic attacks on the phosphorus atoms facilitated by iron coordination. Some other metal (hydr)oxides (e.g., hematite) also catalyzed RNA hydrolysis after hours of adsorption, indicating this reaction might be common in soils. Our results suggest mineral-mediated RNA hydrolysis, a novel pathway, may explain the low persistence of RNA in soils.

Mineral-catalyzed RNA hydrolysis

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ACS Fall 2022

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