Prions Adhere to Soil Minerals and Remain Infectious

Abstract

An unidentified environmental reservoir of infectivity contributes to the natural transmission of prion diseases (transmissible spongiform encephalopathies [TSEs]) in sheep, deer, and elk. Prion infectivity may enter soil environments via shedding from diseased animals and decomposition of infected carcasses. Burial of TSE-infected cattle, sheep, and deer as a means of disposal has resulted in unintentional introduction of prions into subsurface environments. We examined the potential for soil to serve as a TSE reservoir by studying the interaction of the disease-associated prion protein (PrP^Sc) with common soil minerals. In this study, we demonstrated substantial PrP^Sc adsorption to two clay minerals, quartz, and four whole soil samples. We quantified the PrP^Sc-binding capacities of each mineral. Furthermore, we observed that PrP^Sc desorbed from montmorillonite clay was cleaved at an N-terminal site and the interaction between PrP^Sc and Mte was strong, making desorption of the protein difficult. Despite cleavage and avid binding, PrP^Sc bound to Mte remained infectious. Results from our study suggest that PrP^Sc released into soil environments may be preserved in a bioavailable form, perpetuating prion disease epizootics and exposing other species to the infectious agent. Transmissible spongiform encephalopathies (TSEs) are a group of incurable diseases likely caused by a misfolded form of the prion protein (PrP^Sc). TSEs include scrapie in sheep, bovine spongiform encephalopathy (“mad cow” disease) in cattle, chronic wasting disease (CWD) in deer and elk, and Creutzfeldt-Jakob disease in humans. Scrapie and CWD are unique among TSEs because they can be transmitted between animals, and the disease agents appear to persist in environments previously inhabited by infected animals. Soil has been hypothesized to act as a reservoir of infectivity, because PrP^Sc likely enters soil environments through urinary or alimentary shedding and decomposition of infected animals. In this manuscript, the authors test the potential for soil to serve as a reservoir for PrP^Sc and TSE infectivity. They demonstrate that PrP^Sc binds to a variety of soil minerals and to whole soils. They also quantitate the levels of protein binding to three common soil minerals and show that the interaction of PrP^Sc with montmorillonite, a common clay mineral, is remarkably strong. PrP^Sc bound to Mte remained infectious to laboratory animals, suggesting that soil can serve as a reservoir of TSE infectivity.