Extensive PFAS accumulation by human gut bacteria
Anna E. LindelliD, Anne GrießhammeriD, Lena MichaelisiD, Dimitrios PapagiannidisiD, Hannah OchneriD, Stephan KamradiD, Rui GuaniD, Sonja BlascheiD, Leandro N. VentimigliaiD, Bini RamachandraniD, Hilal Ozgur, Aleksej ZelezniakiD, Nonantzin Beristain‐CovarrubiasiD, Juan Carlos Yam‐PuciD, Indra RouxiD, L. P. BarroniD, Alexandra K. Richardson, Maria Guerra Martin, Vladimı́r BenešiD, Nobuhiro MoroneiD, James E. D. ThaventhiraniD, Tanmay A. M. BharatiD, Mikhail M. SavitskiiD, Lisa MaieriD, Kiran Raosaheb PatiliD
Abstract
Per- and polyfluoroalkyl Substances (PFAS) - the so-called forever chemicals - are a major cause of environmental and health concern due to their toxicity and long-term persistence1,2. Yet, no efficient mechanisms for their removal have been identified. Here we report bioaccumulation of PFAS by several gut bacterial species over a wide range of concentrations from nanomolar up to 500 M. For bioaccumulating Bacteroides uniformis, a highly prevalent species, we estimate intracellular PFAS concentration in the mM range - above that of most native metabolites. Despite this high bioaccumulation, B. uniformis cells could grow appreciably up to 250 M perfluorononanoic acid (PFNA) exposure. Escherichia coli, which accumulated PFAS to a much lesser extent, substantially increased PFAS bioaccumulation when lacking TolC efflux pump indicating trans-membrane transport in PFAS bioaccumulation. Electron microscopy and cryogenic Focused Ion Beam-Secondary Ion Mass-spectrometry revealed distinct morphological changes and intracellular localisation of PFNA aggregates. Bioaccumulation of PFAS and transmembrane transport is also evident in proteomics, metabolomics, thermal proteome profiling, and mutations following adaptive laboratory evolution. In an in vivo context, mice colonized with human gut bacteria showed, compared to germ-free controls or those colonized with low-bioaccumulating bacteria, higher PFNA levels in excreted feces. As the gut microbiota is a critical interface between exposure and human body, our results have implications for understanding and utilizing microbial contribution to PFAS clearance.
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