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Ehrl, B. ; Mogusu, E.O. ; Kim, K.* ; Hofstetter, H.* ; Pedersen, J.A.* ; Elsner, M.

High permeation rates in liposome systems explain rapid glyphosate biodegradation associated with strong isotope fractionation.

Environ. Sci. Technol. 52, 7259-7268 (2018)

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Bacterial uptake of charged organic pollutants such as the widely used herbicide glyphosate is typically attributed to active transporters, whereas passive membrane permeation as an uptake pathway is usually neglected. For 1-palmitoyl-2-oleoyl-snglycero-3-phosphocholine (POPC) liposomes, the pH-dependent apparent membrane permeation coefficients (P-app) of glyphosate, determined by nuclear magnetic resonance (NMR) spectroscopy, varied from P-app (pH 7.0) = 3.7 (+/- 0.3) x 10(-7) m.s(-1) to P-app (pH 4.1) = 4.2 (+/- 0.1) x 10(-6) m.s(-1). The magnitude of this surprisingly rapid membrane permeation depended on glyphosate speciation and was, at circumneutral pH, in the range of polar, noncharged molecules. These findings point to passive membrane permeation as a potential uptake pathway during glyphosate biodegradation. To test this hypothesis, a Gram-negative glyphosate degrader, Ochrobactrum sp. FrEM, was isolated from glyphosate-treated soil and glyphosate permeation rates inferred from the liposome model system were compared to bacterial degradation rates. Estimated maximum permeation rates were, indeed, 2 orders of magnitude higher than degradation rates of glyphosate. In addition, biodegradation of millimolar glyphosate concentrations gave rise to pronounced carbon isotope fractionation with an apparent kinetic isotope effect, AKIE(carbon), of 1.014 +/- 0.003. This value lies in the range typical of non-masked enzymatic isotope fractionation demonstrating that glyphosate biodegradation was not subject to mass transfer limitations and glyphosate exchange across the cell membrane was rapid relative to enzymatic turnover.

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