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Aerobic radical polymerization mediated by microbial metabolism

Abstract

Performing radical polymerizations under ambient conditions is a major challenge because molecular oxygen is an effective radical quencher. Here we show that the facultative electrogen Shewanella oneidensis can control metal-catalysed living radical polymerizations under apparent aerobic conditions by first consuming dissolved oxygen via aerobic respiration, and then directing extracellular electron flux to a metal catalyst. In both open and closed containers, S. oneidensis enabled living radical polymerizations without requiring the preremoval of oxygen. Polymerization activity was closely tied to S. oneidensis anaerobic metabolism through specific extracellular electron transfer proteins and was effective for a variety of monomers using low (parts per million) concentrations of metal catalysts. Finally, polymerizations survived repeated challenges of oxygen exposure and could be initiated using lyophilized or spent (recycled) cells. Overall, our results demonstrate how the unique ability of S. oneidensis to use both oxygen and metals as respiratory electron acceptors can be leveraged to address salient challenges in polymer synthesis.

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Fig. 1: Carbon oxidation in S. oneidensis is coupled to either oxygen reduction under aerobic conditions or EET pathways under anaerobic conditions.
Fig. 2: S. oneidensis rapidly consumes dissolved oxygen and activates radical polymerization in cultures for which no additional steps were taken to remove oxygen.
Fig. 3: S. oneidensis strain and Cu(ii/i) ligand control polymerization kinetics under anaerobic and aerobic conditions.
Fig. 4: Radical polymerization was effective for a variety of metal catalysts in addition to Cu.
Fig. 5: Aerobic S. oneidensis polymerizations can be used to prepare block copolymers and restarts automatically after multiple oxygen exposures.
Fig. 6: Aerobic polymerizations are effective using lyophilized and spent S. oneidensis cells.

Data availability

Raw data supporting the findings in this study are available through the Texas Data Repository (https://doi.org/10.18738/T8/KHF1AY).

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Acknowledgements

We thank G. Bora, J. Imbrogno, M. Chwatko and J. Wagner for their experimental assistance. S. oneidensis knockouts were a generous gift from J. Gralnick. A.J.G. was supported through a National Science Foundation Graduate Research Fellowship (Program Award no. DGE-1610403). J.K. was supported through the Welch Foundation (Grant H-F-0001) during the Welch Summer Scholars Program. We gratefully acknowledge the use of facilities within the core microscopy lab of the Institute for Cellular and Molecular Biology, University of Texas at Austin. H. Alper is thanked for the use of a BioLector Pro. The research reported in this publication was supported by the National Institute of General Medical Sciences of the National Institutes of Health under Award no. R35GM133640. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health. Additional research support was provided by the Welch Foundation (Grants F-1929 and F-1904) and by the National Science Foundation through the Center for Dynamics and Control of Materials—an NSF Materials Research Science and Engineering Center under Cooperative Agreement DMR- 1720595. NMR spectra were collected on a Bruker Avance III 500 funded by the NIH (Award 1 S10 OD021508-01) and a Bruker Avance III HD 400 funded by the NSF (Award CHE 1626211).

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G.F., A.J.G., N.A.L. and B.K.K. designed the research; G.F., A.J.G. and J.K. performed the research; N.A.L. contributed new reagents and analytic tools; G.F., A.J.G., N.A.L. and B.K.K. analysed the data and wrote the paper.

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Correspondence to Benjamin K. Keitz.

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Supplementary Information containing a description of the Materials and Methods, Tables 1–5 and Figs. 1–24.

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Fan, G., Graham, A.J., Kolli, J. et al. Aerobic radical polymerization mediated by microbial metabolism. Nat. Chem. 12, 638–646 (2020). https://doi.org/10.1038/s41557-020-0460-1

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