Abstract
Sugar O-methylation shields algal polysaccharides against microbial hydrolytic enzymes. Here, we describe cytochrome P450 monooxygenases from marine bacteria that, together with appropriate redox-partner proteins, catalyze the oxidative demethylation of 6-O-methyl-d-galactose, which is an abundant monosaccharide of the algal polysaccharides agarose and porphyran. This previously unknown biological function extends the group of carbohydrate-active enzymes to include the class of cytochrome P450 monooxygenases.
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Change history
08 March 2018
In the version of this article originally published, the line of conditions shown for NADH in Figure 2b was shifted out of place. The error has been corrected in the HTML and PDF versions of the article.
References
Field, C. B., Behrenfeld, M. J., Randerson, J. T. & Falkowski, P. Science 281, 237–240 (1998).
Kraan, S. in Carbohydrates–Comprehensive Studies on Glycobiology and Glycotechnology (ed. Chang, C.-F.) Ch. 22 https://doi.org/10.5772/51572 (INTECH Open Access Publisher, 2012).
Wargacki, A. J. et al. Science 335, 308–313 (2012).
Motone, K., Takagi, T., Sasaki, Y., Kuroda, K. & Ueda, M. J. Biotechnol. 231, 129–135 (2016).
Panagiotopoulos, C., Repeta, D. J., Mathieu, L., Rontani, J. F. & Sempéré, R. Mar. Chem. 154, 34–45 (2013).
Gabrielii, I., Gatenholm, P., Glasser, W. G., Jain, R. K. & Kenne, L. Carbohydr. Polym. 43, 367–374 (2000).
Hehemann, J. H., Kelly, A. G., Pudlo, N. A., Martens, E. C. & Boraston, A. B. Proc. Natl. Acad. Sci. USA 109, 19786–19791 (2012).
Rees, D. A. & Conway, E. Biochem. J. 84, 411–416 (1962).
Chiovitti, A., Bacic, A., Craik, D. J., Kraft, G. T. & Liao, M. L. Carbohydr. Res. 339, 1459–1466 (2004).
Guengerich, F. P. Chem. Res. Toxicol. 14, 611–650 (2001).
Lewis, J. C. et al. Proc. Natl. Acad. Sci. USA 106, 16550–16555 (2009).
Katagiri, M., Ganguli, B. N. & Gunsalus, I. C. J. Biol. Chem. 243, 3543–3546 (1968).
Janusz, G., Kucharzyk, K. H., Pawlik, A., Staszczak, M. & Paszczynski, A. J. Enzyme Microb. Technol. 52, 1–12 (2013).
Hemsworth, G. R. et al. J. Am. Chem. Soc. 135, 6069–6077 (2013).
Levasseur, A., Drula, E., Lombard, V., Coutinho, P. M. & Henrissat, B. Biotechnol. Biofuels 6, 41 (2013).
Yin, D. T. et al. Nat. Commun. 6, 10197 (2015).
Vuong, T. V., Liu, B., Sandgren, M. & Master, E. R. Biomacromolecules 18, 610–616 (2017).
Mann, A. J. et al. Appl. Environ. Microbiol. 79, 6813–6822 (2013).
Girhard, M., Tieves, F., Weber, E., Smit, M. S. & Urlacher, V. B. Appl. Microbiol. Biotechnol. 97, 1625–1635 (2013).
Kim, H. T., Lee, S., Kim, K. H. & Choi, I. G. Bioresour. Technol. 107, 301–306 (2012).
Girhard, M. et al. Microb. Cell Fact. 8, 36 (2009).
Nickerson, D. P. & Wong, L. L. Protein Eng. 10, 1357–1361 (1997).
Li, C. et al. BMC Biotechnol. 11, 92 (2011).
Purdy, M. M., Koo, L. S., Ortiz de Montellano, P. R. & Klinman, J. P. Biochemistry 43, 271–281 (2004).
Omura, T. & Sato, R. J. Biol. Chem. 239, 2370–2378 (1964).
Jefcoate, C. R. Methods Enzymol. 52, 258–279 (1978).
Ruiz-Matute, A. I., Hernández-Hernández, O., Rodríguez-Sánchez, S., Sanz, M. L. & Martínez-Castro, I. J. Chromatogr. B Analyt. Technol. Biomed. Life Sci. 879, 1226–1240 (2011).
Kumar, S., Stecher, G. & Tamura, K. Mol. Biol. Evol. 33, 1870–1874 (2016).
Altschul, S. F., Gish, W., Miller, W., Myers, E. W. & Lipman, D. J. J. Mol. Biol. 215, 403–410 (1990).
Edgar, R. C. Nucleic Acids Res. 32, 1792–1797 (2004).
Hehemann, J. H., Smyth, L., Yadav, A., Vocadlo, D. J. & Boraston, A. B. J. Biol. Chem. 287, 13985–13995 (2012).
Finn, R. D. et al. Nucleic Acids Res. 44, D279–D285 (2016). D1.
Yin, Y. et al. Nucleic Acids Res. 40, W445–W451 (2012).
Krzywinski, M. et al. Genome Res. 19, 1639–1645 (2009).
Krogh, A., Larsson, B., von Heijne, G. & Sonnhammer, E. L. J. Mol. Biol. 305, 567–580 (2001).
Acknowledgements
We thank the German Research Foundation (DFG) for funding through the Research Unit FOR2406. J.-H.H. acknowledges funding by the Emmy Noether Program of the DFG, grant number HE 7217/1-1. We are also grateful to V. Urlacher (Düsseldorf, Germany) for providing the genes encoding P450cam, PdX, PdR and CPR. We thank D. Nelson (Memphis, USA) for assigning the P450s to a subfamily in the P450 database.
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J.-H.H., T.S. and U.T.B. initiated the study and directed the project. J.E. together with L.R. cloned, expressed and purified the P450 enzymes and performed preliminary studies; H.C.B. and L.R. cloned, expressed and purified all other enzymes and performed all further experiments. S.T. and J.-H.H. performed the computational analysis. L.R., H.C.B., J.-H.H. and U.T.B. prepared the manuscript, which was revised and approved by all authors.
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A correction to this article is available online at https://doi.org/10.1038/s41589-018-0020-9.
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Reisky, L., Büchsenschütz, H.C., Engel, J. et al. Oxidative demethylation of algal carbohydrates by cytochrome P450 monooxygenases. Nat Chem Biol 14, 342–344 (2018). https://doi.org/10.1038/s41589-018-0005-8
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DOI: https://doi.org/10.1038/s41589-018-0005-8
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