Abstract
Since ancient times, people have been attracted by dyes and they were a symbol of power. Some of the oldest dyes are indigo and its derivative Tyrian purple, which were extracted from plants and snails, respectively. These ‘indigoid dyes’ were and still are used for coloration of textiles and as a food additive. Traditional Chinese medicine also knows indigoid dyes as pharmacologically active compounds and several studies support their effects. Further, they are interesting for future technologies like organic electronics. In these cases, especially the indigo derivatives are of interest but unfortunately hardly accessible by chemical synthesis. In recent decades, more and more enzymes have been discovered that are able to produce these indigoid dyes and therefore have gained attention from the scientific community. In this study, group E monooxygenases (styrene monooxygenase and indole monooxygenase) were used for the selective oxygenation of indole (derivatives). It was possible for the first time to show that the product of the enzymatic reaction is an epoxide. Further, we synthesized and extracted indigoid dyes and could show that there is only minor by-product formation (e.g. indirubin or isoindigo). Thus, group E monooxygenase can be an alternative biocatalyst for the biosynthesis of indigoid dyes.
Funding source: Sächsische Aufbaubank
Award Identifier / Grant number: 100263733
Funding statement: This research was funded by the Saxon Government (SAB) Sächsische Aufbaubank, Funder Id: http://dx.doi.org/10.13039/501100006298, grant number: 100263733 and the DECHEMA (Max-Buchner Fellowship to D.T.) grant number MBFSt 3339. We thank Jan Zuber from the Institute for Analytical Chemistry and Lucas Siegel (TU Bergakademie Freiberg) for support in the implementation of the analytics.
References
Arora, P.K., Sharma, A., and Bae, H. (2015). Microbial degradation of indole and its derivatives. J. Chem. 2015, 1–13.10.1155/2015/129159Search in Google Scholar
Boyd, C., Larkin, M.J., Reid, K.A., Sharma, N.D., and Wilson, K. (1997). Metabolism of naphthalene, 1-naphthol, indene, and indole by Rhodococcus sp. strain NCIMB 12038. Appl. Environ. Microbiol. 63, 151–155.10.1128/aem.63.1.151-155.1997Search in Google Scholar
Cerniglia, C.E., Freeman, J.P., and Evans, F.E. (1984). Evidence for an arene oxide-NIH shift pathway in the transformation of naphthalene to 1-naphthol by Bacillus cereus. Arch. Microbiol. 138, 283–286.10.1007/BF00410891Search in Google Scholar
Dua, A., Chauhan, K., and Pathak, H. (2014). Biotransformation of indigo pigment by indigenously isolated Pseudomonas sp. HAV-1 and assessment of its antioxidant property. Biotechnol. Res. Int. 2014, 109249.10.1155/2014/109249Search in Google Scholar
Dupard-Julien, C.L., Kandlakunta, B., and Uppu, R.M. (2007). Determination of epoxides by high-performance liquid chromatography following derivatization with N,N-diethyldithiocarbamate. Anal. Bioanal. Chem. 387, 1027–1032.10.1007/s00216-006-1003-3Search in Google Scholar
Eisenbrand, G., Hippe, F., Jakobs, S., and Muehlbeyer, S. (2004). Molecular mechanisms of indirubin and its derivatives: novel anticancer molecules with their origin in traditional Chinese phytomedicine. J. Cancer Res. Clin. Oncol. 130, 627–635.10.1007/s00432-004-0579-2Search in Google Scholar
Ensley, B.D., Ratzkin, B.J., Osslund, T.D., Simon, M.J., Wackett, L.P., and Gibson, D.T. (1983). Expression of naphthalene oxidation genes in Escherichia coli results in the biosynthesis of indigo. Science 222, 167–169.10.1126/science.6353574Search in Google Scholar
Farias-Silva, E., Cola, M., Calvo, T.R., Barbastefano, V., Ferreira, A.L., De Paula Michelatto, D., Alves de Almeida, A.C., Hiruma-Lima, C.A., Vilegas, W., and Brito, A.R. (2007). Antioxidant activity of indigo and its preventive effect against ethanol-induced DNA damage in rat gastric mucosa. Planta Med. 73, 1241–1246.10.1055/s-2007-981613Search in Google Scholar
Fleischmann, C., Lievenbrück, M., and Ritter, H. (2015). Polymers and dyes. Developments and applications. Polymers 7, 717–746.10.3390/polym7040717Search in Google Scholar
Fujioka, M. and Wada, H. (1968). The bacterial oxidation of indole. Biochim. Biophys. Acta Gen. Subj. 158, 70–78.10.1016/0304-4165(68)90073-1Search in Google Scholar
Fukuoka, K., Tanaka, K., Ozeki, Y., and Kanaly, R.A. (2015). Biotransformation of indole by Cupriavidus sp. strain KK10 proceeds through N-heterocyclic- and carbocyclic-aromatic ring cleavage and production of indigoids. Int. Biodeterior. Biodegradation 97, 13–24.10.1016/j.ibiod.2014.11.007Search in Google Scholar
Glawischnig, E., Grün, S., Frey, M., and Gierl, A. (1999). Cytochrome P450 monooxygenases of DIBOA biosynthesis. Specificity and conservation among grasses. Phytochemistry 50, 925–930.10.1016/S0031-9422(98)00318-5Search in Google Scholar
Głowacki, E.D., Voss, G., Leonat, L., Irimia-Vladu, M., Bauer, S., and Sariciftci, N.S. (2012). Indigo and tyrian purple – from ancient natural dyes to modern organic semiconductors. Isr. J. Chem. 52, 540–551.10.1002/ijch.201100130Search in Google Scholar
Gröning, J.A.D., Kaschabek, S.R., Schlömann, M., and Tischler, D. (2014). A mechanistic study on SMOB-ADP1: an NADH:flavin oxidoreductase of the two-component styrene monooxygenase of Acinetobacter baylyi ADP1. Arch. Microbiol. 196, 829–845.10.1007/s00203-014-1022-ySearch in Google Scholar PubMed
Guengerich, F.P., Martin, M.V., McCormick, W.A., Nguyen, L.P., Glover, E., and Bradfield, C.A. (2004a). Aryl hydrocarbon receptor response to indigoids in vitro and in vivo. Arch. Biochem. Biophys. 423, 309–316.10.1016/j.abb.2004.01.002Search in Google Scholar PubMed
Guengerich, F.P., Sorrells, J.L., Schmitt, S., Krauser, J.A., Aryal,P., and Meijer, L. (2004b). Generation of new protein kinase inhibitors utilizing cytochrome p450 mutant enzymes for indigoid synthesis. J. Med. Chem. 47, 3236–3241.10.1021/jm030561bSearch in Google Scholar PubMed
Gursky, L.J., Nikodinovic-Runic, J., Feenstra, K.A., and O’Connor, K.E. (2010). In vitro evolution of styrene monooxygenase from Pseudomonas putida CA-3 for improved epoxide synthesis. Appl. Microbiol. Biotechnol. 85, 995–1004.10.1007/s00253-009-2096-3Search in Google Scholar PubMed
Harrer, R. (2012). Indigo auf Speicherchips. Chem. Unser. Zeit 46, 136.10.1002/ciuz.201290032Search in Google Scholar
He, B., Pun, A.B., Zherebetskyy, D., Liu, Y., Liu, F., Klivansky, L.M., McGough, A.M., Zhang, B.A., Lo, K., Russell, T.P., et al. (2014). New form of an old natural dye: bay-annulated indigo (BAI) as an excellent electron accepting unit for high performance organic semiconductors. J. Am. Chem. Soc. 136, 15093–15101.10.1021/ja508807mSearch in Google Scholar PubMed
Heine, T., Großmann, C., Hofmann, S., and Tischler, D. (2018a). Enzymgesteuerte Indigoproduktion. Biospektrum 24, 446–448.10.1007/s12268-018-0938-1Search in Google Scholar
Heine, T., van Berkel, W.J.H., Gassner, G., van Pée, K.-H., and Tischler, D. (2018b). Two-component fad-dependent monooxygenases. Current knowledge and biotechnological opportunities. Biology (Basel) 7, 42.10.3390/biology7030042Search in Google Scholar
Heine, T., Zimmerling, J., Ballmann, A., Kleeberg, S.B., Rückert, C., Busche, T., Winkler, A., Kalinowski, J., Poetsch, A., Scholtissek, A., et al. (2018c). On the enigma of glutathione-dependent styrene degradation in Gordonia rubripertincta CWB2. Appl. Environ. Microbiol. 84, e00154-18.10.1128/AEM.00154-18Search in Google Scholar
Hoessel, R., Leclerc, S., Endicott, J.A., Nobel, M.E., Lawrie, A., Tunnah, P., Leost, M., Damiens, E., Marie, D., Marko, D., et al. (1999). Indirubin, the active constituent of a Chinese antileukaemia medicine, inhibits cyclin-dependent kinases. Nat. Cell Biol. 1, 60–67.10.1038/9035Search in Google Scholar
Hössel, R. (1999). Synthese von Derivaten des Indirubins und Untersuchungen zur Mechanismusaufklärung ihrer antineoplastischen Wirkung.Search in Google Scholar
Hsu, T.M., Welner, D.H., Russ, Z.N., Cervantes, B., Prathuri, R.L., Adams, P.D., and Dueber, J.E. (2018). Employing a biochemical protecting group for a sustainable indigo dyeing strategy. Nat. Chem. Biol. 14, 256–261.10.1038/nchembio.2552Search in Google Scholar
Irimia-Vladu, M., Głowacki, E.D., Troshin, P.A., Schwabegger, G., Leonat, L., Susarova, D.K., Krystal, O., Ullah, M., Kanbur, Y., Bodea, M.A., et al. (2012). Indigo – a natural pigment for high performance ambipolar organic field effect transistors and circuits. Adv. Mater. Weinheim 24, 375–380.10.1002/adma.201102619Search in Google Scholar
Kapadia, G.J., Tokuda, H., Sridhar, R., Balasubramanian, V., Takayasu, J., Bu, P., Konoshima, T., and Nishino, H. (1998). Cancer chemopreventive activity of synthetic colorants used in foods, pharmaceuticals and cosmetic preparations. Cancer Lett. 129, 87–95.10.1016/S0304-3835(98)00087-1Search in Google Scholar
Kim, J. and Park, W. (2015). Indole: a signaling molecule or a mere metabolic byproduct that alters bacterial physiology at a high concentration? J. Microbiol. 53, 421–428.10.1007/s12275-015-5273-3Search in Google Scholar
Kunikata, T., Tatefuji, T., Aga, H., Iwaki, K., Ikeda, M., and Kurimoto, M. (2000). Indirubin inhibits inflammatory reactions in delayed-type hypersensitivity. Eur. J. Pharmacol. 410, 93–100.10.1016/S0014-2999(00)00879-7Search in Google Scholar
Leclerc, S., Garnier, M., Hoessel, R., Marko, D., Bibb, J.A., Snyder, G.L., Greengard, P., Biernat, J., Wu, Y.Z., Mandelkow, E.M., et al. (2001). Indirubins inhibit glycogen synthase kinase-3 beta and CDK5/p25, two protein kinases involved in abnormal tau phosphorylation in Alzheimer’s disease. A property common to most cyclin-dependent kinase inhibitors? J. Biol. Chem. 276, 251–260.10.1074/jbc.M002466200Search in Google Scholar PubMed
Lee, J.-H., Wood, T.K., and Lee, J. (2015). Roles of indole as an interspecies and interkingdom signaling molecule. Trends Microbiol. 23, 707–718.10.1016/j.tim.2015.08.001Search in Google Scholar PubMed
Li, G. and Young, K.D. (2013). Indole production by the tryptophanase TnaA in Escherichia coli is determined by the amount of exogenous tryptophan. Microbiology (Reading) 159, 402–410.10.1099/mic.0.064139-0Search in Google Scholar PubMed
Lin, G.-H., Chen, H.-P., Huang, J.-H., Liu, T.-T., Lin, T.-K., Wang, S.-J., Tseng, C.-H., and Shu, H.-Y. (2012). Identification and characterization of an indigo-producing oxygenase involved in indole 3-acetic acid utilization by Acinetobacter baumannii. Antonie van Leeuwenhoek 101, 881–890.10.1007/s10482-012-9704-4Search in Google Scholar PubMed
Lin, G.-H., Chen, H.-P., Shu, H.-Y., and Lee, S.-W. (2015). Detoxification of indole by an indole-induced flavoprotein oxygenase from Acinetobacter baumannii. PLoS One 10, e0138798.10.1371/journal.pone.0138798Search in Google Scholar PubMed PubMed Central
Ma, Q., Qu, Y., Zhang, X., Liu, Z., Li, H., Zhang, Z., Wang, J., Shen,W., and Zhou, J. (2015). Systematic investigation and microbial community profile of indole degradation processes in two aerobic activated sludge systems. Sci. Rep. 5, 17674.10.1038/srep17674Search in Google Scholar PubMed PubMed Central
Ma, Q., Liu, Z., Yang, B., Dai, C., and Qu, Y. (2018a). Characterization and functional gene analysis of a newly isolated indole-degrading bacterium Burkholderia sp. IDO3. J. Hazard. Mater. 367, 144–151.10.1016/j.jhazmat.2018.12.068Search in Google Scholar PubMed
Ma, Q., Zhang, X., and Qu, Y. (2018b). Biodegradation and biotransformation of indole. Advances and perspectives. Front. Microbiol. 9, 2625.10.3389/fmicb.2018.02625Search in Google Scholar PubMed PubMed Central
McClay, K., Boss, C., Keresztes, I., and Steffan, R.J. (2005). Mutations of toluene-4-monooxygenase that alter regiospecificity of indole oxidation and lead to production of novel indigoid pigments. Appl. Environ. Microbiol. 71, 5476–5483.10.1128/AEM.71.9.5476-5483.2005Search in Google Scholar PubMed PubMed Central
Mermod, N., Harayama, S., and Timmis, K.N. (1986). New route to bacterial production of indigo. Nat. Biotechnol. 4, 321–324.10.1038/nbt0486-321Search in Google Scholar
Meyer, A. (2002). Hydroxylation of indole by laboratory-evolved 2-hydroxybiphenyl 3-monooxygenase. J. Biol. Chem. 277, 34161–34167.10.1074/jbc.M205621200Search in Google Scholar PubMed
Miyamoto, K., Okuro, K., and Ohta, H. (2007). Substrate specificity and reaction mechanism of recombinant styrene oxide isomerase from Pseudomonas putida S12. Tetrahedron Lett. 48, 3255–3257.10.1016/j.tetlet.2007.03.016Search in Google Scholar
Montersino, S., Tischler, D., Gassner, G.T., and van Berkel, W.J.H. (2011). Catalytic and structural features of flavoprotein hydroxylases and epoxidases. Adv. Synth. Catal. 353, 2301–2319.10.1002/adsc.201100384Search in Google Scholar
Murdock, D., Ensley, B.D., Serdar, C., and Thalen, M. (1993). Construction of metabolic operons catalyzing the de novo biosynthesis of indigo in Escherichia coli. Bio/Technology 11, 381–386.10.1038/nbt0393-381Search in Google Scholar PubMed
Namgung, S., Park, H.A., Kim, J., Lee, P.-G., Kim, B.-G., Yang, Y.-H., and Choi, K.-Y. (2019). Ecofriendly one-pot biosynthesis of indigo derivative dyes using CYP102G4 and PrnA halogenase. Dyes Pigm. 162, 80–88.10.1016/j.dyepig.2018.10.009Search in Google Scholar
O’Connor, K.E., Dobson, A.D., and Hartmans, S. (1997). Indigo formation by microorganisms expressing styrene monooxygenase activity. Appl. Environ. Microbiol. 63, 4287–4291.10.1128/aem.63.11.4287-4291.1997Search in Google Scholar PubMed PubMed Central
Otto, K., Hofstetter, K., Röthlisberger, M., Witholt, B., and Schmid,A. (2004). Biochemical characterization of StyAB from Pseudomonas sp. strain VLB120 as a two-component flavin-diffusible monooxygenase. J. Bacteriol. 186, 5292–5302.10.1128/JB.186.16.5292-5302.2004Search in Google Scholar PubMed PubMed Central
Pathak, H. and Madamwar, D. (2010). Biosynthesis of indigo dye by newly isolated naphthalene-degrading strain Pseudomonas sp. HOB1 and its application in dyeing cotton fabric. Appl. Biochem. Biotechnol. 160, 1616–1626.10.1007/s12010-009-8638-4Search in Google Scholar PubMed
Paul, C.E., Tischler, D., Riedel, A., Heine, T., Itoh, N., and Hollmann, F. (2015). Nonenzymatic regeneration of styrene monooxygenase for catalysis. ACS Catal. 5, 2961–2965.10.1021/acscatal.5b00041Search in Google Scholar
Perpète, E.A., Preat, J., André, J.-M., and Jacquemin, D. (2006). An ab initio study of the absorption spectra of indirubin, isoindigo, and related derivatives. J. Phys. Chem. A 110, 5629–5635.10.1021/jp060069eSearch in Google Scholar PubMed
Petermayer, C. and Dube, H. (2018). Indigoid photoswitches. Visible light responsive molecular tools. Acc. Chem. Res. 51, 1153–1163.10.1021/acs.accounts.7b00638Search in Google Scholar PubMed
Qu, Y., Ma, Q., Liu, Z., Wang, W., Tang, H., Zhou, J., and Xu, P. (2017). Unveiling the biotransformation mechanism of indole in a Cupriavidus sp. strain. Mol. Microbiol. 106, 905–918.10.1111/mmi.13852Search in Google Scholar PubMed
Riedel, A., Heine, T., Westphal, A.H., Conrad, C., Rathsack, P., van Berkel, W.J.H., and Tischler, D. (2015). Catalytic and hydrodynamic properties of styrene monooxygenases from Rhodococcus opacus 1CP are modulated by cofactor binding. AMB Express 5, 112.10.1186/s13568-015-0112-9Search in Google Scholar PubMed PubMed Central
Sadauskas, M., Vaitekūnas, J., Gasparavičiūtė, R., and Meškys,R. (2017). Indole biodegradation in Acinetobacter sp. strain O153. Genetic and biochemical characterization. Appl. Environ. Microbiol. 83.10.1128/AEM.01453-17Search in Google Scholar PubMed PubMed Central
Sambrook, J. and Russell, D.W., eds. (2001). Molecular Cloning. A Laboratory Manual. (Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press).Search in Google Scholar
Sharma, V., Kumar, P., and Pathak, D. (2010). Biological importance of the indole nucleus in recent years: a comprehensive review. J. Heterocyclic Chem. 39, 491–502.10.1002/jhet.349Search in Google Scholar
Studier, F.W. (2005). Protein production by auto-induction in high density shaking cultures. Protein Expr. Purif. 41, 207–234.10.1016/j.pep.2005.01.016Search in Google Scholar PubMed
Tan, C., Zhang, X., Zhu, Z., Xu, M., Yang, T., Osire, T., Yang, S., and Rao, Z. (2019). Asp305Gly mutation improved the activity and stability of the styrene monooxygenase for efficient epoxide production in Pseudomonas putida KT2440. Microb. Cell. Fact. 18, 12. doi: 10.1186/s12934-019-1065-5.10.1186/s12934-019-1065-5Search in Google Scholar PubMed PubMed Central
Tischler, D., Eulberg, D., Lakner, S., Kaschabek, S.R., van Berkel, W.J.H., and Schlömann, M. (2009). Identification of a novel self-sufficient styrene monooxygenase from Rhodococcus opacus 1CP. J. Bacteriol. 191, 4996–5009.10.1128/JB.00307-09Search in Google Scholar PubMed PubMed Central
Tischler, D., Kermer, R., Gröning, J.A.D., Kaschabek, S.R., van Berkel, W.J.H., and Schlömann, M. (2010). StyA1 and StyA2B from Rhodococcus opacus 1CP: a Multifunctional styrene monooxygenase system. J. Bacteriol. 192, 5220–5227.10.1128/JB.00723-10Search in Google Scholar PubMed PubMed Central
Tischler, D., Gröning, J.A.D., Kaschabek, S.R., and Schlömann, M. (2012). One-component styrene monooxygenases: an evolutionary view on a rare class of flavoproteins. Appl. Biochem. Biotechnol. 167, 931–944.10.1007/s12010-012-9659-ySearch in Google Scholar PubMed
Tischler, D., Schwabe, R., Siegel, L., Joffroy, K., Kaschabek, S., Scholtissek, A., and Heine, T. (2018). VpStyA1/VpStyA2B of Variovorax paradoxus EPS. An aryl alkyl sulfoxidase rather than a styrene epoxidizing monooxygenase. Molecules (Basel, Switzerland) 23, 809. doi: 10.3390/molecules23040809.10.3390/molecules23040809Search in Google Scholar PubMed PubMed Central
Toda, H., Imae, R., Komio, T., and Itoh, N. (2012). Expression and characterization of styrene monooxygenases of Rhodococcus sp. ST-5 and ST-10 for synthesizing enantiopure (S)-epoxides. Appl. Microbiol. Biotechnol. 96, 407–418.10.1007/s00253-011-3849-3Search in Google Scholar PubMed
Uehara, K., Takagishi, K., and Tanaka, M. (1987). The Al/Indigo/Au photovoltaic cell. Solar Cells 22, 295–301.10.1016/0379-6787(87)90059-7Search in Google Scholar
van Hellemond, E.W., Janssen, D.B., Fraaije, M.W., Janssen, D.B., and Fraaije, M.W. (2007). Discovery of a novel styrene monooxygenase originating from the metagenome. Appl. Environ. Microbiol. 73, 5832–5839.10.1128/AEM.02708-06Search in Google Scholar PubMed PubMed Central
Wu, Z.-L., Aryal, P., Lozach, O., Meijer, L., and Guengerich, F.P. (2005). Biosynthesis of new indigoid inhibitors of protein kinases using recombinant cytochrome P450 2A6. Chem. Biodivers. 2, 51–65.10.1002/cbdv.200490166Search in Google Scholar PubMed
Xiao, Z., Hao, Y., Liu, B., and Qian, L. (2002). Indirubin and meisoindigo in the treatment of chronic myelogenous leukemia in China. Leuk. Lymphoma 43, 1763–1768.10.1080/1042819021000006295Search in Google Scholar PubMed
Yuan, L.-J. (2011). Biooxidation of indole and characteristics of the responsible enzymes. Afr. J. Biotechnol. 10, 83B807F36739.10.5897/AJBX11.008Search in Google Scholar
Zhang, X., Jing, J., Zhang, L., Song, Z., Zhou, H., Wu, M., Qu, Y., and Liu, L. (2018). Biodegradation characteristics and genomic functional analysis of indole-degrading bacterial strain Acinetobacter sp. JW. J. Chem. Technol. Biotechnol. Doi: 10.1002/jctb.5858.10.1002/jctb.5858Search in Google Scholar
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