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Flavin-Dependent Monooxygenases Involved in Bacterial Degradation of Chlorophenols

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Abstract

Aerobic bacterial degradation of chlorophenols in bacteria occurs via two main pathways and, first of all, depends on the degree of halogenation of the substrate. Mono- and dichlorophenols are hydroxylated to (chloro)catechols and are further metabolized by the ortho-clearance pathway. Polychlorinated phenols are utilized by bacteria via hydroquinone/hydroxyhydroquinone followed by the meta-cleavage of its aromatic ring with the formation of maleylacetate and then β-ketoadipate. Most research has been focused on organisms and catabolic pathways that involve the degradation of (chloro)aromatic substrates via catechols, while the alternative hydroquinone pathway remains poorly understood and described. This review provides information on the metabolic pathways of p-chloro-substituted phenols, where special attention is paid to flavin-dependent monooxygenases that catalyze the primary reactions of substrate oxidation.

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REFERENCES

  1. Czaplicka, M., Sci. Total Environ., 2004, vol. 322, nos. 1–3, pp. 21–39.https://doi.org/10.1016/j.scitotenv.2003.09.015

  2. Crawford, R.L., Jung, C.M., and Strap, J.L., Biodegradation, 2007, vol. 18, no. 5, pp. 525–539. https://doi.org/10.1007/s10532-006-9090-6

    Article  CAS  PubMed  Google Scholar 

  3. Arora, P.K.;. and Bae, H., Microb. Cell Fact., 2014, vol. 13, no. 1, p. 31. https://doi.org/10.1186/1475-2859-13-31

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Zaborina, O., Daubaras, D.L., Zago, A., Xun, L., Saido, K., Klem, T., Nikolic, D., and Chakrabarty, A.M., J. Bacteriol., 1998, vol. 180, no. 17, pp. 4667–4675. https://doi.org/10.1128/JB.180.17.4667-4675.1998

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Louie, T.M., Webster, C.M., and Xun, L., J. Bacteriol., 2002, vol. 184, no. 13, pp. 3492–3500. https://doi.org/10.1128/JB.184.13.3492-3500.2002

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Xun, L. and Webster, C.M., J. Biol. Chem., 2004, vol. 279, no. 8, pp. 6696–6700. https://doi.org/10.1074/jbc.M312072200

    Article  CAS  PubMed  Google Scholar 

  7. Hatta, T., Fujii, E., and Takizawa, N., Biosci. Biotechnol. Biochem., 2012, vol. 76, no. 5, pp. 892–899. https://doi.org/10.1271/bbb.110843

    Article  CAS  PubMed  Google Scholar 

  8. Nordin, K., Unell, M., and Jansson, J.K., Appl. Environ. Microbiol., 2005, vol. 71, no. 11, pp. 6538–6544. https://doi.org/10.1128/AEM.71.11.6538-6544.2005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Chenprakhon, P., Wongnate, T., and Chaiyen, P., Protein Sci., 2019, vol. 28, no. 1, pp. 8–29. https://doi.org/10.1002/pro.3525

    Article  CAS  PubMed  Google Scholar 

  10. Chenprakhon, P., Pimviriyakul, P., Tongsook, C., and Chaiyen, P., Enzymes, 2020, vol. 47, pp. 283–326. https://doi.org/10.1016/bs.enz.2020.05.008

    Article  CAS  PubMed  Google Scholar 

  11. van Berkel, W.J.H., Kamerbeek, N.M., and Fraaije, M.W., J. Biotechnol., 2006, vol. 124, no. 4, pp. 670–689. https://doi.org/10.1016/j.jbiotec.2006.03.044

    Article  CAS  PubMed  Google Scholar 

  12. Perry, L.L. and Zylstra, G.J., J. Bacteriol., 2007, vol. 189, no. 21, pp. 7563–7572. https://doi.org/10.1128/JB.01849-06

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Zhang, J.J., Liu, H., Xiao, Y., Zhang, X.E., and Zhou, N.Y., J. Bacteriol., 2009, vol. 191, no. 8, pp. 2703–2710. https://doi.org/10.1128/JB.01566-08

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Zhang, S., Sun, W., Xu, L., Zheng, X., Chu, X., Tian, J., Wu, N., and Fan, Y., BMC Microbiol., 2012, vol. 12, p. 27. https://doi.org/10.1186/1471-2180-12-27

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Wei, M., Zhang, J.-J., Liu, H., and Zhou, N.-Y., Biodegradation, 2010, vol. 21, no. 6, pp. 915–921. https://doi.org/10.1007/s10532-010-9351-2

    Article  CAS  PubMed  Google Scholar 

  16. Shen, W., Liu, W., Zhang, J., Tao, J., Deng, H., Cao, H., and Cui, Z., Bioresour. Technol., 2010, vol. 101, no. 19, pp. 7516–7522. https://doi.org/10.1016/j.biortech.2010.04.052

    Article  CAS  PubMed  Google Scholar 

  17. Kadiyala, V. and Spain, J.C., Appl. Environ. Microbiol., 1998, vol. 64, no. 7, pp. 2479–2484. https://doi.org/10.1128/AEM.64.7.2479-2484.1998

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Kitagawa, W., Kimura, N., and Kamagata, Y., J. Bacteriol., 2004, vol. 186, no. 15, pp. 4894–4902. https://doi.org/10.1128/JB.186.15.4894-4902.2004

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Takeo, M., Murakami, M., Niihara, S., Yamamoto, K., Nishimura, M., Kato, D., and Negoro, S., J. Bacteriol., 2008, vol. 190, no. 22, pp. 7367–7374. https://doi.org/10.1128/JB.00742-08

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Liu, P.P., Zhang, J.J., and Zhou, N.Y., Int. Biodeterior. Biodegrad., 2010, vol. 64, no. 4, pp. 293–299. https://doi.org/10.1016/j.ibiod.2010.03.001

    Article  CAS  Google Scholar 

  21. Yamamoto, K., Nishimura, M., Kato, D.I., Takeo, M., and Negoro, S., J. Biosci. Bioeng., 2011, vol. 111, no. 6, pp. 687–694. https://doi.org/10.1016/j.jbiosc.2011.01.016

    Article  CAS  PubMed  Google Scholar 

  22. Moiseeva, O.V., Solyanikova, I.P., Kaschabek, S.R., Groning, J., Thiel, M., Golovleva, L.A., and Schlomann, M., J. Bacteriol., 2002, vol. 184, no. 19, pp. 5282–5292. https://doi.org/10.1128/JB.184.19.5282-5292.2002

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Field, J.A. and Sierra-Alvarez, R., Biodegradation, 2008, vol. 19, no. 4, pp. 463–480. https://doi.org/10.1007/s10532-007-9155-1

    Article  CAS  PubMed  Google Scholar 

  24. Takeo, M., Yasukawa, T., Abe, Y., Niihara, S., Maeda, Y., and Negoro, S., J. Biosci. Bioeng., 2003, vol. 95, pp. 139–145.

    Article  CAS  PubMed  Google Scholar 

  25. Galan, B., Diaz, E., Prieto, M.A., and Garcia, J.L., J. Bacteriol., 2000, vol. 182, no. 3, pp. 627–636. https://doi.org/10.1128/JB.182.3.627-636.2000

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Min, J., Zhang, J.J., and Zhou, N.Y., Appl. Environ. Microbiol., 2014, vol. 80, no. 19, pp. 6212–6222. https://doi.org/10.1128/AEM.02093-14

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Spain, J.C. and Gibson, D.T., Appl. Environ. Microbiol., 1991, vol. 57, no. 3, pp. 812–819. https://doi.org/10.1128/aem.57.3.812-819.1991

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Wei, Q., Liu, H., Zhang, J.J., Wang, S.H., Xiao, Y., and Zhou, N.Y., Biodegradation, 2010, vol. 21, no. 4, pp. 575–584. https://doi.org/10.1007/s10532-009-9325-4

    Article  CAS  PubMed  Google Scholar 

  29. Bae, H.S., Lee, J.M., and Lee, S.-T., FEMS Microbiol. Lett., 1996, vol. 145, no. 1, pp. 125–129. https://doi.org/10.1111/j.1574-6968.1996.tb08566.x

    Article  CAS  PubMed  Google Scholar 

  30. Cho, Y.-G., Yoon, J.-H., Park, Y.-H., and Lee, S.-T., J. Gen. Appl. Microbiol., 1998, vol. 44, no. 5, pp. 303–309. https://doi.org/10.2323/jgam.44.303

    Article  CAS  PubMed  Google Scholar 

  31. Ferreira, M.I.M., Marchesi, J.R., and Janssen, D.B., Appl. Microbiol. Biotechnol., 2008, vol. 78, pp. 709–717. https://doi.org/10.1007/s00253-008-1343-3

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Chapman, P.J. and Hopper, D.J., Biochem. J., 1968, vol. 110, no. 3, pp. 491–498. https://doi.org/10.1042/bj1100491

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Webb, B.N., Ballinger, J.W., Kim, E., Belchik, S.M., Lam, Ka-Sum., Youn, B., Nissen, M.S., Xun, L., and Kang, C., J. Biol. Chem., 2010, vol. 285, no. 3, pp. 2014–2027. https://doi.org/10.1074/jbc.M109.056135

    Article  CAS  PubMed  Google Scholar 

  34. Danganan, C.E., Ye, R.W., Daubaras, D.L., Xun, L., and Chakrabarty, A.M., Appl. Environ. Microbiol., 1994, vol. 60, no. 11, pp. 4100–4106. https://doi.org/10.1128/aem.60.11.4100-4106.1994

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Daubaras, D.L., Saido, K., and Chakrabarty, A.M., Appl. Environ. Microbiol., 1996, vol. 62, no. 11, pp. 4276–4279. https://doi.org/10.1128/aem.62.11.4276-4279.1996

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Gisi, M.R. and Xun, L., J. Bacteriol., 2003, vol. 185, no. 9, pp. 2786–2792. https://doi.org/10.1128/JB.185.9.2786-2792.2003

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Hayes, R.P., Lewis, K.M., Xun, L., and Kang, C., J. Biol. Chem., 2013, vol. 288, no. 40, pp. 28447–28456. https://doi.org/10.1074/jbc.M113.499368

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Pimviriyakul, P. and Chaiyen, P., J. Biol. Chem., 2018, vol. 293, no. 48, pp. 18525–18539. https://doi.org/10.1074/jbc.RA118.005538

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Sanchez, M.A. and Gonzalez, B., Appl. Environ. Microbiol., 2007, vol. 73, no. 9, pp. 2769–2776. https://doi.org/10.1128/AEM.02584-06

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Hayes, R.P., Webb, B.N., Subramanian, A.K., Nissen, M., Popchock, A., Xun, L., and Kang, C., Int. J. Mol. Sci., 2012, vol. 13, no. 8, pp. 9769–9784. https://doi.org/10.3390/ijms13089769

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Kilbane, J.J., Chatterjee, D.K., Karns, J.S., Kellogg, S.T., and Chakrabarty, A.M., Appl. Environ. Microbiol., 1982, vol. 44, no. 1, pp. 72–78. https://doi.org/10.1128/aem.44.1.72-78.1982

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Lopez-Echartea, E., Macek, T., Demnerova, K., and Uhlik, O., Int. J. Environ. Res. Public Health, vol. 13, no. 11, p. 1146. https://doi.org/10.3390/ijerph13111146

  43. Copley, S.D., Rokicki, J., Turner, P., Daligault, H., Nolan, M., and Land, M., Genome Biol. Evol., 2012, vol. 4, no. 2, pp. 184–198. https://doi.org/10.1093/gbe/evr137

    Article  PubMed  Google Scholar 

  44. Cai, M. and Xun, L., J. Bacteriol., 2002, vol. 184, no. 17, pp. 4672–4680. https://doi.org/10.1128/JB.184.17.4672-4680.2002

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Dai, M., Rogers, J.B., Warner, J.R., and Copley, S.D., J. Bacteriol., 2003, vol. 185, no. 1, pp. 302–310. https://doi.org/10.1128/JB.185.1.302-310.2003

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Dai, M. and Copley, S.D., Appl. Environ. Microbiol., 2004, vol. 70, no. 4, pp. 2391–2397. https://doi.org/10.1128/AEM.70.4.2391-2397.2004

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Hlouchova, K., Rudolph, J., Pietari, J.M., Behlen, L.S., and Copley, S.D., Biochemistry, 2012, vol. 51, no. 18, pp. 3848–3860. https://doi.org/10.1021/bi300261p

    Article  CAS  PubMed  Google Scholar 

  48. Xun, L., Topp, E., and Orser, C.S., J. Bacteriol., 1992, vol. 174, no. 24, pp. 8003–8007. https://doi.org/10.1128/jb.174.24.8003-8007.1992

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Huang, Y., Xun, R., Chen, G., and Xun, L., J. Bacteriol., 2008, vol. 190, no. 23, pp. 7595–7600. https://doi.org/10.1128/JB.00489-08

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Xun, L., Bohuslavek, J., and Cai, M., Biochem. Biophys. Res. Commun., 1999, vol. 266, no. 2, pp. 322–325. https://doi.org/10.1006/bbrc.1999.1805

    Article  CAS  PubMed  Google Scholar 

  51. Xu, L., Lawson, S.L., Resing, K., Babbitt, P.C., and Copley, S.D., Biochemistry, 1999, vol. 38, no. 24, pp. 7659–7669. https://doi.org/10.1021/bi990103y

    Article  CAS  PubMed  Google Scholar 

  52. Ohtsubo, Y., Miyauchi, K., Kanda, K., Hatta, T., Kiyohara, H., Senda, T., Nagata, Y., Mitsui, Y., and Takagi, M., FEBS Lett., 1999, vol. 459, no. 3, pp. 395–398. https://doi.org/10.1016/S0014-5793(99)01305-8

    Article  CAS  PubMed  Google Scholar 

  53. Nagata, Y., Ohtsubo, Y., Endo, R., Ichikawa, N., Ankai, A., Oguchi, A., Fukui, S., Fujita, N., and Tsuda, M., J. Bacteriol., 2010, vol. 192, no. 21, pp. 5852–5853. https://doi.org/10.1128/JB.00961-10

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Neujahr, H.Y. and Gaal, A., Eur. J. Biochem., 1973, vol. 35, no. 2, pp. 386–400. https://doi.org/10.1111/j.1432-1033.1973.tb02851.x

    Article  CAS  PubMed  Google Scholar 

  55. van Berkel, W., Westphal, A., Eschrich, K., Eppink, M., and de Kok, A., Eur. J. Biochem., 1992, vol. 210, no. 2, pp. 411–419. https://doi.org/10.1111/j.1432-1033.1992.tb17436.x

    Article  CAS  PubMed  Google Scholar 

  56. Tiirola, M.A., Mannisto, M.K., Puhakka, J.A., and Kulomaa, M.S., Appl. Environ. Microbiol., 2002, vol. 68, no. 1, pp. 173–180. https://doi.org/10.1128/AEM.68.1.173-180.2002

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Tiirola, M.A., Wang, H., Paulin, L., and Kulomaa, M.S., Appl. Environ. Microbiol., 2002, vol. 68, no. 9, pp. 4495–4501. https://doi.org/10.1128/AEM.68.9.4495-4501.2002

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Cassidy, M.B., Lee, H., Trevors, J.T., and Zablotowicz, R.B., J. Ind. Microbiol. Biotechnol., 1999, vol. 23, nos. 4–5, pp. 232–241. https://doi.org/10.1038/sj.jim.2900749

    Article  CAS  PubMed  Google Scholar 

  59. Beaulieu, M., Becaert, V., Deschenes, L., and Villemur, R., Microb. Ecol., 2000, vol. 40, no. 4, pp. 345–355. https://doi.org/10.1007/s002480000055

    Article  CAS  PubMed  Google Scholar 

  60. Miyauchi, K., Suh, S.K., Nagata, Y., and Takagi, M., J. Bacteriol., 1998, vol. 180, no. 6, pp. 1354–1359. https://doi.org/10.1128/JB.180.6.1354-1359.1998

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Anandarajah, K., Kiefer, P.M., Donohoe, B.S., and Copley, S.D., Biochemistry, 2000, vol. 39, no. 18, pp. 5303–5311. https://doi.org/10.1021/bi9923813

    Article  CAS  PubMed  Google Scholar 

  62. Warner, J.R. and Copley, S.D., Biochemistry, 2007, vol. 46, no. 14, pp. 4438–4447. https://doi.org/10.1021/bi0620104

    Article  CAS  PubMed  Google Scholar 

  63. Endo, R., Kamakura, M., Miyauchi, K., Fukuda, M., Ohtsubo, Y., Tsuda, M., and Nagata, Y., J. Bacteriol., 2005, vol. 187, no. 3, pp. 847–853. https://doi.org/10.1128/JB.187.3.847-853.2005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Duffner, F.M., Kirchner, U., Bauer, M.P., and Muller, R., Gene, 2000, vol. 256, nos. 1–2, pp. 215–221. https://doi.org/10.1016/S0378-1119(00)00352-8

    Article  CAS  PubMed  Google Scholar 

  65. Kirchner, U., Westphal, A.H., Muller, R., and van Berkel, W.J., J. Biol. Chem., 2003, vol. 278, no. 48, pp. 47545–47553. https://doi.org/10.1074/jbc.M307397200

    Article  CAS  PubMed  Google Scholar 

  66. Heuvel, R.H., Westphal, A.H., Heck, A.J., Walsh, M.A., Rovida, S., van Berkel, W.J., and Mattevi, A., J. Biol. Chem., 2004, vol. 279, no. 13, pp. 12860–12867. https://doi.org/10.1074/jbc.M313765200

    Article  CAS  PubMed  Google Scholar 

  67. Duffner, F.M. and Muller, R., FEMS Microbiol. Lett., 1998, vol. 161, no. 1, pp. 37–45. https://doi.org/10.1111/j.1574-6968.1998.tb12926.x

    Article  CAS  PubMed  Google Scholar 

  68. Hubner, A., Danganan, C.E., Xun, L., Chakrabarty, A.M., and Hendrickson, W., Appl. Environ. Microbiol., 1998, vol. 64, no. 6, pp. 2086–2093. https://doi.org/10.1128/AEM.64.6.2086-2093.1998

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Takizawa, N., Yokoyama, H., Yanagihara, K., Hatta, T., and Kiyohara, H., J. Ferment. Bioeng., 1995, vol. 80, no. 4, pp. 318–326. https://doi.org/10.1016/0922-338X(95)94198-Z

    Article  CAS  Google Scholar 

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The study was performed within the framework of the state task of the Ministry of Education and Science of Russia no. 075-00326-19-00 on the topic no. AAAA-A18-118022190098-9.

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  1. Ufa Institute of Biology of Ufa Federal Research Center,Russian Academy of Sciences, 450054, Ufa, Russia

    N. V. Zharikova, V. V. Korobov & E. I. Zhurenko

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Zharikova, N.V., Korobov, V.V. & Zhurenko, E.I. Flavin-Dependent Monooxygenases Involved in Bacterial Degradation of Chlorophenols. Appl Biochem Microbiol 58, 677–691 (2022). https://doi.org/10.1134/S0003683822060175

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