Identification and characterization of the cytochrome p450 complement in <i>Streptomyces cavourensis</i> YBQ59

Ngoc Tung Quach; Thi Hanh Nguyen Vu; Thi  Mai Phuong Nguyen; Quyet Tien Phi; Thi Bich Thuy Ly

doi:10.15625/vjbt-21610

Author affiliations

Authors

Ngoc Tung Quach \(^1\) Institute of Biotechnology- Vietnam Academy of Science and Technology, 18 Hoang Quoc Viet, Ha Noi,10000, Vietnam.
Thi Hanh Nguyen Vu \(^1\) Institute of Biotechnology- Vietnam Academy of Science and Technology, 18 Hoang Quoc Viet, Ha Noi,10000, Vietnam.
Thi Mai Phuong Nguyen \(^1\) Institute of Biotechnology- Vietnam Academy of Science and Technology, 18 Hoang Quoc Viet, Ha Noi,10000, Vietnam.
Quyet Tien Phi \(^1\) Institute of Biotechnology- Vietnam Academy of Science and Technology, 18 Hoang Quoc Viet, Ha Noi,10000, Vietnam.
Thi Bich Thuy Ly \(^1\) Institute of Biotechnology- Vietnam Academy of Science and Technology, 18 Hoang Quoc Viet, Ha Noi,10000, Vietnam.

DOI:

https://doi.org/10.15625/vjbt-21610

Keywords:

cytochrome P450, ferredoxin, ferredoxin reductase, genome, streptomyces cavourensis

Abstract

Cytochrome P450 enzymes (CYPs) are regarded as some of the most versatile biocatalysts. They are attractive candidates for natural product development because of their ability to selectively oxidize a broad range of substrates. Streptomyces spp. are not only producers of biologically active secondary metabolites but also a rich source of P450 enzymes. However, only a limited number of studies have explored the function and potential of P450 enzymes encoded in the Streptomyces genomes. In this study, the endophytic Streptomyces cavourensis YBQ59 isolated from Cinnamomum cassia J. Presl was sequenced using the Illumina sequencing platform to identify its P450 enzymes. The genome of YBQ59 was approximately 8,126,002 bp in size, with a G + C content of 72.1% and contained 7,020 genes. Genome annotation identified 21 CYP genes, distributed across 10 CYP families and 17 subfamilies. The possible role of these P450 enzymes in the synthesis of secondary metabolites was discussed. Since CYPs often require electron transport proteins to function, we analyzed the physical map of the genes encoding ferredoxins and ferredoxin reductases found in the genome of S. cavourensis YBQ59. Additionally, a phylogenetic tree was constructed to compare the P450 enzyme system from S. cavourensis YBQ59 with those of closely related and well-studied Streptomyces species, including Streptomyces sp. CFMR7, S. fulvissimus DSM 40593, S. griseus IFO 13350, and S. globisporus 1912. These results provide a basis for exploiting potential P450 enzymes from S. cavourensis YBQ59 for agricultural and medicinal applications.

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References

Bernhardt R., 2006. Cytochromes P450 as versatile biocatalysts. Journal of Biotechnology, 124:128−145. https://doi.org/10.1016/j.jbiotec.2006.01.026

Bogazkaya A.M., von Bühler C.J., Kriening S., Busch A., Seifert A., Pleiss J., Laschat S., and Urlacher V.B., 2014. Selective allylic hydroxylation of acyclic terpenoids by CYP154E1 from Thermobifida fusca YX. Beilstein Journal of Organic Chemistry, 10: 1347−1353. https://doi.org/10.3762/bjoc.10.137

Cheng Q., Lamb D.C., Kelly S.L., Lei L., and Guengerich F.P., 2010. Cyclization of a cellular dipentaenone by Streptomyces coelicolor cytochrome P450 154A1 without oxidation/reduction. Journal of the American Chemical Society, 132: 15173−15175. https://doi.org/10.1021/ja107801v

Chong E.T.J., Chiang C., Png K.K., Abidueva E., Zaitseva S., Sun C., and Lee P.C., 2023. Dataset of the complete genome of Streptomyces cavourensis strain 2BA6PGT isolated from sediment from the bottom of the salt lake Verkhnee Beloe (Buryatia, Russia). Data in Brief, 46: 108877. https://doi.org/10.1016/j.dib.2022.108877

Dawson, J.H., Holm, R.H., Trudell, J.R., Barth, G., Linder, R.E., Bunnenberg, E., Djerassi, C., and Tang, S.C., 1976. Oxidized cytochrome P-450. Magnetic circular dichroism evidence for thiolate ligation in the substrate-bound form: Implications for the catalytic mechanism. Journal of the American Chemical Society, 98: 3707−3708. https://doi.org/10.1021/ja00428a054

Hannemann, F., Bichet, A., Ewen, K.M., and Bernhardt, R., 2007. Cytochrome P450 systems—biological variations of electron transport chains. Biochimica et Biophysica Acta, 1770: 330−344. https://doi.org/10.1016/j.bbagen.2006.07.017

Hasemann, C.A., Kurumbail, R.G., Boddupalli, S.S., Peterson, J.A., and Deisenhofer, J., 1995. Structure and function of cytochromes P450: a comparative analysis of three crystal structures. Structure, 3: 41−62. https://doi.org/10.1016/s0969-2126(01)00134-4

Huang, D.F., Xu, J.G., Liu, J.X., Zhang, H., and Hua, Q.P., 2014. Chemical constituents, antibacterial activity and mechanism of action of the essential oil from Cinnamomum cassia bark against four food-related bacteria. Microbiology, 83: 357−365. http://dx.doi.org/10.1134/S0026261714040067

Jackson, S.A., Crossman, L., Almeida, E.L., Margassery, L.M., Kennedy, J., and Dobson, A.D.W., 2018. Diverse and abundant secondary metabolism biosynthetic gene clusters in the genomes of marine sponge-derived Streptomyces spp. isolates. Marine Drugs, 16: 67. https://doi.org/10.3390/md16020067

Jensen, L. and Estrada, D.F., 2023. Characterization of a novel bifunctional cytochrome P450 enzyme CYP107 from bacterium Sebekia benihana. Journal of Pharmacology and Experimental Therapeutics, 385(S3): 580. https://doi.org/10.1124/jpet.122.260550

Johnston, J.B., Kells, P.M., Podust, L.M., and Ortiz de Montellano, P.R., 2009. Biochemical and structural characterization of CYP124: a methyl-branched lipid omega-hydroxylase from Mycobacterium tuberculosis. Proceedings of the National Academy of Sciences, 106: 20687−20692. https://doi.org/10.1073/pnas.0907398106

Khatri, Y., Ringle, M., Lisurek, M., von Kries, J.P., Zapp, J., and Bernhardt, R., 2016. Substrate hunting for the myxobacterial CYP260A1 revealed new 1α-hydroxylated products from C-19 steroids. ChemBioChem, 17(1): 90−101. https://doi.org/10.1002/cbic.201500420

Lamb, D.C., Ikeda, H., Nelson, D.R., Ishikawa, J., Skaug, T., Jackson, C., Omura, S., Waterman, M.R., and Kelly, S.L., 2003. Cytochrome P450 complement (CYPome) of the avermectin-producer Streptomyces avermitilis and comparison to that of Streptomyces coelicolor A3(2). Biochemical and Biophysical Research Communications, 307: 610−619. https://doi.org/10.1016/s0006291x(03)01231-2

Lei, L., Waterman, M.R., Fulco, A.J., Kelly, S.L., and Lamb, D.C., 2004. Availability of specific reductases controls the temporal activity of the cytochrome P450 complement of Streptomyces coelicolor A3(2). Proceedings of the National Academy of Sciences, 101: 494−499. https://doi.org/10.1073/pnas.2435922100

Li, X., Lei, X., Zhang, C., Jiang, Z., Shi, Y., Wang, S., Wang, L., and Hong, B., 2016. Complete genome sequence of Streptomyces globisporus C-1027, the producer of an enediyne antibiotic lidamycin. Journal of Biotechnology, 222: 9−10. https://doi.org/10.1016/j.jbiotec.2016.02.004

Lin, S., Ma, B., Gao, Q., Yang, J., Lai, G., Lin, R., Yang, B., Han, B.N., and Xu, L.H., 2022. The 16α-hydroxylation of progesterone by cytochrome P450 107X1 from Streptomyces avermitilis. ChemBioDivers, 19: e202200177. https://doi.org/10.1002/cbdv.202200177

Makino, T., Katsuyama, Y., Otomatsu, T., Misawa, N., and Ohnishi, Y., 2014. Regio- and stereospecific hydroxylation of various steroids at the 16α position of the D ring by the Streptomyces griseus cytochrome P450 CYP154C3. Applied and Environmental Microbiology, 80: 1371−1379. https://doi.org/10.1128/aem.03504-13

Martinis, S.A., Atkins, W.M., Stayton, P.S., and Sligar, S., 1989. A conserved residue of cytochrome P-450 is involved in heme-oxygen stability and activation. Journal of the American Chemical Society, 111: 9252−9253. https://doi.org/10.1021/ja00208a031

Milhim, M., Putkaradze, N., Abdulmughni, A., Kern, F., Hartz, P., and Bernhardt, R., 2016. Identification of a new plasmid-encoded cytochrome P450 CYP107DY1 from Bacillus megaterium with a catalytic activity towards mevastatin. Journal of Biotechnology, 240: 68−75. https://doi.org/10.1016/j.jbiotec.2016.11.002

Mnguni, F.C., Padayachee, T., Chen, W., Gront, D., Yu, J.H., Nelson, D.R., and Syed, K., 2020. More P450s are involved in secondary metabolite biosynthesis in Streptomyces compared to Bacillus, Cyanobacteria, and Mycobacterium. International Journal of Molecular Sciences, 21: 4814. https://doi.org/10.3390/ijms21134814

Myronovskyi, M., Tokovenko, B., Manderscheid, N., Petzke, L., and Luzhetskyy, A., 2013. Complete genome sequence of Streptomyces fulvissimus. Journal of Biotechnology, 168: 117−118. https://doi.org/10.1016/j.jbiotec.2013.08.013

Nanthini, J., Chia, K.H., Thottathil, G.P., Taylor, T.D., Kondo, S., Najimudin, N., Baybayan, P., Singh, S., and Sudesh, K., 2015. Complete genome sequence of Streptomyces sp. strain CFMR 7, a natural rubber degrading actinomycete isolated from Penang, Malaysia. Journal of Biotechnology, 214: 47−48. https://doi.org/10.1016/j.jbiotec.2015.09.007

Nguyen, K.T., Virus, C., Günnewich, N., Hannemann, F., and Bernhardt, R., 2012. Changing the regioselectivity of a P450 from C15 to C11 hydroxylation of progesterone. ChemBioChem, 13(8): 1161−1166. https://doi.org/10.1002/cbic.201100811

Nguyen, Q.H., Vu, N.T.H., Ha, H.C., Son, K.C., Ha, H., Thanh, T.T., Cuong, N., Linh, D.T.M., Hien, T.T.T., and Tien, Q.P., 2018. Draft genome sequence of Streptomyces cavourensis YBQ59, an endophytic producer of antibiotics bafilomycin D, nonactic acid, prelactone B, and 5,11-epoxy-10-cadinanol. Microbiology Resource Announcements, 7: e01056−18. https://doi.org/10.1128/mra.01056-18

Ohnishi, Y., Ishikawa, J., Hara, H., Suzuki, H., Ikenoya, M., Ikeda, H., Yamashita, A., Hattori, M., and Horinouchi, S., 2008. Genome sequence of the streptomycin-producing microorganism Streptomyces griseus IFO 13350. Journal of Bacteriology, 190: 4050−4060. https://doi.org/10.1128/jb.00204-08

Pandey, B.P., Lee, N., Choi, K.Y., Kim, J.N., Kim, E.J., and Kim, B.G., 2014. Identification of the specific electron transfer proteins, ferredoxin, and ferredoxin reductase, for CYP105D7 in Streptomyces avermitilis MA4680. Applied Microbiology and Biotechnology, 98: 5009−5017. https://doi.org/10.1007/s00253-014-5525-x

Parajuli, N., Basnet, D.B., Chan Lee, H., Sohng, J.K., and Liou, K., 2004. Genome analyses of Streptomyces peucetius ATCC 27952 for the identification and comparison of cytochrome P450 complement with other Streptomyces. Archives of Biochemistry and Biophysics, 425: 233−241. https://doi.org/10.1016/j.abb.2004.03.011

Podust, L.M., Kim, Y., Arase, M., Neely, B.A., Beck, B.J., Bach, H., Sherman, D.H., Lamb, D.C., Kelly, S.L., and Waterman, M.R., 2003. The 1.92-Å structure of Streptomyces coelicolor A3(2) CYP154C1. A new monooxygenase that functionalizes macrolide ring systems. Journal of Biological Chemistry, 278: 12214−12221. https://doi.org/10.1074/jbc.M212210200

Rudolf, J.D., Chang, C.Y., Ma, M., and Shen, B., 2017. Cytochromes P450 for natural product biosynthesis in Streptomyces: sequence, structure, and function. Nature Product Reports, 34: 1141−1172. https://doi.org/10.1039/c7np00034k

Rupasinghe, S., Schuler, M.A., Kagawa, N., Yuan, H., Lei, L., Zhao, B., Kelly, S.L., Waterman, M.R., and Lamb, D.C., 2006. The cytochrome P450 gene family CYP157 does not contain EXXR in the K-helix reducing the absolute conserved P450 residues to a single cysteine. FEBS Letters, 580: 6338−6342. https://doi.org/10.1016/j.febslet.2006.10.043

Senate, L.M., Tjatji, M.P., Pillay, K., Chen, W., Zondo, N.M., Syed, P.R., Mnguni, F.C., Chiliza, Z.E., Bamal, H.D., Karpoormath, R., Khoza, T., Mashele, S.S., Blackburn, J.M., Yu, J.H., Nelson, D.R., and Syed, K., 2019. Similarities, variations, and evolution of cytochrome P450s in Streptomyces versus Mycobacterium. Scientific Reports, 9: 3962. https://doi.org/10.1038/s41598-019-40646-y

Tangwattanachuleeporn, M., Ruangsuj, P., Yamprayoonswat, W., Sittihan, S., Jumpathong, W., and Yasawong, M., 2021. Genome sequence of Streptomyces cavourensis BUU135, isolated from soil from a tropical fruit farm in Thailand. Microbiology Resource Announcements, 10: e01428−20. https://doi.org/10.1128/mra.01428-20

Tian, Z., Cheng, Q., Yoshimoto, F.K., Lei, L., Lamb, D.C., and Guengerich, F.P., 2013. Cytochrome P450 107U1 is required for sporulation and antibiotic production in Streptomyces coelicolor. Archives of Biochemistry and Biophysics, 530: 101−107. https://doi.org/10.1016/j.abb.2013.01.001

Vargas, H.H.A., Santos, S.N., Padilla, G., and Melo, I.S., 2019. Genome sequence of Streptomyces cavourensis 1AS2a, a rhizobacterium isolated from the Brazilian Cerrado Biome. Microbiology Resource Announcements, 8: e00065−19. https://doi.org/10.1128/mra.00065-19

Vu, H.T., Nguyen, D.T., Nguyen, H.Q., Chu, H.H., Chu, S.K., Chau, M.V., and Phi, Q.T., 2018. Antimicrobial and cytotoxic properties of bioactive metabolites produced by Streptomyces cavourensis YBQ59 isolated from Cinnamomum cassia Prels in Yen Bai province of Vietnam. Current Microbiology, 75: 1247−1255. https://doi.org/10.1007/s00284-018-1517-x

Watve, M.G., Tickoo, R., Jog, M.M., and Bhole, B.D., 2001. How many antibiotics are produced by the genus Streptomyces? Archives of Microbiology, 176: 386−390. https://doi.org/10.1007/s002030100345

Xu, L.H., Fushinobu, S., Takamatsu, S., Wakagi, T., Ikeda, H., and Shoun, H., 2010. Regio- and stereospecificity of filipin hydroxylation sites revealed by crystal structures of cytochrome P450 105P1 and 105D6 from Streptomyces avermitilis. Journal of Biological Chemistry, 285: 16844−16853. https://doi.org/10.1074/jbc.M109.092460