Biosynthesis of polybrominated aromatic organic compounds by marine bacteria

Nature Chemical Biology

Volumn 10, Issue 8, 2014, Pages 640-647

  Agarwal, Vinayak ^a   El Gamal, Abrahim A ^a   Yamanaka, Kazuya ^b,e   Poth, Dennis ^b   Kersten, Roland D ^b,e,f   Schorn, Michelle ^b   Allen, Eric E ^a,b,c   Moore, Bradley S ^a,b,d  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^c UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^d UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^e CHISSO CORPORATION   (Japan)

^f SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AROMATIC COMPOUND; BACTERIAL ENZYME; BROMINASE; ORGANOBROMINE DERIVATIVE; PHENOL DERIVATIVE; POLYBROMINATED DIPHENYL ETHER; PYRROLE DERIVATIVE; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BIOMASS PRODUCTION; BIOSYNTHESIS; BIOTA; BROMINATION; CONTROLLED STUDY; DECARBOXYLATION; HALOGENATION; IN VITRO STUDY; MARINE BACTERIUM; MOLECULAR MODEL; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PSEUDOALTEROMONAS; SEQUENCE DATABASE;

BACTERIA (MICROORGANISMS);

AQUATIC ORGANISMS; GENOME, BACTERIAL; HALOGENATED DIPHENYL ETHERS; HALOGENATION; MOLECULAR SEQUENCE DATA; MULTIGENE FAMILY; OXIDOREDUCTASES; PSEUDOALTEROMONAS; PYRROLES;

EID: 84904748135     PISSN: 15524450     EISSN: 15524469     Source Type: Journal    
DOI: 10.1038/nchembio.1564     Document Type: Article

References (55)

1. Gribble, G.W. Te natural production of organobromine compounds. Environ. Sci. Pollut. Res. Int. 7, 37-47 (2000).
2. Gribble, G.W. Naturally Occurring Organohalogen Compounds- a Comprehensive Update. Vol. 91 (Springer Vienna, 2010).
3. Liu, Y.N. et al. Spatial and temporal distributions of bromoform and dibromomethane in the Atlantic Ocean and their relationship with photosynthetic biomass. J. Geophys. Res.-Oceans 118, 3950-3965 (2013).
4. Al-Mourabit, A., Zancanella, M.A., Tilvi, S. & Romo, D. Biosynthesis, asymmetric synthesis, and pharmacology, including cellular targets, of the pyrrole-2-aminoimidazole marine alkaloids. Nat. Prod. Rep. 28, 1229-1260 (2011).
5. Gaul, S. et al. Identifcation of the natural product 2, 3, 4, 5-tetrabromo-1-methylpyrrole in Pacifc biota, passive samplers and seagrass from Queensland, Australia. Mar. Pollut. Bull. 62, 2463-2468 (2011).
6. Kitamura, M., Koyama, T., Nakano, Y. & Uemura, D. Corallinafuran and Corallinaether, novel toxic compounds from crustose coralline red algae. Chem. Lett. 34, 1272-1273 (2005).
7. Kuniyoshi, M., Yamada, K. & Higa, T. A biologically-active diphenyl ether from the green-alga Cladophora fascicularis. Experientia 41, 523-524 (1985).
8. Malmväm, A., Zebuhr, Y., Kautsky, L., Bergman, K. & Asplund, L. Hydroxylated and methoxylated polybrominated diphenyl ethers and polybrominated dibenzo-p-dioxins in red alga and cyanobacteria living in the Baltic Sea. Chemosphere 72, 910-916 (2008).
9. King, G.M., Giray, C. & Kornfeld, I. Biogeographical, biochemical and genetic diferentiation among North-American Saccoglossids (Hemichordata, Enteropneusta, Harrimaniidae). Mar. Biol. 123, 369-377 (1995).
10. Unson, M.D., Holland, N.D. & Faulkner, D.J. A brominated secondary metabolite synthesized by the cyanobacterial symbiont of a marine sponge and accumulation of the crystalline metabolite in the sponge tissue. Mar. Biol. 119, 1-11 (1994).
11. Calcul, L. et al. NMR strategy for unraveling structures of bioactive sponge-derived oxy-polyhalogenated diphenyl ethers. J. Nat. Prod. 72, 443-449 (2009).
12. Löfstrand, K. et al. Brominated phenols, anisoles, and dioxins present in blue mussels from the Swedish coastline. Environ. Sci. Pollut. Res. Int. 17, 1460-1468 (2010).
13. Vetter, W., Scholz, E., Gaus, C., Müller, J.F. & Haynes, D. Anthropogenic and natural organohalogen compounds in blubber of dolphins and dugongs (Dugong dugon) from northeastern Australia. Arch. Environ. Contam. Toxicol. 41, 221-231 (2001).
14. Marsh, G. et al. Identifcation, quantifcation, and synthesis of a novel dimethoxylated polybrominated biphenyl in marine mammals caught of the coast of Japan. Environ. Sci. Technol. 39, 8684-8690 (2005).
15. Teuten, E.L., Xu, L. & Reddy, C.M. Two abundant bioaccumulated halogenated compounds are natural products. Science 307, 917-920 (2005).
16. Wan, Y. et al. Origin of hydroxylated brominated diphenyl ethers: natural compounds or man-made fame retardants? Environ. Sci. Technol. 43, 7536-7542 (2009).
17. Ren, X.M. & Guo, L.H. Molecular toxicology of polybrominated diphenyl ethers: nuclear hormone receptor mediated pathways. Environ. Sci. Process. Impacts 15, 702-708 (2013).
18. T, against methicillin-resistant Staphylococcus aureus. Antimicrob. Agents Chemother. 47, 480-488 (2003).
19. Andersen, R.J., Wolfe, M.S. & Faulkner, D.J. Autotoxic antibiotic production by a marine chromobacterium. Mar. Biol. 27, 281-285 (1974).
20. Burkholder, P.R., Pfster, R.M. & Leitz, F.H. Production of a pyrrole antibiotic by a marine bacterium. Appl. Microbiol. 14, 649-653 (1966).
21. Holmström, C. & Kjelleberg, S. Marine Pseudoalteromonas species are associated with higher organisms and produce biologically active extracellular agents. FEMS Microbiol. Ecol. 30, 285-293 (1999).
22. Vetter, W. Polyhalogenated alkaloids in environmental and food samples. Alkaloids Chem. Biol. 71, 211-276 (2012).
23. Rypien, K.L., Ward, J.R. & Azam, F. Antagonistic interactions among coral-associated bacteria. Environ. Microbiol. 12, 28-39 (2010).
24. Dorrestein, P.C., Yeh, E., Garneau-Tsodikova, S., Kelleher, N.L. & Walsh, C.T. Dichlorination of a pyrrolyl-S-carrier protein by FADH2-dependent halogenase PltA during pyoluteorin biosynthesis. Proc. Natl. Acad. Sci. USA 102, 13843-13848 (2005).
25. Peschke, J.D., Hanefeld, U. & Laatsch, H. Biosynthesis of the marine antibiotic pentabromopseudilin. 2. Te pyrrole ring. Biosci. Biotechnol. Biochem. 69, 628-630 (2005).
26. T). Stand. Genomic Sci. 6, 63-73 (2012).
27. Donia, M.S., Fricke, W.F., Ravel, J. & Schmidt, E.W. Variation in tropical reef symbiont metagenomes defned by secondary metabolism. PLoS ONE 6, e17897 (2011).
28. Sorokin, D.Y., Tourova, T.P., Lysenko, A.M., Mityushina, L.L. & Kuenen, J.G. Tioalkalivibrio thiocyanoxidans sp. Nov. and Tioalkalivibrio paradoxus sp. Nov., novel alkaliphilic, obligately autotrophic, sulfur-oxidizing bacteria capable of growth on thiocyanate, from soda lakes. Int. J. Syst. Evol. Microbiol. 52, 657-664 (2002).
29. Walsh, C.T., Garneau-Tsodikova, S. & Howard-Jones, A.R. Biological formation of pyrroles: nature's logic and enzymatic machinery. Nat. Prod. Rep. 23, 517-531 (2006).
30. Buedenbender, S., Rachid, S., Muller, R. & Schulz, G.E. Structure and action of the myxobacterial chondrochloren halogenase CndH: a new variant of FAD-dependent halogenases. J. Mol. Biol. 385, 520-530 (2009).
31. van Pée, K.H. Enzymatic chlorination and bromination. Methods Enzymol. 516, 237-257 (2012).
32. Eichhorn, E., van der Ploeg, J.R. & Leisinger, T. Characterization of a two-component alkanesulfonate monooxygenase from Escherichia coli. J. Biol. Chem. 274, 26639-26646 (1999).
33. Blasiak, L.C. & Drennan, C.L. Structural perspective on enzymatic halogenation. Acc. Chem. Res. 42, 147-155 (2009).
34. Gribble, G.W. Occurrence of halogenated alkaloids. Alkaloids Chem. Biol. 71, 1-165 (2012).
35. Hanefeld, U., Floss, H.G. & Laatsch, H. Biosynthesis of the marine antibiotic pentabromopseudilin. 1. Te benzene-ring. J. Org. Chem. 59, 3604-3608 (1994).
36. Walsh, C.T. & Wencewicz, T.A. Flavoenzymes: versatile catalysts in biosynthetic pathways. Nat. Prod. Rep. 30, 175-200 (2013).
37. Hewson, W.D. & Hager, L.P. Bromoperoxidases and halogenated lipids in marine-algae. J. Phycol. 16, 340-345 (1980).
38. Borchardt, S.A. et al. Reaction of acylated homoserine lactone bacterial signaling molecules with oxidized halogen antimicrobials. Appl. Environ. Microbiol. 67, 3174-3179 (2001).
39. Beissner, R.S., Guilford, W.J., Coates, R.M. & Hager, L.P. Synthesis of brominated heptanones and bromoform by a bromoperoxidase of marine origin. Biochemistry 20, 3724-3731 (1981).
40. Fehér, D., Barlow, R., McAtee, J. & Hemscheidt, T.K. Highly brominated antimicrobial metabolites from a marine Pseudoalteromonas sp. J. Nat. Prod. 73, 1963-1966 (2010).
41. Mas, S. et al. Comprehensive liquid chromatography-ion-spray tandem mass spectrometry method for the identifcation and quantifcation of eight hydroxylated brominated diphenyl ethers in environmental matrices. J. Mass Spectrom. 42, 890-899 (2007).
42. Makino, M. et al. Crystal structures and catalytic mechanism of cytochrome P450 StaP that produces the indolocarbazole skeleton. Proc. Natl. Acad. Sci. USA 104, 11591-11596 (2007).
43. Ballou, D.P., Entsch, B. & Cole, L.J. Dynamics involved in catalysis by single-component and two-component favin-dependent aromatic hydroxylases. Biochem. Biophys. Res. Commun. 338, 590-598 (2005).
44. Eppink, M.H., Cammaart, E., Van Wassenaar, D., Middelhoven, W.J. & van Berkel, W.J. Purifcation and properties of hydroquinone hydroxylase, a FAD-dependent monooxygenase involved in the catabolism of 4-hydroxybenzoate in Candida parapsilosis CBS604. Eur. J. Biochem. 267, 6832-6840 (2000).
45. Eppink, M.H., Boeren, S.A., Vervoort, J. & van Berkel, W.J. Purifcation and properties of 4-hydroxybenzoate 1-hydroxylase (decarboxylating), a novel favin adenine dinucleotide-dependent monooxygenase from Candida parapsilosis CBS604. J. Bacteriol. 179, 6680-6687 (1997).
46. Blunt, J.W., Copp, B.R., Keyzers, R.A., Munro, M.H. & Prinsep, M.R. Marine natural products. Nat. Prod. Rep. 30, 237-323 (2013).
47. Wiseman, S.B. et al. Polybrominated diphenyl ethers and their hydroxylated/methoxylated analogs: environmental sources, metabolic relationships, and relative toxicities. Mar. Pollut. Bull. 63, 179-188 (2011).
48. Ucán-Marin, F., Arukwe, A., Mortensen, A.S., Gabrielsen, G.W. & Letcher, R.J. Recombinant albumin and transthyretin transport proteins from two gull species and human: chlorinated and brominated contaminant binding and thyroid hormones. Environ. Sci. Technol. 44, 497-504 (2010).
49. Meerts, I.A. et al. Potent competitive interactions of some brominated fame retardants and related compounds with human transthyretin in vitro. Toxicol. Sci. 56, 95-104 (2000).
50. Dorrestein, P.C. & Kelleher, N.L. Dissecting non-ribosomal and polyketide biosynthetic machineries using electrospray ionization Fourier-Transform mass spectrometry. Nat. Prod. Rep. 23, 893-918 (2006).
51. John, E.A., Pollet, P., Gelbaum, L. & Kubanek, J. Regioselective syntheses of 2, 3, 4-tribromopyrrole and 2, 3, 5-tribromopyrrole. J. Nat. Prod. 67, 1929-1931 (2004).
52. Markowitz, V.M. et al. IMG ER: a system for microbial genome annotation expert review and curation. Bioinformatics 25, 2271-2278 (2009).
53. Kouprina, N. & Larionov, V. Selective isolation of genomic loci from complex genomes by transformation-associated recombination cloning in the yeast Saccharomyces cerevisiae. Nat. Protoc. 3, 371-377 (2008).
54. Gust, B., Challis, G.L., Fowler, K., Kieser, T. & Chater, K.F. PCR-targeted Streptomyces gene replacement identifes a protein domain needed for biosynthesis of the sesquiterpene soil odor geosmin. Proc. Natl. Acad. Sci. USA 100, 1541-1546 (2003).
55. Li, D.B. et al. Chapter 19. In vitro studies of phenol coupling enzymes involved in vancomycin biosynthesis. Methods Enzymol. 458, 487-509 (2009).