Metagenomic discovery of polybrominated diphenyl ether biosynthesis by marine sponges

Agarwal, Vinayak; Blanton, Jessica M.; Podell, Sheila; Taton, Arnaud; Schorn, Michelle A.; Busch, Julia; Lin, Zhenjian; Schmidt, Eric W.; Jensen, Paul R.; Paul, Valerie J.; Biggs, Jason S.; Golden, James W.; Allen, Eric E.; Moore, Bradley S.

doi:10.1038/NCHEMBIO.2330

Metagenomic discovery of polybrominated diphenyl ether biosynthesis by marine sponges

Journal Article · Mon Mar 20 00:00:00 EDT 2017 · Nature Chemical Biology

DOI:https://doi.org/10.1038/NCHEMBIO.2330· OSTI ID:1463262

Agarwal, Vinayak ^[1]; Blanton, Jessica M. ^[2]; ^[2]; Taton, Arnaud ^[2]; Schorn, Michelle A. ^[2]; Busch, Julia ^[2]; Lin, Zhenjian ^[3]; Schmidt, Eric W. ^[3]; Jensen, Paul R. ^[2]; Paul, Valerie J. ^[4]; ^[5]; Golden, James W. ^[2]; Allen, Eric E. ^[2]; ^[2]

Univ. of California, San Diego, CA (United States); OSTI
Univ. of California, San Diego, CA (United States)
Univ. of Utah, Salt Lake City, UT (United States)
Smithsonian Marin Station, Fort Pierce, FL (United States)
Univ. of Guam Marine Lab., Mangilao (Guam)

Naturally produced polybrominated diphenyl ethers (PBDEs) pervade the marine environment and structurally resemble toxic man-made brominated flame retardants. PBDEs bioaccumulate in marine animals and are likely transferred to the human food chain. However, the biogenic basis for PBDE production in one of their most prolific sources, marine sponges of the order Dysideidae, remains unidentified. Here, we report the discovery of PBDE biosynthetic gene clusters within sponge microbiome-associated cyanobacterial endosymbionts by employing an unbiased metagenome mining approach. By expression of PBDE biosynthetic genes in heterologous cyanobacterial hosts, we correlate the structural diversity of naturally produced PBDEs to modifications within PBDE biosynthetic gene clusters in multiple sponge holobionts. Our results establish the genetic and molecular foundation for the production of PBDEs in one of the most abundant natural sources of these molecules, further setting the stage for a metagenomic-based inventory of other PBDE sources in the marine environment.

View Accepted Manuscript (DOE)

Research Organization:: Univ. of California, San Diego, CA (United States)

Sponsoring Organization:: USDOE

Grant/Contract Number:: EE0003373

OSTI ID:: 1463262

Journal Information:: Nature Chemical Biology, Journal Name: Nature Chemical Biology Journal Issue: 5 Vol. 13; ISSN 1552-4450

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

References (59)

Approaches to Identify, Clone, and Express Symbiont Bioactive Metabolite Genes Hildebrand, Mark; Waggoner, Laura E.; Lim, Grace E. ChemInform, Vol. 35, Issue 17 https://doi.org/10.1002/chin.200417288	journal	April 2004
Sponge halogenated natural products found at parts-per-million levels in marine mammals Vetter, Walter; Stoll, Elke; Garson, Mary J. Environmental Toxicology and Chemistry, Vol. 21, Issue 10 https://doi.org/10.1002/etc.5620211002	journal	October 2002
Specialized Techniques for Site-Directed Mutagenesis in Cyanobacteria Clerico, Eugenia M.; Ditty, Jayna L.; Golden, Susan S. Methods in Molecular Biology https://doi.org/10.1007/978-1-59745-257-1_11	book	January 2007
A brominated secondary metabolite synthesized by the cyanobacterial symbiont of a marine sponge and accumulation of the crystalline metabolite in the sponge tissue Unson, M. D.; Holland, N. D.; Faulkner, D. J. Marine Biology, Vol. 119, Issue 1 https://doi.org/10.1007/BF00350100	journal	April 1994
Isolation of Oscillatoria spongeliae, the filamentous cyanobacterial symbiont of the marine sponge Dysidea herbacea Hinde, R.; Pironet, F.; Borowitzka, M. A. Marine Biology, Vol. 119, Issue 1 https://doi.org/10.1007/BF00350111	journal	April 1994
Host specificity of the symbiotic cyanobacterium Oscillatoria spongeliae in marine sponges, Dysidea spp. Thacker, R. W.; Starnes, S. Marine Biology, Vol. 142, Issue 4 https://doi.org/10.1007/s00227-002-0971-x	journal	February 2003
Identification of the cellular site of polychlorinated peptide biosynthesis in the marine sponge Dysidea (Lamellodysidea) herbacea and symbiotic cyanobacterium Oscillatoria spongeliae by CARD-FISH analysis Flatt, Patricia M.; Gautschi, Jeffrey T.; Thacker, Robert W. Marine Biology, Vol. 147, Issue 3 https://doi.org/10.1007/s00227-005-1614-9	journal	April 2005
Evolution, radiation and chemotaxonomy of Lamellodysidea, a demosponge genus with anti-plasmodial metabolites Erpenbeck, Dirk; Hooper, John N. A.; Bonnard, Isabelle Marine Biology, Vol. 159, Issue 5 https://doi.org/10.1007/s00227-012-1891-z	journal	February 2012
Effects of sponge secondary metabolites in different diets on feeding by three groups of consumers Pennings, Steven C.; Pablo, Sonia R.; Paul, Valerie J. Journal of Experimental Marine Biology and Ecology, Vol. 180, Issue 1 https://doi.org/10.1016/0022-0981(94)90083-3	journal	July 1994
Sequence and mutational analysis of the devBCA gene cluster encoding a putative ABC transporter in the cyanobacterium Anabaena variabilis ATCC 29413 Fiedler, Gabriele; Arnold, Matthias; Maldener, Iris Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 1375, Issue 1-2 https://doi.org/10.1016/S0005-2736(98)00147-3	journal	October 1998
Polybrominated diphenyl ethers from Dysidea herbacea, Dysidea chlorea and Phyllospongia foliascens Carté, Brad; Faulkner, D. John Tetrahedron, Vol. 37, Issue 13 https://doi.org/10.1016/S0040-4020(01)88886-4	journal	January 1981
Studies on the antimicrobial substances of sponges. VI. Structures of two antibacterial substances isolated from the marine sponge Dysidea herbacea. Sharma, G. M.; Vig, B. Tetrahedron Letters, Vol. 13, Issue 17 https://doi.org/10.1016/S0040-4039(01)84729-8	journal	January 1972
Chapter 23 Cyanobactin Ribosomally Synthesized Peptides—A Case of Deep Metagenome Mining Schmidt, Eric W.; Donia, Mohamed S. Complex Enzymes in Microbial Natural Product Biosynthesis, Part A: Overview Articles and Peptides https://doi.org/10.1016/S0076-6879(09)04823-X	book	January 2009
Speciation and Biosynthetic Variation in Four Dictyoceratid Sponges and Their Cyanobacterial Symbiont, Oscillatoria spongeliae Ridley, Christian P.; Bergquist, Patricia R.; Harper, Mary Kay Chemistry & Biology, Vol. 12, Issue 3 https://doi.org/10.1016/j.chembiol.2005.02.003	journal	March 2005
Hydroxylated and methoxylated polybrominated diphenyl ethers and polybrominated dibenzo-p-dioxins in red alga and cyanobacteria living in the Baltic Sea Malmvärn, Anna; Zebühr, Yngve; Kautsky, Lena Chemosphere, Vol. 72, Issue 6 https://doi.org/10.1016/j.chemosphere.2008.03.036	journal	June 2008
Hydroxylated and methoxylated polybrominated diphenyl ethers in blood plasma of humans in Hong Kong Wang, Hong-Sheng; Chen, Zhuo-Jia; Ho, Ka-Lok Environment International, Vol. 47 https://doi.org/10.1016/j.envint.2012.06.004	journal	October 2012
Polybrominated diphenyl ethers and their hydroxylated/methoxylated analogs: Environmental sources, metabolic relationships, and relative toxicities Wiseman, Steve B.; Wan, Yi; Chang, Hong Marine Pollution Bulletin, Vol. 63, Issue 5-12 https://doi.org/10.1016/j.marpolbul.2011.02.008	journal	January 2011
Bromination of phenols in bromoperoxidase-catalyzed oxidations Wischang, Diana; Hartung, Jens Tetrahedron, Vol. 68, Issue 46 https://doi.org/10.1016/j.tet.2012.08.081	journal	November 2012
Ichthyotoxic brominated diphenyl ethers from a mixed assemblage of a red alga and cyanobacterium: Structure clarification and biological properties Suyama, Takashi L.; Cao, Zhengyu; Murray, Thomas F. Toxicon, Vol. 55, Issue 2-3 https://doi.org/10.1016/j.toxicon.2009.07.020	journal	February 2010
Enzymatic Synthesis of Polybrominated Dioxins from the Marine Environment Agarwal, Vinayak; Moore, Bradley S. ACS Chemical Biology, Vol. 9, Issue 9 https://doi.org/10.1021/cb5004338	journal	July 2014
Identification, Quantification, and Synthesis of a Novel Dimethoxylated Polybrominated Biphenyl in Marine Mammals Caught Off the Coast of Japan Marsh, GÖran; Athanasiadou, Maria; Athanassiadis, Ioannis Environmental Science & Technology, Vol. 39, Issue 22 https://doi.org/10.1021/es051153v	journal	November 2005
Hydroxylated Polybrominated Diphenyl Ethers and Bisphenol A in Pregnant Women and Their Matching Fetuses: Placental Transfer and Potential Risks Wan, Yi; Choi, Kyungho; Kim, Sunmi Environmental Science & Technology, Vol. 44, Issue 13 https://doi.org/10.1021/es1002764	journal	July 2010
Dioxins: An Overview and History ^† Hites, Ronald A. Environmental Science & Technology, Vol. 45, Issue 1 https://doi.org/10.1021/es1013664	journal	January 2011
Hydroxylated Polybrominated Diphenyl Ethers in Paired Maternal and Cord Sera Chen, Aimin; Park, June-Soo; Linderholm, Linda Environmental Science & Technology, Vol. 47, Issue 8 https://doi.org/10.1021/es3046839	journal	April 2013
Nontargeted Biomonitoring of Halogenated Organic Compounds in Two Ecotypes of Bottlenose Dolphins ( Tursiops truncatus ) from the Southern California Bight Shaul, Nellie J.; Dodder, Nathan G.; Aluwihare, Lihini I. Environmental Science & Technology, Vol. 49, Issue 3 https://doi.org/10.1021/es505156q	journal	January 2015
Complexity of Naturally Produced Polybrominated Diphenyl Ethers Revealed via Mass Spectrometry Agarwal, Vinayak; Li, Jie; Rahman, Imran Environmental Science & Technology, Vol. 49, Issue 3 https://doi.org/10.1021/es505440j	journal	January 2015
Enzymatic Reductive Dehalogenation Controls the Biosynthesis of Marine Bacterial Pyrroles El Gamal, Abrahim; Agarwal, Vinayak; Rahman, Imran Journal of the American Chemical Society, Vol. 138, Issue 40 https://doi.org/10.1021/jacs.6b08512	journal	September 2016
New polychlorinated amino acid derivatives from the marine sponge Dysidea herbacea Unson, Mia D.; Rose, Charles B.; Faulkner, D. John The Journal of Organic Chemistry, Vol. 58, Issue 23 https://doi.org/10.1021/jo00075a029	journal	November 1993
Spongiadioxins A and B, Two New Polybrominated Dibenzo- p -dioxins from an Australian Marine Sponge Dysidea dendyi Utkina, Natalia K.; Denisenko, Vladimir A.; Scholokova, Olga V. Journal of Natural Products, Vol. 64, Issue 2 https://doi.org/10.1021/np0003544	journal	February 2001
Localization Studies of Bioactive Cyclic Peptides in the Ascidian Lissoclinum p atella Salomon, Christine E.; Faulkner, D. John Journal of Natural Products, Vol. 65, Issue 5 https://doi.org/10.1021/np010556f	journal	May 2002
Two New Minor Polybrominated Dibenzo- p -dioxins from the Marine Sponge Dysidea dendyi Utkina, Natalia K.; Denisenko, Vladimir A.; Virovaya, Marina V. Journal of Natural Products, Vol. 65, Issue 8 https://doi.org/10.1021/np0106438	journal	August 2002
NMR Strategy for Unraveling Structures of Bioactive Sponge-Derived Oxy-polyhalogenated Diphenyl Ethers ^⊥ Calcul, Laurent; Chow, Raymond; Oliver, Allen G. Journal of Natural Products, Vol. 72, Issue 3 https://doi.org/10.1021/np800737z	journal	March 2009
Biosynthesis of polybrominated aromatic organic compounds by marine bacteria Agarwal, Vinayak; El Gamal, Abrahim A.; Yamanaka, Kazuya Nature Chemical Biology, Vol. 10, Issue 8 https://doi.org/10.1038/nchembio.1564	journal	June 2014
Polyketide assembly lines of uncultivated sponge symbionts from structure-based gene targeting Fisch, Katja M.; Gurgui, Cristian; Heycke, Nina Nature Chemical Biology, Vol. 5, Issue 7 https://doi.org/10.1038/nchembio.176	journal	May 2009
Computational approaches to natural product discovery Medema, Marnix H.; Fischbach, Michael A. Nature Chemical Biology, Vol. 11, Issue 9 https://doi.org/10.1038/nchembio.1884	journal	August 2015
Fast gapped-read alignment with Bowtie 2 Langmead, Ben; Salzberg, Steven L. Nature Methods, Vol. 9, Issue 4 https://doi.org/10.1038/nmeth.1923	journal	March 2012
Differential abundance analysis for microbial marker-gene surveys Paulson, Joseph N.; Stine, O. Colin; Bravo, Héctor Corrada Nature Methods, Vol. 10, Issue 12 https://doi.org/10.1038/nmeth.2658	journal	September 2013
Genomic insights into the marine sponge microbiome Hentschel, Ute; Piel, Jörn; Degnan, Sandie M. Nature Reviews Microbiology, Vol. 10, Issue 9 https://doi.org/10.1038/nrmicro2839	journal	July 2012
Analysis of immune, microbiota and metabolome maturation in infants in a clinical trial of Lactobacillus paracasei CBA L74-fermented formula Roggero, Paola; Liotto, Nadia; Pozzi, Chiara Nature Communications, Vol. 11, Issue 1 https://doi.org/10.1038/s41467-020-16582-1	journal	June 2020
Defensive symbioses of animals with prokaryotic and eukaryotic microorganisms Flórez, Laura V.; Biedermann, Peter H. W.; Engl, Tobias Natural Product Reports, Vol. 32, Issue 7 https://doi.org/10.1039/C5NP00010F	journal	January 2015
Approaches to identify, clone, and express symbiont bioactive metabolite genes Hildebrand, Mark; Waggoner, Laura E.; Lim, Grace E. Natural Product Reports, Vol. 21, Issue 1 https://doi.org/10.1039/b302336m	journal	January 2004
Vanadate-dependent bromoperoxidases from Ascophyllum nodosum in the synthesis of brominated phenols and pyrroles Wischang, Diana; Radlow, Madlen; Hartung, Jens Dalton Transactions, Vol. 42, Issue 33 https://doi.org/10.1039/c3dt51582f	journal	January 2013
Patellamide A and C biosynthesis by a microcin-like pathway in Prochloron didemni, the cyanobacterial symbiont of Lissoclinum patella Schmidt, E. W.; Nelson, J. T.; Rasko, D. A. Proceedings of the National Academy of Sciences, Vol. 102, Issue 20 https://doi.org/10.1073/pnas.0501424102	journal	May 2005
Biosynthetic origin of natural products isolated from marine microorganism-invertebrate assemblages Simmons, T. L.; Coates, R. C.; Clark, B. R. Proceedings of the National Academy of Sciences, Vol. 105, Issue 12 https://doi.org/10.1073/pnas.0709851105	journal	February 2008
Genome streamlining and chemical defense in a coral reef symbiosis Kwan, J. C.; Donia, M. S.; Han, A. W. Proceedings of the National Academy of Sciences, Vol. 109, Issue 50 https://doi.org/10.1073/pnas.1213820109	journal	November 2012
Biosynthesis of coral settlement cue tetrabromopyrrole in marine bacteria by a uniquely adapted brominase–thioesterase enzyme pair El Gamal, Abrahim; Agarwal, Vinayak; Diethelm, Stefan Proceedings of the National Academy of Sciences, Vol. 113, Issue 14 https://doi.org/10.1073/pnas.1519695113	journal	March 2016
The Sequence Alignment/Map format and SAMtools Li, H.; Handsaker, B.; Wysoker, A. Bioinformatics, Vol. 25, Issue 16 https://doi.org/10.1093/bioinformatics/btp352	journal	June 2009
PyNAST: a flexible tool for aligning sequences to a template alignment Caporaso, J. G.; Bittinger, K.; Bushman, F. D. Bioinformatics, Vol. 26, Issue 2 https://doi.org/10.1093/bioinformatics/btp636	journal	November 2009
Phylogeny and Systematics of Demospongiae in Light of New Small-Subunit Ribosomal DNA (18S) Sequences Redmond, N. E.; Morrow, C. C.; Thacker, R. W. Integrative and Comparative Biology, Vol. 53, Issue 3 https://doi.org/10.1093/icb/ict078	journal	June 2013
The SILVA ribosomal RNA gene database project: improved data processing and web-based tools Quast, Christian; Pruesse, Elmar; Yilmaz, Pelin Nucleic Acids Research, Vol. 41, Issue D1 https://doi.org/10.1093/nar/gks1219	journal	November 2012
Broad-host-range vector system for synthetic biology and biotechnology in cyanobacteria Taton, Arnaud; Unglaub, Federico; Wright, Nicole E. Nucleic Acids Research, Vol. 42, Issue 17 https://doi.org/10.1093/nar/gku673	journal	July 2014
Every base matters: assessing small subunit rRNA primers for marine microbiomes with mock communities, time series and global field samples: Primers for marine microbiome studies Parada, Alma E.; Needham, David M.; Fuhrman, Jed A. Environmental Microbiology, Vol. 18, Issue 5 https://doi.org/10.1111/1462-2920.13023	journal	October 2015
Two Abundant Bioaccumulated Halogenated Compounds Are Natural Products Teuten, E. L. Science, Vol. 307, Issue 5711 https://doi.org/10.1126/science.1106882	journal	February 2005
Regulation of Gene Expression in Diverse Cyanobacterial Species by Using Theophylline-Responsive Riboswitches Ma, Amy T.; Schmidt, Calvin M.; Golden, James W. Applied and Environmental Microbiology, Vol. 80, Issue 21 https://doi.org/10.1128/AEM.01697-14	journal	August 2014
PCR primers to amplify 16S rRNA genes from cyanobacteria. Nübel, U.; Garcia-Pichel, F.; Muyzer, G. Applied and environmental microbiology, Vol. 63, Issue 8 https://doi.org/10.1128/AEM.63.8.3327-3332.1997	journal	January 1997
Molecular Evidence for a Uniform Microbial Community in Sponges from Different Oceans Hentschel, U.; Hopke, J.; Horn, M. Applied and Environmental Microbiology, Vol. 68, Issue 9 https://doi.org/10.1128/AEM.68.9.4431-4440.2002	journal	September 2002
Investigation of Oscillatoria spongeliae-Dominated Bacterial Communities in Four Dictyoceratid Sponges Ridley, C. P.; John Faulkner, D.; Haygood, M. G. Applied and Environmental Microbiology, Vol. 71, Issue 11 https://doi.org/10.1128/AEM.71.11.7366-7375.2005	journal	November 2005
Assembly-Driven Community Genomics of a Hypersaline Microbial Ecosystem Podell, Sheila; Ugalde, Juan A.; Narasingarao, Priya PLoS ONE, Vol. 8, Issue 4 https://doi.org/10.1371/journal.pone.0061692	journal	April 2013
Effects of depth and light on secondary metabolites and cyanobacterial symbionts of the sponge Dysidea granulosa Becerro, Ma; Paul, Vj Marine Ecology Progress Series, Vol. 280 https://doi.org/10.3354/meps280115	journal	January 2004

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