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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

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Abstract

Populations of the sponge Dysidea (Lamellodysidea) herbacea, which host the cyanobacterium Oscillatoria spongeliae, vary in their production of polychlorinated peptides. Peptide natural products previously isolated from D. herbacea are often halogenated and include dysidin, dysidinin, and a series of chlorinated diketopiperazines. Strikingly, the distinctive leucine-derived trichloromethyl signature of these compounds is shared only with metabolites of the marine cyanobacterium Lyngbya majuscula, and includes such compounds as barbamide and nordysidinin. Genetic information available for the barbamide biosynthetic gene cluster was used to successfully polymerase chain reaction (PCR) amplify a barB1 homolog (dysB1) from D. herbacea samples collected in Papua New Guinea. Catalyzed reporter deposition fluorescence in situ hybridization (CARD-FISH) analysis showed that dysB1 oligonucleotide probes hybridized to sequences in the filamentous cyanobacterial symbiont O. spongeliae. Consistent with this finding, a D. herbacea/O. spongeliae collection devoid of the polychlorinated peptides did not contain the barB1 homologs.

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Acknowledgements

We thank Patrick Erwin from the Department of Biology at the University of Alabama at Birmingham (UAB) for providing laboratory assistance and Kathy Cook from the Department of Botany and Plant Pathology at Oregon State University for the preparation of the mounted sections of Dysidea herbacea. We would also like to thank the Center of Gene Research and Biotechnology at Oregon State University and the Center for AIDS Research at UAB for DNA sequencing. Special thanks are extended to Karen Tenney for expert collection of D. herbacea samples. This research was supported by the National Institutes of Health (NIH) under grant nos. GM20657 (W.H.G. and P.F.), CA83155 (W.H.G. and P.C.), CA45295 (P.C.) and supplement equipment (ESI-TOF-LCMS) grant to NIH CA52955 (P.C.), and the National Science Foundation under grant no. 0209329 (R.W.T.). We would like to acknowledge and deeply thank the governments of Papua New Guinea, Curacao, and Panama for sponsoring the collection and use of materials for this study.

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  1. College of Pharmacy, Oregon State University, Corvallis, OR, 97331, USA

    Patricia M. Flatt, Mirjam Musafija-Girt & William H. Gerwick

  2. Department of Chemistry and Biochemistry and Institute of Marine Sciences, University of California, Santa Cruz, CA , 95064, USA

    Jeffrey T. Gautschi & Phillip Crews

  3. Department of Biology, University of Alabama at Birmingham, Birmingham, AL , 35294, USA

    Robert W. Thacker

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  1. Patricia M. Flatt
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Communicated by P.W. Sammarco, Chauvin

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Flatt, P.M., Gautschi, J.T., Thacker, R.W. et al. 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. Marine Biology 147, 761–774 (2005). https://doi.org/10.1007/s00227-005-1614-9

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