A multiproducer microbiome generates chemical diversity in the marine sponge Mycale hentscheli

Michael Rust, Eric J.N. Helfrich, Michael F. Freeman, Pakjira Nanudorn, Christopher M. Field, Christian Rückert, Tomas Kündig, Michael J. Page, Victoria L. Webb, Jörn Kalinowski, Shinichi Sunagawa, Jörn Piel

Research output: Contribution to journalArticle

1 Scopus citations

Abstract

Bacterial specialized metabolites are increasingly recognized as important factors in animal–microbiome interactions: for example, by providing the host with chemical defenses. Even in chemically rich animals, such compounds have been found to originate from individual members of more diverse microbiomes. Here, we identified a remarkable case of a moderately complex microbiome in the sponge host Mycale hentscheli in which multiple symbionts jointly generate chemical diversity. In addition to bacterial pathways for three distinct polyketide families comprising microtubule-inhibiting peloruside drug candidates, mycalamide-type contact poisons, and the eukaryotic translation-inhibiting pateamines, we identified extensive biosynthetic potential distributed among a broad phylogenetic range of bacteria. Biochemical data on one of the orphan pathways suggest a previously unknown member of the rare polytheonamide-type cytotoxin family as its product. Other than supporting a scenario of cooperative symbiosis based on bacterial metabolites, the data provide a rationale for the chemical variability of M. hentscheli and could pave the way toward biotechnological peloruside production. Most bacterial lineages in the compositionally unusual sponge microbiome were not known to synthesize bioactive metabolites, supporting the concept that microbial dark matter harbors diverse producer taxa with as yet unrecognized drug discovery potential.

Original languageEnglish (US)
Pages (from-to)9508-9518
Number of pages11
JournalProceedings of the National Academy of Sciences of the United States of America
Volume117
Issue number17
DOIs
StatePublished - Apr 28 2020

Keywords

  • Biosynthesis
  • Symbiosis
  • sponges
  • | microbiomes
  • | natural products

PubMed: MeSH publication types

  • Journal Article
  • Research Support, Non-U.S. Gov't

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  • Cite this

    Rust, M., Helfrich, E. J. N., Freeman, M. F., Nanudorn, P., Field, C. M., Rückert, C., Kündig, T., Page, M. J., Webb, V. L., Kalinowski, J., Sunagawa, S., & Piel, J. (2020). A multiproducer microbiome generates chemical diversity in the marine sponge Mycale hentscheli. Proceedings of the National Academy of Sciences of the United States of America, 117(17), 9508-9518. https://doi.org/10.1073/pnas.1919245117