Metagenomic Exploration of the Marine Sponge <italic toggle="yes">Mycale hentscheli</italic> Uncovers Multiple Polyketide-Producing Bacterial Symbionts

ABSTRACT Marine sponges have been a prolific source of unique bioactive compounds that are presumed to act as a deterrent to predation. Many of these compounds have potential therapeutic applications; however, the lack of efficient and sustainable synthetic routes frequently limits clinical developm...

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Autores principales:	Mathew A. Storey, Sarah K. Andreassend, Joe Bracegirdle, Alistair Brown, Robert A. Keyzers, David F. Ackerley, Peter T. Northcote, Jeremy G. Owen
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2020
Materias:	biosynthesis metagenomics polyketides secondary metabolism symbiosis Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/94c3f8add06a48ba9ee2fb71c7a960c2
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spelling	oai:doaj.org-article:94c3f8add06a48ba9ee2fb71c7a960c22021-11-15T15:57:02ZMetagenomic Exploration of the Marine Sponge <italic toggle="yes">Mycale hentscheli</italic> Uncovers Multiple Polyketide-Producing Bacterial Symbionts10.1128/mBio.02997-192150-7511https://doaj.org/article/94c3f8add06a48ba9ee2fb71c7a960c22020-04-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.02997-19https://doaj.org/toc/2150-7511ABSTRACT Marine sponges have been a prolific source of unique bioactive compounds that are presumed to act as a deterrent to predation. Many of these compounds have potential therapeutic applications; however, the lack of efficient and sustainable synthetic routes frequently limits clinical development. Here, we describe a metagenomic investigation of Mycale hentscheli, a chemically gifted marine sponge that possesses multiple distinct chemotypes. We applied shotgun metagenomic sequencing, hybrid assembly of short- and long-read data, and metagenomic binning to obtain a comprehensive picture of the microbiome of five specimens, spanning three chemotypes. Our data revealed multiple producing species, each having relatively modest secondary metabolomes, that contribute collectively to the chemical arsenal of the holobiont. We assembled complete genomes for multiple new genera, including two species that produce the cytotoxic polyketides pateamine and mycalamide, as well as a third high-abundance symbiont harboring a proteusin-type biosynthetic pathway that appears to encode a new polytheonamide-like compound. We also identified an additional 188 biosynthetic gene clusters, including a pathway for biosynthesis of peloruside. These results suggest that multiple species cooperatively contribute to defensive symbiosis in M. hentscheli and reveal that the taxonomic diversity of secondary-metabolite-producing sponge symbionts is larger and richer than previously recognized. IMPORTANCE Mycale hentscheli is a marine sponge that is rich in bioactive small molecules. Here, we use direct metagenomic sequencing to elucidate highly complete and contiguous genomes for the major symbiotic bacteria of this sponge. We identify complete biosynthetic pathways for the three potent cytotoxic polyketides which have previously been isolated from M. hentscheli. Remarkably, and in contrast to previous studies of marine sponges, we attribute each of these metabolites to a different producing microbe. We also find that the microbiome of M. hentscheli is stably maintained among individuals, even over long periods of time. Collectively, our data suggest a cooperative mode of defensive symbiosis in which multiple symbiotic bacterial species cooperatively contribute to the defensive chemical arsenal of the holobiont.Mathew A. StoreySarah K. AndreassendJoe BracegirdleAlistair BrownRobert A. KeyzersDavid F. AckerleyPeter T. NorthcoteJeremy G. OwenAmerican Society for Microbiologyarticlebiosynthesismetagenomicspolyketidessecondary metabolismsymbiosisMicrobiologyQR1-502ENmBio, Vol 11, Iss 2 (2020)
institution	DOAJ
collection	DOAJ
language	EN
topic	biosynthesis metagenomics polyketides secondary metabolism symbiosis Microbiology QR1-502
spellingShingle	biosynthesis metagenomics polyketides secondary metabolism symbiosis Microbiology QR1-502 Mathew A. Storey Sarah K. Andreassend Joe Bracegirdle Alistair Brown Robert A. Keyzers David F. Ackerley Peter T. Northcote Jeremy G. Owen Metagenomic Exploration of the Marine Sponge <italic toggle="yes">Mycale hentscheli</italic> Uncovers Multiple Polyketide-Producing Bacterial Symbionts
description	ABSTRACT Marine sponges have been a prolific source of unique bioactive compounds that are presumed to act as a deterrent to predation. Many of these compounds have potential therapeutic applications; however, the lack of efficient and sustainable synthetic routes frequently limits clinical development. Here, we describe a metagenomic investigation of Mycale hentscheli, a chemically gifted marine sponge that possesses multiple distinct chemotypes. We applied shotgun metagenomic sequencing, hybrid assembly of short- and long-read data, and metagenomic binning to obtain a comprehensive picture of the microbiome of five specimens, spanning three chemotypes. Our data revealed multiple producing species, each having relatively modest secondary metabolomes, that contribute collectively to the chemical arsenal of the holobiont. We assembled complete genomes for multiple new genera, including two species that produce the cytotoxic polyketides pateamine and mycalamide, as well as a third high-abundance symbiont harboring a proteusin-type biosynthetic pathway that appears to encode a new polytheonamide-like compound. We also identified an additional 188 biosynthetic gene clusters, including a pathway for biosynthesis of peloruside. These results suggest that multiple species cooperatively contribute to defensive symbiosis in M. hentscheli and reveal that the taxonomic diversity of secondary-metabolite-producing sponge symbionts is larger and richer than previously recognized. IMPORTANCE Mycale hentscheli is a marine sponge that is rich in bioactive small molecules. Here, we use direct metagenomic sequencing to elucidate highly complete and contiguous genomes for the major symbiotic bacteria of this sponge. We identify complete biosynthetic pathways for the three potent cytotoxic polyketides which have previously been isolated from M. hentscheli. Remarkably, and in contrast to previous studies of marine sponges, we attribute each of these metabolites to a different producing microbe. We also find that the microbiome of M. hentscheli is stably maintained among individuals, even over long periods of time. Collectively, our data suggest a cooperative mode of defensive symbiosis in which multiple symbiotic bacterial species cooperatively contribute to the defensive chemical arsenal of the holobiont.
format	article
author	Mathew A. Storey Sarah K. Andreassend Joe Bracegirdle Alistair Brown Robert A. Keyzers David F. Ackerley Peter T. Northcote Jeremy G. Owen
author_facet	Mathew A. Storey Sarah K. Andreassend Joe Bracegirdle Alistair Brown Robert A. Keyzers David F. Ackerley Peter T. Northcote Jeremy G. Owen
author_sort	Mathew A. Storey
title	Metagenomic Exploration of the Marine Sponge <italic toggle="yes">Mycale hentscheli</italic> Uncovers Multiple Polyketide-Producing Bacterial Symbionts
title_short	Metagenomic Exploration of the Marine Sponge <italic toggle="yes">Mycale hentscheli</italic> Uncovers Multiple Polyketide-Producing Bacterial Symbionts
title_full	Metagenomic Exploration of the Marine Sponge <italic toggle="yes">Mycale hentscheli</italic> Uncovers Multiple Polyketide-Producing Bacterial Symbionts
title_fullStr	Metagenomic Exploration of the Marine Sponge <italic toggle="yes">Mycale hentscheli</italic> Uncovers Multiple Polyketide-Producing Bacterial Symbionts
title_full_unstemmed	Metagenomic Exploration of the Marine Sponge <italic toggle="yes">Mycale hentscheli</italic> Uncovers Multiple Polyketide-Producing Bacterial Symbionts
title_sort	metagenomic exploration of the marine sponge <italic toggle="yes">mycale hentscheli</italic> uncovers multiple polyketide-producing bacterial symbionts
publisher	American Society for Microbiology
publishDate	2020
url	https://doaj.org/article/94c3f8add06a48ba9ee2fb71c7a960c2
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Metagenomic Exploration of the Marine Sponge <italic toggle="yes">Mycale hentscheli</italic> Uncovers Multiple Polyketide-Producing Bacterial Symbionts

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