Comparative Genomics of Cyanobacterial Symbionts Reveals Distinct, Specialized Metabolism in Tropical <italic toggle="yes">Dysideidae</italic> Sponges

ABSTRACT Marine sponges are recognized as valuable sources of bioactive metabolites and renowned as petri dishes of the sea, providing specialized niches for many symbiotic microorganisms. Sponges of the family Dysideidae are well documented to be chemically talented, often containing high levels of...

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Autores principales:	Michelle A. Schorn, Peter A. Jordan, Sheila Podell, Jessica M. Blanton, Vinayak Agarwal, Jason S. Biggs, Eric E. Allen, Bradley S. Moore
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2019
Materias:	biosynthesis cyanobacteria halogenated compounds marine microbiology metagenomics natural products Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/53894f45b705493bbfe838c6d6acb2f3
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spelling	oai:doaj.org-article:53894f45b705493bbfe838c6d6acb2f32021-11-15T15:55:24ZComparative Genomics of Cyanobacterial Symbionts Reveals Distinct, Specialized Metabolism in Tropical <italic toggle="yes">Dysideidae</italic> Sponges10.1128/mBio.00821-192150-7511https://doaj.org/article/53894f45b705493bbfe838c6d6acb2f32019-06-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00821-19https://doaj.org/toc/2150-7511ABSTRACT Marine sponges are recognized as valuable sources of bioactive metabolites and renowned as petri dishes of the sea, providing specialized niches for many symbiotic microorganisms. Sponges of the family Dysideidae are well documented to be chemically talented, often containing high levels of polyhalogenated compounds, terpenoids, peptides, and other classes of bioactive small molecules. This group of tropical sponges hosts a high abundance of an uncultured filamentous cyanobacterium, Hormoscilla spongeliae. Here, we report the comparative genomic analyses of two phylogenetically distinct Hormoscilla populations, which reveal shared deficiencies in essential pathways, hinting at possible reasons for their uncultivable status, as well as differing biosynthetic machinery for the production of specialized metabolites. One symbiont population contains clustered genes for expanded polybrominated diphenylether (PBDE) biosynthesis, while the other instead harbors a unique gene cluster for the biosynthesis of the dysinosin nonribosomal peptides. The hybrid sequencing and assembly approach utilized here allows, for the first time, a comprehensive look into the genomes of these elusive sponge symbionts. IMPORTANCE Natural products provide the inspiration for most clinical drugs. With the rise in antibiotic resistance, it is imperative to discover new sources of chemical diversity. Bacteria living in symbiosis with marine invertebrates have emerged as an untapped source of natural chemistry. While symbiotic bacteria are often recalcitrant to growth in the lab, advances in metagenomic sequencing and assembly now make it possible to access their genetic blueprint. A cell enrichment procedure, combined with a hybrid sequencing and assembly approach, enabled detailed genomic analysis of uncultivated cyanobacterial symbiont populations in two chemically rich tropical marine sponges. These population genomes reveal a wealth of secondary metabolism potential as well as possible reasons for historical difficulties in their cultivation.Michelle A. SchornPeter A. JordanSheila PodellJessica M. BlantonVinayak AgarwalJason S. BiggsEric E. AllenBradley S. MooreAmerican Society for Microbiologyarticlebiosynthesiscyanobacteriahalogenated compoundsmarine microbiologymetagenomicsnatural productsMicrobiologyQR1-502ENmBio, Vol 10, Iss 3 (2019)
institution	DOAJ
collection	DOAJ
language	EN
topic	biosynthesis cyanobacteria halogenated compounds marine microbiology metagenomics natural products Microbiology QR1-502
spellingShingle	biosynthesis cyanobacteria halogenated compounds marine microbiology metagenomics natural products Microbiology QR1-502 Michelle A. Schorn Peter A. Jordan Sheila Podell Jessica M. Blanton Vinayak Agarwal Jason S. Biggs Eric E. Allen Bradley S. Moore Comparative Genomics of Cyanobacterial Symbionts Reveals Distinct, Specialized Metabolism in Tropical <italic toggle="yes">Dysideidae</italic> Sponges
description	ABSTRACT Marine sponges are recognized as valuable sources of bioactive metabolites and renowned as petri dishes of the sea, providing specialized niches for many symbiotic microorganisms. Sponges of the family Dysideidae are well documented to be chemically talented, often containing high levels of polyhalogenated compounds, terpenoids, peptides, and other classes of bioactive small molecules. This group of tropical sponges hosts a high abundance of an uncultured filamentous cyanobacterium, Hormoscilla spongeliae. Here, we report the comparative genomic analyses of two phylogenetically distinct Hormoscilla populations, which reveal shared deficiencies in essential pathways, hinting at possible reasons for their uncultivable status, as well as differing biosynthetic machinery for the production of specialized metabolites. One symbiont population contains clustered genes for expanded polybrominated diphenylether (PBDE) biosynthesis, while the other instead harbors a unique gene cluster for the biosynthesis of the dysinosin nonribosomal peptides. The hybrid sequencing and assembly approach utilized here allows, for the first time, a comprehensive look into the genomes of these elusive sponge symbionts. IMPORTANCE Natural products provide the inspiration for most clinical drugs. With the rise in antibiotic resistance, it is imperative to discover new sources of chemical diversity. Bacteria living in symbiosis with marine invertebrates have emerged as an untapped source of natural chemistry. While symbiotic bacteria are often recalcitrant to growth in the lab, advances in metagenomic sequencing and assembly now make it possible to access their genetic blueprint. A cell enrichment procedure, combined with a hybrid sequencing and assembly approach, enabled detailed genomic analysis of uncultivated cyanobacterial symbiont populations in two chemically rich tropical marine sponges. These population genomes reveal a wealth of secondary metabolism potential as well as possible reasons for historical difficulties in their cultivation.
format	article
author	Michelle A. Schorn Peter A. Jordan Sheila Podell Jessica M. Blanton Vinayak Agarwal Jason S. Biggs Eric E. Allen Bradley S. Moore
author_facet	Michelle A. Schorn Peter A. Jordan Sheila Podell Jessica M. Blanton Vinayak Agarwal Jason S. Biggs Eric E. Allen Bradley S. Moore
author_sort	Michelle A. Schorn
title	Comparative Genomics of Cyanobacterial Symbionts Reveals Distinct, Specialized Metabolism in Tropical <italic toggle="yes">Dysideidae</italic> Sponges
title_short	Comparative Genomics of Cyanobacterial Symbionts Reveals Distinct, Specialized Metabolism in Tropical <italic toggle="yes">Dysideidae</italic> Sponges
title_full	Comparative Genomics of Cyanobacterial Symbionts Reveals Distinct, Specialized Metabolism in Tropical <italic toggle="yes">Dysideidae</italic> Sponges
title_fullStr	Comparative Genomics of Cyanobacterial Symbionts Reveals Distinct, Specialized Metabolism in Tropical <italic toggle="yes">Dysideidae</italic> Sponges
title_full_unstemmed	Comparative Genomics of Cyanobacterial Symbionts Reveals Distinct, Specialized Metabolism in Tropical <italic toggle="yes">Dysideidae</italic> Sponges
title_sort	comparative genomics of cyanobacterial symbionts reveals distinct, specialized metabolism in tropical <italic toggle="yes">dysideidae</italic> sponges
publisher	American Society for Microbiology
publishDate	2019
url	https://doaj.org/article/53894f45b705493bbfe838c6d6acb2f3
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Comparative Genomics of Cyanobacterial Symbionts Reveals Distinct, Specialized Metabolism in Tropical <italic toggle="yes">Dysideidae</italic> Sponges

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