Microbial Strategies for Survival in the Glass Sponge <italic toggle="yes">Vazella pourtalesii</italic>

ABSTRACT Few studies have explored the microbiomes of glass sponges (Hexactinellida). The present study seeks to elucidate the composition of the microbiota associated with the glass sponge Vazella pourtalesii and the functional strategies of the main symbionts. We combined microscopic approaches wi...

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Autores principales:	Kristina Bayer, Kathrin Busch, Ellen Kenchington, Lindsay Beazley, Sören Franzenburg, Jan Michels, Ute Hentschel, Beate M. Slaby
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2020
Materias:	glass sponge Porifera Hexactinellida symbiosis microbiome microbial metabolism Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/fc2edceb76f24f7087b8c9ffdee1514c
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spelling	oai:doaj.org-article:fc2edceb76f24f7087b8c9ffdee1514c2021-12-02T18:23:16ZMicrobial Strategies for Survival in the Glass Sponge <italic toggle="yes">Vazella pourtalesii</italic>10.1128/mSystems.00473-202379-5077https://doaj.org/article/fc2edceb76f24f7087b8c9ffdee1514c2020-08-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00473-20https://doaj.org/toc/2379-5077ABSTRACT Few studies have explored the microbiomes of glass sponges (Hexactinellida). The present study seeks to elucidate the composition of the microbiota associated with the glass sponge Vazella pourtalesii and the functional strategies of the main symbionts. We combined microscopic approaches with metagenome-guided microbial genome reconstruction and amplicon community profiling toward this goal. Microscopic imaging revealed that the host and microbial cells appeared within dense biomass patches that are presumably syncytial tissue aggregates. Based on abundances in amplicon libraries and metagenomic data, SAR324 bacteria, Crenarchaeota, Patescibacteria, and Nanoarchaeota were identified as abundant members of the V. pourtalesii microbiome; thus, their genomic potentials were analyzed in detail. A general pattern emerged in that the V. pourtalesii symbionts had very small genome sizes, in the range of 0.5 to 2.2 Mb, and low GC contents, even below those of seawater relatives. Based on functional analyses of metagenome-assembled genomes (MAGs), we propose two major microbial strategies: the “givers,” namely, Crenarchaeota and SAR324, heterotrophs and facultative anaerobes, produce and partly secrete all required amino acids and vitamins. The “takers,” Nanoarchaeota and Patescibacteria, are anaerobes with reduced genomes that tap into the microbial community for resources, e.g., lipids and DNA, likely using pilus-like structures. We posit that the existence of microbial cells in sponge syncytia together with the low-oxygen conditions in the seawater environment are factors that shape the unique compositional and functional properties of the microbial community associated with V. pourtalesii. IMPORTANCE We investigated the microbial community of V. pourtalesii that forms globally unique, monospecific sponge grounds under low-oxygen conditions on the Scotian Shelf, where it plays a key role in its vulnerable ecosystem. The microbial community was found to be concentrated within biomass patches and is dominated by small cells (<1 μm). MAG analyses showed consistently small genome sizes and low GC contents, which is unusual compared to known sponge symbionts. These properties, as well as the (facultatively) anaerobic metabolism and a high degree of interdependence between the dominant symbionts regarding amino acid and vitamin synthesis, are likely adaptations to the unique conditions within the syncytial tissue of their hexactinellid host and the low-oxygen environment.Kristina BayerKathrin BuschEllen KenchingtonLindsay BeazleySören FranzenburgJan MichelsUte HentschelBeate M. SlabyAmerican Society for Microbiologyarticleglass spongePoriferaHexactinellidasymbiosismicrobiomemicrobial metabolismMicrobiologyQR1-502ENmSystems, Vol 5, Iss 4 (2020)
institution	DOAJ
collection	DOAJ
language	EN
topic	glass sponge Porifera Hexactinellida symbiosis microbiome microbial metabolism Microbiology QR1-502
spellingShingle	glass sponge Porifera Hexactinellida symbiosis microbiome microbial metabolism Microbiology QR1-502 Kristina Bayer Kathrin Busch Ellen Kenchington Lindsay Beazley Sören Franzenburg Jan Michels Ute Hentschel Beate M. Slaby Microbial Strategies for Survival in the Glass Sponge <italic toggle="yes">Vazella pourtalesii</italic>
description	ABSTRACT Few studies have explored the microbiomes of glass sponges (Hexactinellida). The present study seeks to elucidate the composition of the microbiota associated with the glass sponge Vazella pourtalesii and the functional strategies of the main symbionts. We combined microscopic approaches with metagenome-guided microbial genome reconstruction and amplicon community profiling toward this goal. Microscopic imaging revealed that the host and microbial cells appeared within dense biomass patches that are presumably syncytial tissue aggregates. Based on abundances in amplicon libraries and metagenomic data, SAR324 bacteria, Crenarchaeota, Patescibacteria, and Nanoarchaeota were identified as abundant members of the V. pourtalesii microbiome; thus, their genomic potentials were analyzed in detail. A general pattern emerged in that the V. pourtalesii symbionts had very small genome sizes, in the range of 0.5 to 2.2 Mb, and low GC contents, even below those of seawater relatives. Based on functional analyses of metagenome-assembled genomes (MAGs), we propose two major microbial strategies: the “givers,” namely, Crenarchaeota and SAR324, heterotrophs and facultative anaerobes, produce and partly secrete all required amino acids and vitamins. The “takers,” Nanoarchaeota and Patescibacteria, are anaerobes with reduced genomes that tap into the microbial community for resources, e.g., lipids and DNA, likely using pilus-like structures. We posit that the existence of microbial cells in sponge syncytia together with the low-oxygen conditions in the seawater environment are factors that shape the unique compositional and functional properties of the microbial community associated with V. pourtalesii. IMPORTANCE We investigated the microbial community of V. pourtalesii that forms globally unique, monospecific sponge grounds under low-oxygen conditions on the Scotian Shelf, where it plays a key role in its vulnerable ecosystem. The microbial community was found to be concentrated within biomass patches and is dominated by small cells (<1 μm). MAG analyses showed consistently small genome sizes and low GC contents, which is unusual compared to known sponge symbionts. These properties, as well as the (facultatively) anaerobic metabolism and a high degree of interdependence between the dominant symbionts regarding amino acid and vitamin synthesis, are likely adaptations to the unique conditions within the syncytial tissue of their hexactinellid host and the low-oxygen environment.
format	article
author	Kristina Bayer Kathrin Busch Ellen Kenchington Lindsay Beazley Sören Franzenburg Jan Michels Ute Hentschel Beate M. Slaby
author_facet	Kristina Bayer Kathrin Busch Ellen Kenchington Lindsay Beazley Sören Franzenburg Jan Michels Ute Hentschel Beate M. Slaby
author_sort	Kristina Bayer
title	Microbial Strategies for Survival in the Glass Sponge <italic toggle="yes">Vazella pourtalesii</italic>
title_short	Microbial Strategies for Survival in the Glass Sponge <italic toggle="yes">Vazella pourtalesii</italic>
title_full	Microbial Strategies for Survival in the Glass Sponge <italic toggle="yes">Vazella pourtalesii</italic>
title_fullStr	Microbial Strategies for Survival in the Glass Sponge <italic toggle="yes">Vazella pourtalesii</italic>
title_full_unstemmed	Microbial Strategies for Survival in the Glass Sponge <italic toggle="yes">Vazella pourtalesii</italic>
title_sort	microbial strategies for survival in the glass sponge <italic toggle="yes">vazella pourtalesii</italic>
publisher	American Society for Microbiology
publishDate	2020
url	https://doaj.org/article/fc2edceb76f24f7087b8c9ffdee1514c
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Microbial Strategies for Survival in the Glass Sponge <italic toggle="yes">Vazella pourtalesii</italic>

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