Microbial strategies for survival in the glass sponge Vazella pourtalesii

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 w...

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Published in:mSystems
Main Authors: Bayer, Kristina, Busch, Kathrin, Kenchington, Ellen, Beazley, Lindsay, Franzenburg, Sören, Michelis, Jan, Hentschel, Ute, Slaby, Beate M
Format: Article in Journal/Newspaper
Language:unknown
Published: Zenodo 2020
Subjects:
Online Access:https://doi.org/10.1128/mSystems.00473-20
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spelling ftzenodo:oai:zenodo.org:3982649 2024-09-15T18:24:10+00:00 Microbial strategies for survival in the glass sponge Vazella pourtalesii Bayer, Kristina Busch, Kathrin Kenchington, Ellen Beazley, Lindsay Franzenburg, Sören Michelis, Jan Hentschel, Ute Slaby, Beate M 2020-08-11 https://doi.org/10.1128/mSystems.00473-20 unknown Zenodo https://msystems.asm.org/content/5/4/e00473-20 https://doi .pangaea.de/10.1594/PANGAEA.917599 https://www.ncbi.nlm.nih.gov/bioproject/?term=PRJNA613976 https://figshare.com/articles/Genomic_annotations_of_Vazella_pourtalesii_symbionts/12280313 https://zenodo.org/communities/sponges https://zenodo.org/communities/eu https://doi.org/10.1128/mSystems.00473-20 oai:zenodo.org:3982649 info:eu-repo/semantics/openAccess Creative Commons Attribution 4.0 International https://creativecommons.org/licenses/by/4.0/legalcode mSystems, 5, e00473-20, (2020-08-11) glass sponge Porifera Hexactinellida symbiosis microbiome microbial metabolism metagenomic binning SAR324 Crenarchaeota Patescibacteria Nanoarchaeota European Union (EU) Horizon 2020 Grant Agreement No 679849 Deep-sea Sponge Grounds Ecosystems of the North Atlantic: an integrated approach towards their preservation and sustainable exploitation SponGES info:eu-repo/semantics/article 2020 ftzenodo https://doi.org/10.1128/mSystems.00473-20 2024-07-25T20:28:26Z 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 ... Article in Journal/Newspaper North Atlantic Glass sponges Zenodo mSystems 5 4
institution Open Polar
collection Zenodo
op_collection_id ftzenodo
language unknown
topic glass sponge
Porifera
Hexactinellida
symbiosis
microbiome
microbial metabolism
metagenomic binning
SAR324
Crenarchaeota
Patescibacteria
Nanoarchaeota
European Union (EU)
Horizon 2020
Grant Agreement No 679849
Deep-sea Sponge Grounds Ecosystems of the North Atlantic: an integrated approach towards their preservation and sustainable exploitation
SponGES
spellingShingle glass sponge
Porifera
Hexactinellida
symbiosis
microbiome
microbial metabolism
metagenomic binning
SAR324
Crenarchaeota
Patescibacteria
Nanoarchaeota
European Union (EU)
Horizon 2020
Grant Agreement No 679849
Deep-sea Sponge Grounds Ecosystems of the North Atlantic: an integrated approach towards their preservation and sustainable exploitation
SponGES
Bayer, Kristina
Busch, Kathrin
Kenchington, Ellen
Beazley, Lindsay
Franzenburg, Sören
Michelis, Jan
Hentschel, Ute
Slaby, Beate M
Microbial strategies for survival in the glass sponge Vazella pourtalesii
topic_facet glass sponge
Porifera
Hexactinellida
symbiosis
microbiome
microbial metabolism
metagenomic binning
SAR324
Crenarchaeota
Patescibacteria
Nanoarchaeota
European Union (EU)
Horizon 2020
Grant Agreement No 679849
Deep-sea Sponge Grounds Ecosystems of the North Atlantic: an integrated approach towards their preservation and sustainable exploitation
SponGES
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 ...
format Article in Journal/Newspaper
author Bayer, Kristina
Busch, Kathrin
Kenchington, Ellen
Beazley, Lindsay
Franzenburg, Sören
Michelis, Jan
Hentschel, Ute
Slaby, Beate M
author_facet Bayer, Kristina
Busch, Kathrin
Kenchington, Ellen
Beazley, Lindsay
Franzenburg, Sören
Michelis, Jan
Hentschel, Ute
Slaby, Beate M
author_sort Bayer, Kristina
title Microbial strategies for survival in the glass sponge Vazella pourtalesii
title_short Microbial strategies for survival in the glass sponge Vazella pourtalesii
title_full Microbial strategies for survival in the glass sponge Vazella pourtalesii
title_fullStr Microbial strategies for survival in the glass sponge Vazella pourtalesii
title_full_unstemmed Microbial strategies for survival in the glass sponge Vazella pourtalesii
title_sort microbial strategies for survival in the glass sponge vazella pourtalesii
publisher Zenodo
publishDate 2020
url https://doi.org/10.1128/mSystems.00473-20
genre North Atlantic
Glass sponges
genre_facet North Atlantic
Glass sponges
op_source mSystems, 5, e00473-20, (2020-08-11)
op_relation https://msystems.asm.org/content/5/4/e00473-20
https://doi .pangaea.de/10.1594/PANGAEA.917599
https://www.ncbi.nlm.nih.gov/bioproject/?term=PRJNA613976
https://figshare.com/articles/Genomic_annotations_of_Vazella_pourtalesii_symbionts/12280313
https://zenodo.org/communities/sponges
https://zenodo.org/communities/eu
https://doi.org/10.1128/mSystems.00473-20
oai:zenodo.org:3982649
op_rights info:eu-repo/semantics/openAccess
Creative Commons Attribution 4.0 International
https://creativecommons.org/licenses/by/4.0/legalcode
op_doi https://doi.org/10.1128/mSystems.00473-20
container_title mSystems
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