Stability of a dominant sponge‐symbiont in spite of antibiotic‐induced microbiome disturbance

Abstract Marine sponges are known for their complex and stable microbiomes. However, the lack of a gnotobiotic sponge‐model and experimental methods to manipulate both the host and the microbial symbionts currently limit our mechanistic understanding of sponge‐microbial symbioses. We have used the N...

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Published in:Environmental Microbiology
Main Authors: Schmittmann, Lara, Rahn, Tanja, Busch, Kathrin, Fraune, Sebastian, Pita, Lucía, Hentschel, Ute
Other Authors: “la Caixa” Foundation, Deutsche Forschungsgemeinschaft, Gordon and Betty Moore Foundation, H2020 Marie Skłodowska-Curie Actions
Format: Article in Journal/Newspaper
Language:English
Published: Wiley 2022
Subjects:
Online Access:http://dx.doi.org/10.1111/1462-2920.16249
https://onlinelibrary.wiley.com/doi/pdf/10.1111/1462-2920.16249
https://onlinelibrary.wiley.com/doi/full-xml/10.1111/1462-2920.16249
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spelling crwiley:10.1111/1462-2920.16249 2024-09-15T18:23:33+00:00 Stability of a dominant sponge‐symbiont in spite of antibiotic‐induced microbiome disturbance Schmittmann, Lara Rahn, Tanja Busch, Kathrin Fraune, Sebastian Pita, Lucía Hentschel, Ute “la Caixa” Foundation Deutsche Forschungsgemeinschaft Gordon and Betty Moore Foundation H2020 Marie Skłodowska-Curie Actions 2022 http://dx.doi.org/10.1111/1462-2920.16249 https://onlinelibrary.wiley.com/doi/pdf/10.1111/1462-2920.16249 https://onlinelibrary.wiley.com/doi/full-xml/10.1111/1462-2920.16249 en eng Wiley http://creativecommons.org/licenses/by/4.0/ Environmental Microbiology volume 24, issue 12, page 6392-6410 ISSN 1462-2912 1462-2920 journal-article 2022 crwiley https://doi.org/10.1111/1462-2920.16249 2024-07-09T04:13:34Z Abstract Marine sponges are known for their complex and stable microbiomes. However, the lack of a gnotobiotic sponge‐model and experimental methods to manipulate both the host and the microbial symbionts currently limit our mechanistic understanding of sponge‐microbial symbioses. We have used the North Atlantic sponge species Halichondria panicea to evaluate the use of antibiotics to generate gnotobiotic sponges. We further asked whether the microbiome can be reestablished via recolonization with the natural microbiome. Experiments were performed in marine gnotobiotic facilities equipped with a custom‐made, sterile, flow‐through aquarium system. Bacterial abundance dynamics were monitored qualitatively and quantitatively by 16 S rRNA gene amplicon sequencing and qPCR, respectively. Antibiotics induced dysbiosis by favouring an increase of opportunistic, antibiotic‐resistant bacteria, resulting in more complex, but less specific bacteria‐bacteria interactions than in untreated sponges. The abundance of the dominant symbiont, Candidatus Halichondribacter symbioticus, remained overall unchanged, reflecting its obligately symbiotic nature. Recolonization with the natural microbiome could not reverse antibiotic‐induced dysbiosis. However, single bacterial taxa that were transferred, successfully recolonized the sponge and affected bacteria‐bacteria interactions. By experimentally manipulating microbiome composition, we could show the stability of a sponge‐symbiont clade despite microbiome dysbiosis. This study contributes to understanding both host‐bacteria and bacteria‐bacteria interactions in the sponge holobiont. Article in Journal/Newspaper North Atlantic Wiley Online Library Environmental Microbiology 24 12 6392 6410
institution Open Polar
collection Wiley Online Library
op_collection_id crwiley
language English
description Abstract Marine sponges are known for their complex and stable microbiomes. However, the lack of a gnotobiotic sponge‐model and experimental methods to manipulate both the host and the microbial symbionts currently limit our mechanistic understanding of sponge‐microbial symbioses. We have used the North Atlantic sponge species Halichondria panicea to evaluate the use of antibiotics to generate gnotobiotic sponges. We further asked whether the microbiome can be reestablished via recolonization with the natural microbiome. Experiments were performed in marine gnotobiotic facilities equipped with a custom‐made, sterile, flow‐through aquarium system. Bacterial abundance dynamics were monitored qualitatively and quantitatively by 16 S rRNA gene amplicon sequencing and qPCR, respectively. Antibiotics induced dysbiosis by favouring an increase of opportunistic, antibiotic‐resistant bacteria, resulting in more complex, but less specific bacteria‐bacteria interactions than in untreated sponges. The abundance of the dominant symbiont, Candidatus Halichondribacter symbioticus, remained overall unchanged, reflecting its obligately symbiotic nature. Recolonization with the natural microbiome could not reverse antibiotic‐induced dysbiosis. However, single bacterial taxa that were transferred, successfully recolonized the sponge and affected bacteria‐bacteria interactions. By experimentally manipulating microbiome composition, we could show the stability of a sponge‐symbiont clade despite microbiome dysbiosis. This study contributes to understanding both host‐bacteria and bacteria‐bacteria interactions in the sponge holobiont.
author2 “la Caixa” Foundation
Deutsche Forschungsgemeinschaft
Gordon and Betty Moore Foundation
H2020 Marie Skłodowska-Curie Actions
format Article in Journal/Newspaper
author Schmittmann, Lara
Rahn, Tanja
Busch, Kathrin
Fraune, Sebastian
Pita, Lucía
Hentschel, Ute
spellingShingle Schmittmann, Lara
Rahn, Tanja
Busch, Kathrin
Fraune, Sebastian
Pita, Lucía
Hentschel, Ute
Stability of a dominant sponge‐symbiont in spite of antibiotic‐induced microbiome disturbance
author_facet Schmittmann, Lara
Rahn, Tanja
Busch, Kathrin
Fraune, Sebastian
Pita, Lucía
Hentschel, Ute
author_sort Schmittmann, Lara
title Stability of a dominant sponge‐symbiont in spite of antibiotic‐induced microbiome disturbance
title_short Stability of a dominant sponge‐symbiont in spite of antibiotic‐induced microbiome disturbance
title_full Stability of a dominant sponge‐symbiont in spite of antibiotic‐induced microbiome disturbance
title_fullStr Stability of a dominant sponge‐symbiont in spite of antibiotic‐induced microbiome disturbance
title_full_unstemmed Stability of a dominant sponge‐symbiont in spite of antibiotic‐induced microbiome disturbance
title_sort stability of a dominant sponge‐symbiont in spite of antibiotic‐induced microbiome disturbance
publisher Wiley
publishDate 2022
url http://dx.doi.org/10.1111/1462-2920.16249
https://onlinelibrary.wiley.com/doi/pdf/10.1111/1462-2920.16249
https://onlinelibrary.wiley.com/doi/full-xml/10.1111/1462-2920.16249
genre North Atlantic
genre_facet North Atlantic
op_source Environmental Microbiology
volume 24, issue 12, page 6392-6410
ISSN 1462-2912 1462-2920
op_rights http://creativecommons.org/licenses/by/4.0/
op_doi https://doi.org/10.1111/1462-2920.16249
container_title Environmental Microbiology
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