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...
Published in: | Environmental Microbiology |
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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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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 |
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Wiley Online Library |
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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 |
container_volume |
24 |
container_issue |
12 |
container_start_page |
6392 |
op_container_end_page |
6410 |
_version_ |
1810463773467607040 |