Sequential host-bacteria and bacteria-bacteria interactions determine the microbiome establishment of Nematostella vectensis
Abstract Background The microbiota of multicellular organisms undergoes considerable changes during host ontogeny but the general mechanisms that control community assembly and succession are poorly understood. Here, we use bacterial recolonization experiments in Nematostella vectensis as a model to...
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| Format: | Article |
| Language: | English |
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BMC
2023-11-01
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| Series: | Microbiome |
| Online Access: | https://doi.org/10.1186/s40168-023-01701-z |
| _version_ | 1797557798701105152 |
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| author | H. Domin J. Zimmermann J. Taubenheim G. Fuentes Reyes L. Saueressig D. Prasse M. Höppner R. A. Schmitz U. Hentschel C. Kaleta S. Fraune |
| author_facet | H. Domin J. Zimmermann J. Taubenheim G. Fuentes Reyes L. Saueressig D. Prasse M. Höppner R. A. Schmitz U. Hentschel C. Kaleta S. Fraune |
| author_sort | H. Domin |
| collection | DOAJ |
| description | Abstract Background The microbiota of multicellular organisms undergoes considerable changes during host ontogeny but the general mechanisms that control community assembly and succession are poorly understood. Here, we use bacterial recolonization experiments in Nematostella vectensis as a model to understand general mechanisms determining bacterial establishment and succession. We compared the dynamic establishment of the microbiome on the germfree host and on inert silicone tubes. Results Following the dynamic reconstruction of microbial communities on both substrates, we show that the initial colonization events are strongly influenced by the host but not by the silicone tube, while the subsequent bacteria-bacteria interactions are the main driver of bacterial succession. Interestingly, the recolonization pattern on adult hosts resembles the ontogenetic colonization succession. This process occurs independently of the bacterial composition of the inoculum and can be followed at the level of individual bacteria. To identify potential metabolic traits associated with initial colonization success and potential metabolic interactions among bacteria associated with bacterial succession, we reconstructed the metabolic networks of bacterial colonizers based on their genomes. These analyses revealed that bacterial metabolic capabilities reflect the recolonization pattern, and the degradation of chitin might be a selection factor during early recolonization of the animal. Concurrently, transcriptomic analyses revealed that Nematostella possesses two chitin synthase genes, one of which is upregulated during early recolonization. Conclusions Our results show that early recolonization events are strongly controlled by the host while subsequent colonization depends on metabolic bacteria-bacteria interactions largely independent of host ontogeny. Video Abstract |
| first_indexed | 2024-03-10T17:21:17Z |
| format | Article |
| id | doaj.art-4eecbc7b54e14d55b134876a8756b38f |
| institution | Directory Open Access Journal |
| issn | 2049-2618 |
| language | English |
| last_indexed | 2024-03-10T17:21:17Z |
| publishDate | 2023-11-01 |
| publisher | BMC |
| record_format | Article |
| series | Microbiome |
| spelling | doaj.art-4eecbc7b54e14d55b134876a8756b38f2023-11-20T10:19:37ZengBMCMicrobiome2049-26182023-11-0111111710.1186/s40168-023-01701-zSequential host-bacteria and bacteria-bacteria interactions determine the microbiome establishment of Nematostella vectensisH. Domin0J. Zimmermann1J. Taubenheim2G. Fuentes Reyes3L. Saueressig4D. Prasse5M. Höppner6R. A. Schmitz7U. Hentschel8C. Kaleta9S. Fraune10Institute for Zoology and Organismic Interactions, Heinrich-Heine-University DüsseldorfResearch Group Medical Systems Biology, Institute of Experimental Medicine, Christian-Albrechts-University KielInstitute for Zoology and Organismic Interactions, Heinrich-Heine-University DüsseldorfInstitute for Zoology and Organismic Interactions, Heinrich-Heine-University DüsseldorfInstitute for Zoology and Organismic Interactions, Heinrich-Heine-University DüsseldorfInstitute for General Microbiology, Christian-Albrechts-University KielInstitute for Clinical Molecular Biology, Christian-Albrechts-University KielInstitute for General Microbiology, Christian-Albrechts-University KielRD3 Marine Symbioses, GEOMAR Helmholtz Centre for Ocean ResearchResearch Group Medical Systems Biology, Institute of Experimental Medicine, Christian-Albrechts-University KielInstitute for Zoology and Organismic Interactions, Heinrich-Heine-University DüsseldorfAbstract Background The microbiota of multicellular organisms undergoes considerable changes during host ontogeny but the general mechanisms that control community assembly and succession are poorly understood. Here, we use bacterial recolonization experiments in Nematostella vectensis as a model to understand general mechanisms determining bacterial establishment and succession. We compared the dynamic establishment of the microbiome on the germfree host and on inert silicone tubes. Results Following the dynamic reconstruction of microbial communities on both substrates, we show that the initial colonization events are strongly influenced by the host but not by the silicone tube, while the subsequent bacteria-bacteria interactions are the main driver of bacterial succession. Interestingly, the recolonization pattern on adult hosts resembles the ontogenetic colonization succession. This process occurs independently of the bacterial composition of the inoculum and can be followed at the level of individual bacteria. To identify potential metabolic traits associated with initial colonization success and potential metabolic interactions among bacteria associated with bacterial succession, we reconstructed the metabolic networks of bacterial colonizers based on their genomes. These analyses revealed that bacterial metabolic capabilities reflect the recolonization pattern, and the degradation of chitin might be a selection factor during early recolonization of the animal. Concurrently, transcriptomic analyses revealed that Nematostella possesses two chitin synthase genes, one of which is upregulated during early recolonization. Conclusions Our results show that early recolonization events are strongly controlled by the host while subsequent colonization depends on metabolic bacteria-bacteria interactions largely independent of host ontogeny. Video Abstracthttps://doi.org/10.1186/s40168-023-01701-z |
| spellingShingle | H. Domin J. Zimmermann J. Taubenheim G. Fuentes Reyes L. Saueressig D. Prasse M. Höppner R. A. Schmitz U. Hentschel C. Kaleta S. Fraune Sequential host-bacteria and bacteria-bacteria interactions determine the microbiome establishment of Nematostella vectensis Microbiome |
| title | Sequential host-bacteria and bacteria-bacteria interactions determine the microbiome establishment of Nematostella vectensis |
| title_full | Sequential host-bacteria and bacteria-bacteria interactions determine the microbiome establishment of Nematostella vectensis |
| title_fullStr | Sequential host-bacteria and bacteria-bacteria interactions determine the microbiome establishment of Nematostella vectensis |
| title_full_unstemmed | Sequential host-bacteria and bacteria-bacteria interactions determine the microbiome establishment of Nematostella vectensis |
| title_short | Sequential host-bacteria and bacteria-bacteria interactions determine the microbiome establishment of Nematostella vectensis |
| title_sort | sequential host bacteria and bacteria bacteria interactions determine the microbiome establishment of nematostella vectensis |
| url | https://doi.org/10.1186/s40168-023-01701-z |
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