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Physiological changes during torpor favor association with Endozoicomonas endosymbionts in the urochordate Botrylloides leachii
Environmental perturbations evoke down-regulation of metabolism in some multicellular organisms, leading to dormancy, or torpor. Colonies of the urochordate Botrylloides leachii enter torpor in response to changes in seawater temperature and may survive for months as small vasculature remnants that...
Autores principales: | , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
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Frontiers Media S.A.
2023
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Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10264598/ https://www.ncbi.nlm.nih.gov/pubmed/37323901 http://dx.doi.org/10.3389/fmicb.2023.1072053 |
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author | Hyams, Yosef Rubin-Blum, Maxim Rosner, Amalia Brodsky, Leonid Rinkevich, Yuval Rinkevich, Baruch |
author_facet | Hyams, Yosef Rubin-Blum, Maxim Rosner, Amalia Brodsky, Leonid Rinkevich, Yuval Rinkevich, Baruch |
author_sort | Hyams, Yosef |
collection | PubMed |
description | Environmental perturbations evoke down-regulation of metabolism in some multicellular organisms, leading to dormancy, or torpor. Colonies of the urochordate Botrylloides leachii enter torpor in response to changes in seawater temperature and may survive for months as small vasculature remnants that lack feeding and reproductive organs but possess torpor-specific microbiota. Upon returning to milder conditions, the colonies rapidly restore their original morphology, cytology and functionality while harboring re-occurring microbiota, a phenomenon that has not been described in detail to date. Here we investigated the stability of B. leachii microbiome and its functionality in active and dormant colonies, using microscopy, qPCR, in situ hybridization, genomics and transcriptomics. A novel lineage of Endozoicomonas, proposed here as Candidatus Endozoicomonas endoleachii, was dominant in torpor animals (53–79% read abundance), and potentially occupied specific hemocytes found only in torpid animals. Functional analysis of the metagenome-assembled genome and genome-targeted transcriptomics revealed that Endozoicomonas can use various cellular substrates, like amino acids and sugars, potentially producing biotin and thiamine, but also expressing various features involved in autocatalytic symbiosis. Our study suggests that the microbiome can be linked to the metabolic and physiological states of the host, B. leachii, introducing a model organism for the study of symbioses during drastic physiological changes, such as torpor. |
format | Online Article Text |
id | pubmed-10264598 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2023 |
publisher | Frontiers Media S.A. |
record_format | MEDLINE/PubMed |
spelling | pubmed-102645982023-06-15 Physiological changes during torpor favor association with Endozoicomonas endosymbionts in the urochordate Botrylloides leachii Hyams, Yosef Rubin-Blum, Maxim Rosner, Amalia Brodsky, Leonid Rinkevich, Yuval Rinkevich, Baruch Front Microbiol Microbiology Environmental perturbations evoke down-regulation of metabolism in some multicellular organisms, leading to dormancy, or torpor. Colonies of the urochordate Botrylloides leachii enter torpor in response to changes in seawater temperature and may survive for months as small vasculature remnants that lack feeding and reproductive organs but possess torpor-specific microbiota. Upon returning to milder conditions, the colonies rapidly restore their original morphology, cytology and functionality while harboring re-occurring microbiota, a phenomenon that has not been described in detail to date. Here we investigated the stability of B. leachii microbiome and its functionality in active and dormant colonies, using microscopy, qPCR, in situ hybridization, genomics and transcriptomics. A novel lineage of Endozoicomonas, proposed here as Candidatus Endozoicomonas endoleachii, was dominant in torpor animals (53–79% read abundance), and potentially occupied specific hemocytes found only in torpid animals. Functional analysis of the metagenome-assembled genome and genome-targeted transcriptomics revealed that Endozoicomonas can use various cellular substrates, like amino acids and sugars, potentially producing biotin and thiamine, but also expressing various features involved in autocatalytic symbiosis. Our study suggests that the microbiome can be linked to the metabolic and physiological states of the host, B. leachii, introducing a model organism for the study of symbioses during drastic physiological changes, such as torpor. Frontiers Media S.A. 2023-05-31 /pmc/articles/PMC10264598/ /pubmed/37323901 http://dx.doi.org/10.3389/fmicb.2023.1072053 Text en Copyright © 2023 Hyams, Rubin-Blum, Rosner, Brodsky, Rinkevich and Rinkevich. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms. |
spellingShingle | Microbiology Hyams, Yosef Rubin-Blum, Maxim Rosner, Amalia Brodsky, Leonid Rinkevich, Yuval Rinkevich, Baruch Physiological changes during torpor favor association with Endozoicomonas endosymbionts in the urochordate Botrylloides leachii |
title | Physiological changes during torpor favor association with Endozoicomonas endosymbionts in the urochordate Botrylloides leachii |
title_full | Physiological changes during torpor favor association with Endozoicomonas endosymbionts in the urochordate Botrylloides leachii |
title_fullStr | Physiological changes during torpor favor association with Endozoicomonas endosymbionts in the urochordate Botrylloides leachii |
title_full_unstemmed | Physiological changes during torpor favor association with Endozoicomonas endosymbionts in the urochordate Botrylloides leachii |
title_short | Physiological changes during torpor favor association with Endozoicomonas endosymbionts in the urochordate Botrylloides leachii |
title_sort | physiological changes during torpor favor association with endozoicomonas endosymbionts in the urochordate botrylloides leachii |
topic | Microbiology |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10264598/ https://www.ncbi.nlm.nih.gov/pubmed/37323901 http://dx.doi.org/10.3389/fmicb.2023.1072053 |
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