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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...

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Autores principales: Hyams, Yosef, Rubin-Blum, Maxim, Rosner, Amalia, Brodsky, Leonid, Rinkevich, Yuval, Rinkevich, Baruch
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2023
Materias:
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.
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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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