TY - JOUR
T1 - Physiological changes during torpor favor association with Endozoicomonas endosymbionts in the urochordate Botrylloides leachii
AU - Hyams, Yosef
AU - Rubin-Blum, Maxim
AU - Rosner, Amalia
AU - Brodsky, Leonid
AU - Rinkevich, Yuval
AU - Rinkevich, Baruch
N1 - Publisher Copyright: Copyright © 2023 Hyams, Rubin-Blum, Rosner, Brodsky, Rinkevich and Rinkevich.
PY - 2023/1/1
Y1 - 2023/1/1
N2 - 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.
AB - 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.
KW - Endozoicomonas
KW - aestivation
KW - ascidians
KW - hibernation
KW - metabolism
KW - symbiosis
KW - torpor
UR - http://www.scopus.com/inward/record.url?scp=85161987726&partnerID=8YFLogxK
U2 - 10.3389/fmicb.2023.1072053
DO - 10.3389/fmicb.2023.1072053
M3 - Article
C2 - 37323901
SN - 1664-302X
VL - 14
JO - Frontiers in Microbiology
JF - Frontiers in Microbiology
M1 - 1072053
ER -