Multiomics study of a heterotardigrade, Echinisicus testudo, suggests the possibility of convergent evolution of abundant heat-soluble proteins in Tardigrada

Abstract Background Many limno-terrestrial tardigrades can enter an ametabolic state, known as anhydrobiosis, upon desiccation, in which the animals can withstand extreme environments. Through genomics studies, molecular components of anhydrobiosis are beginning to be elucidated, such as the expansi...

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Autores principales:	Yumi Murai, Maho Yagi-Utsumi, Masayuki Fujiwara, Sae Tanaka, Masaru Tomita, Koichi Kato, Kazuharu Arakawa
Formato:	article
Lenguaje:	EN
Publicado:	BMC 2021
Materias:	Echiniscus testudo Heterotardigrada Heat-soluble protein Anhydrobiosis Multiomics Biotechnology TP248.13-248.65 Genetics QH426-470
Acceso en línea:	https://doaj.org/article/339611e964d14b71aa0b23ae587e53c6
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spelling	oai:doaj.org-article:339611e964d14b71aa0b23ae587e53c62021-11-14T12:26:46ZMultiomics study of a heterotardigrade, Echinisicus testudo, suggests the possibility of convergent evolution of abundant heat-soluble proteins in Tardigrada10.1186/s12864-021-08131-x1471-2164https://doaj.org/article/339611e964d14b71aa0b23ae587e53c62021-11-01T00:00:00Zhttps://doi.org/10.1186/s12864-021-08131-xhttps://doaj.org/toc/1471-2164Abstract Background Many limno-terrestrial tardigrades can enter an ametabolic state, known as anhydrobiosis, upon desiccation, in which the animals can withstand extreme environments. Through genomics studies, molecular components of anhydrobiosis are beginning to be elucidated, such as the expansion of oxidative stress response genes, loss of stress signaling pathways, and gain of tardigrade-specific heat-soluble protein families designated CAHS and SAHS. However, to date, studies have predominantly investigated the class Eutardigrada, and molecular mechanisms in the remaining class, Heterotardigrada, still remains elusive. To address this gap in the research, we report a multiomics study of the heterotardigrade Echiniscus testudo, one of the most desiccation-tolerant species which is not yet culturable in laboratory conditions. Results In order to elucidate the molecular basis of anhydrobiosis in E. testudo, we employed a multi-omics strategy encompassing genome sequencing, differential transcriptomics, and proteomics. Using ultra-low input library sequencing protocol from a single specimen, we sequenced and assembled the 153.7 Mbp genome annotated using RNA-Seq data. None of the previously identified tardigrade-specific abundant heat-soluble genes was conserved, while the loss and expansion of existing pathways were partly shared. Furthermore, we identified two families novel abundant heat-soluble proteins, which we named E. testudo Abundant Heat Soluble (EtAHS), that are predicted to contain large stretches of disordered regions. Likewise the AHS families in eutardigrada, EtAHS shows structural changes from random coil to alphahelix as the water content was decreased in vitro. These characteristics of EtAHS proteins are analogous to those of CAHS in eutardigrades, while there is no conservation at the sequence level. Conclusions Our results suggest that Heterotardigrada have partly shared but distinct anhydrobiosis machinery compared with Eutardigrada, possibly due to convergent evolution within Tardigrada. (276/350).Yumi MuraiMaho Yagi-UtsumiMasayuki FujiwaraSae TanakaMasaru TomitaKoichi KatoKazuharu ArakawaBMCarticleEchiniscus testudoHeterotardigradaHeat-soluble proteinAnhydrobiosisMultiomicsBiotechnologyTP248.13-248.65GeneticsQH426-470ENBMC Genomics, Vol 22, Iss 1, Pp 1-14 (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	Echiniscus testudo Heterotardigrada Heat-soluble protein Anhydrobiosis Multiomics Biotechnology TP248.13-248.65 Genetics QH426-470
spellingShingle	Echiniscus testudo Heterotardigrada Heat-soluble protein Anhydrobiosis Multiomics Biotechnology TP248.13-248.65 Genetics QH426-470 Yumi Murai Maho Yagi-Utsumi Masayuki Fujiwara Sae Tanaka Masaru Tomita Koichi Kato Kazuharu Arakawa Multiomics study of a heterotardigrade, Echinisicus testudo, suggests the possibility of convergent evolution of abundant heat-soluble proteins in Tardigrada
description	Abstract Background Many limno-terrestrial tardigrades can enter an ametabolic state, known as anhydrobiosis, upon desiccation, in which the animals can withstand extreme environments. Through genomics studies, molecular components of anhydrobiosis are beginning to be elucidated, such as the expansion of oxidative stress response genes, loss of stress signaling pathways, and gain of tardigrade-specific heat-soluble protein families designated CAHS and SAHS. However, to date, studies have predominantly investigated the class Eutardigrada, and molecular mechanisms in the remaining class, Heterotardigrada, still remains elusive. To address this gap in the research, we report a multiomics study of the heterotardigrade Echiniscus testudo, one of the most desiccation-tolerant species which is not yet culturable in laboratory conditions. Results In order to elucidate the molecular basis of anhydrobiosis in E. testudo, we employed a multi-omics strategy encompassing genome sequencing, differential transcriptomics, and proteomics. Using ultra-low input library sequencing protocol from a single specimen, we sequenced and assembled the 153.7 Mbp genome annotated using RNA-Seq data. None of the previously identified tardigrade-specific abundant heat-soluble genes was conserved, while the loss and expansion of existing pathways were partly shared. Furthermore, we identified two families novel abundant heat-soluble proteins, which we named E. testudo Abundant Heat Soluble (EtAHS), that are predicted to contain large stretches of disordered regions. Likewise the AHS families in eutardigrada, EtAHS shows structural changes from random coil to alphahelix as the water content was decreased in vitro. These characteristics of EtAHS proteins are analogous to those of CAHS in eutardigrades, while there is no conservation at the sequence level. Conclusions Our results suggest that Heterotardigrada have partly shared but distinct anhydrobiosis machinery compared with Eutardigrada, possibly due to convergent evolution within Tardigrada. (276/350).
format	article
author	Yumi Murai Maho Yagi-Utsumi Masayuki Fujiwara Sae Tanaka Masaru Tomita Koichi Kato Kazuharu Arakawa
author_facet	Yumi Murai Maho Yagi-Utsumi Masayuki Fujiwara Sae Tanaka Masaru Tomita Koichi Kato Kazuharu Arakawa
author_sort	Yumi Murai
title	Multiomics study of a heterotardigrade, Echinisicus testudo, suggests the possibility of convergent evolution of abundant heat-soluble proteins in Tardigrada
title_short	Multiomics study of a heterotardigrade, Echinisicus testudo, suggests the possibility of convergent evolution of abundant heat-soluble proteins in Tardigrada
title_full	Multiomics study of a heterotardigrade, Echinisicus testudo, suggests the possibility of convergent evolution of abundant heat-soluble proteins in Tardigrada
title_fullStr	Multiomics study of a heterotardigrade, Echinisicus testudo, suggests the possibility of convergent evolution of abundant heat-soluble proteins in Tardigrada
title_full_unstemmed	Multiomics study of a heterotardigrade, Echinisicus testudo, suggests the possibility of convergent evolution of abundant heat-soluble proteins in Tardigrada
title_sort	multiomics study of a heterotardigrade, echinisicus testudo, suggests the possibility of convergent evolution of abundant heat-soluble proteins in tardigrada
publisher	BMC
publishDate	2021
url	https://doaj.org/article/339611e964d14b71aa0b23ae587e53c6
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Multiomics study of a heterotardigrade, Echinisicus testudo, suggests the possibility of convergent evolution of abundant heat-soluble proteins in Tardigrada

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