Desiccation-induced fibrous condensation of CAHS protein from an anhydrobiotic tardigrade
Abstract Anhydrobiosis, one of the most extensively studied forms of cryptobiosis, is induced in certain organisms as a response to desiccation. Anhydrobiotic species has been hypothesized to produce substances that can protect their biological components and/or cell membranes without water. In extr...
| Main Authors: | , , , , , , , , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Nature Portfolio
2021-11-01
|
| Series: | Scientific Reports |
| Online Access: | https://doi.org/10.1038/s41598-021-00724-6 |
| _version_ | 1818754110080417792 |
|---|---|
| author | Maho Yagi-Utsumi Kazuhiro Aoki Hiroki Watanabe Chihong Song Seiji Nishimura Tadashi Satoh Saeko Yanaka Christian Ganser Sae Tanaka Vincent Schnapka Ean Wai Goh Yuji Furutani Kazuyoshi Murata Takayuki Uchihashi Kazuharu Arakawa Koichi Kato |
| author_facet | Maho Yagi-Utsumi Kazuhiro Aoki Hiroki Watanabe Chihong Song Seiji Nishimura Tadashi Satoh Saeko Yanaka Christian Ganser Sae Tanaka Vincent Schnapka Ean Wai Goh Yuji Furutani Kazuyoshi Murata Takayuki Uchihashi Kazuharu Arakawa Koichi Kato |
| author_sort | Maho Yagi-Utsumi |
| collection | DOAJ |
| description | Abstract Anhydrobiosis, one of the most extensively studied forms of cryptobiosis, is induced in certain organisms as a response to desiccation. Anhydrobiotic species has been hypothesized to produce substances that can protect their biological components and/or cell membranes without water. In extremotolerant tardigrades, highly hydrophilic and heat-soluble protein families, cytosolic abundant heat-soluble (CAHS) proteins, have been identified, which are postulated to be integral parts of the tardigrades’ response to desiccation. In this study, to elucidate these protein functions, we performed in vitro and in vivo characterizations of the reversible self-assembling property of CAHS1 protein, a major isoform of CAHS proteins from Ramazzottius varieornatus, using a series of spectroscopic and microscopic techniques. We found that CAHS1 proteins homo-oligomerized via the C-terminal α-helical region and formed a hydrogel as their concentration increased. We also demonstrated that the overexpressed CAHS1 proteins formed condensates under desiccation-mimicking conditions. These data strongly suggested that, upon drying, the CAHS1 proteins form oligomers and eventually underwent sol–gel transition in tardigrade cytosols. Thus, it is proposed that the CAHS1 proteins form the cytosolic fibrous condensates, which presumably have variable mechanisms for the desiccation tolerance of tardigrades. These findings provide insights into molecular strategies of organisms to adapt to extreme environments. |
| first_indexed | 2024-12-18T05:18:02Z |
| format | Article |
| id | doaj.art-bd8100bd830e4050bb9c5f0ddb3109b9 |
| institution | Directory Open Access Journal |
| issn | 2045-2322 |
| language | English |
| last_indexed | 2024-12-18T05:18:02Z |
| publishDate | 2021-11-01 |
| publisher | Nature Portfolio |
| record_format | Article |
| series | Scientific Reports |
| spelling | doaj.art-bd8100bd830e4050bb9c5f0ddb3109b92022-12-21T21:19:43ZengNature PortfolioScientific Reports2045-23222021-11-011111910.1038/s41598-021-00724-6Desiccation-induced fibrous condensation of CAHS protein from an anhydrobiotic tardigradeMaho Yagi-Utsumi0Kazuhiro Aoki1Hiroki Watanabe2Chihong Song3Seiji Nishimura4Tadashi Satoh5Saeko Yanaka6Christian Ganser7Sae Tanaka8Vincent Schnapka9Ean Wai Goh10Yuji Furutani11Kazuyoshi Murata12Takayuki Uchihashi13Kazuharu Arakawa14Koichi Kato15Exploratory Research Center on Life and Living Systems (ExCELLS), National Institutes of Natural SciencesExploratory Research Center on Life and Living Systems (ExCELLS), National Institutes of Natural SciencesExploratory Research Center on Life and Living Systems (ExCELLS), National Institutes of Natural SciencesExploratory Research Center on Life and Living Systems (ExCELLS), National Institutes of Natural SciencesGraduate School of Pharmaceutical Sciences, Nagoya City UniversityGraduate School of Pharmaceutical Sciences, Nagoya City UniversityExploratory Research Center on Life and Living Systems (ExCELLS), National Institutes of Natural SciencesExploratory Research Center on Life and Living Systems (ExCELLS), National Institutes of Natural SciencesExploratory Research Center on Life and Living Systems (ExCELLS), National Institutes of Natural SciencesInstitute for Molecular Science (IMS), National Institutes of Natural SciencesInstitute for Molecular Science (IMS), National Institutes of Natural SciencesInstitute for Molecular Science (IMS), National Institutes of Natural SciencesExploratory Research Center on Life and Living Systems (ExCELLS), National Institutes of Natural SciencesExploratory Research Center on Life and Living Systems (ExCELLS), National Institutes of Natural SciencesExploratory Research Center on Life and Living Systems (ExCELLS), National Institutes of Natural SciencesExploratory Research Center on Life and Living Systems (ExCELLS), National Institutes of Natural SciencesAbstract Anhydrobiosis, one of the most extensively studied forms of cryptobiosis, is induced in certain organisms as a response to desiccation. Anhydrobiotic species has been hypothesized to produce substances that can protect their biological components and/or cell membranes without water. In extremotolerant tardigrades, highly hydrophilic and heat-soluble protein families, cytosolic abundant heat-soluble (CAHS) proteins, have been identified, which are postulated to be integral parts of the tardigrades’ response to desiccation. In this study, to elucidate these protein functions, we performed in vitro and in vivo characterizations of the reversible self-assembling property of CAHS1 protein, a major isoform of CAHS proteins from Ramazzottius varieornatus, using a series of spectroscopic and microscopic techniques. We found that CAHS1 proteins homo-oligomerized via the C-terminal α-helical region and formed a hydrogel as their concentration increased. We also demonstrated that the overexpressed CAHS1 proteins formed condensates under desiccation-mimicking conditions. These data strongly suggested that, upon drying, the CAHS1 proteins form oligomers and eventually underwent sol–gel transition in tardigrade cytosols. Thus, it is proposed that the CAHS1 proteins form the cytosolic fibrous condensates, which presumably have variable mechanisms for the desiccation tolerance of tardigrades. These findings provide insights into molecular strategies of organisms to adapt to extreme environments.https://doi.org/10.1038/s41598-021-00724-6 |
| spellingShingle | Maho Yagi-Utsumi Kazuhiro Aoki Hiroki Watanabe Chihong Song Seiji Nishimura Tadashi Satoh Saeko Yanaka Christian Ganser Sae Tanaka Vincent Schnapka Ean Wai Goh Yuji Furutani Kazuyoshi Murata Takayuki Uchihashi Kazuharu Arakawa Koichi Kato Desiccation-induced fibrous condensation of CAHS protein from an anhydrobiotic tardigrade Scientific Reports |
| title | Desiccation-induced fibrous condensation of CAHS protein from an anhydrobiotic tardigrade |
| title_full | Desiccation-induced fibrous condensation of CAHS protein from an anhydrobiotic tardigrade |
| title_fullStr | Desiccation-induced fibrous condensation of CAHS protein from an anhydrobiotic tardigrade |
| title_full_unstemmed | Desiccation-induced fibrous condensation of CAHS protein from an anhydrobiotic tardigrade |
| title_short | Desiccation-induced fibrous condensation of CAHS protein from an anhydrobiotic tardigrade |
| title_sort | desiccation induced fibrous condensation of cahs protein from an anhydrobiotic tardigrade |
| url | https://doi.org/10.1038/s41598-021-00724-6 |
| work_keys_str_mv | AT mahoyagiutsumi desiccationinducedfibrouscondensationofcahsproteinfromananhydrobiotictardigrade AT kazuhiroaoki desiccationinducedfibrouscondensationofcahsproteinfromananhydrobiotictardigrade AT hirokiwatanabe desiccationinducedfibrouscondensationofcahsproteinfromananhydrobiotictardigrade AT chihongsong desiccationinducedfibrouscondensationofcahsproteinfromananhydrobiotictardigrade AT seijinishimura desiccationinducedfibrouscondensationofcahsproteinfromananhydrobiotictardigrade AT tadashisatoh desiccationinducedfibrouscondensationofcahsproteinfromananhydrobiotictardigrade AT saekoyanaka desiccationinducedfibrouscondensationofcahsproteinfromananhydrobiotictardigrade AT christianganser desiccationinducedfibrouscondensationofcahsproteinfromananhydrobiotictardigrade AT saetanaka desiccationinducedfibrouscondensationofcahsproteinfromananhydrobiotictardigrade AT vincentschnapka desiccationinducedfibrouscondensationofcahsproteinfromananhydrobiotictardigrade AT eanwaigoh desiccationinducedfibrouscondensationofcahsproteinfromananhydrobiotictardigrade AT yujifurutani desiccationinducedfibrouscondensationofcahsproteinfromananhydrobiotictardigrade AT kazuyoshimurata desiccationinducedfibrouscondensationofcahsproteinfromananhydrobiotictardigrade AT takayukiuchihashi desiccationinducedfibrouscondensationofcahsproteinfromananhydrobiotictardigrade AT kazuharuarakawa desiccationinducedfibrouscondensationofcahsproteinfromananhydrobiotictardigrade AT koichikato desiccationinducedfibrouscondensationofcahsproteinfromananhydrobiotictardigrade |