Extremotolerant tardigrade genome and improved radiotolerance of human cultured cells by tardigrade-unique protein

Takuma Hashimoto; Daiki D. Horikawa; Yuki Saito; Hirokazu Kuwahara; Hiroko Kozuka-Hata; Tadasu Shin-I; Yohei Minakuchi; Kazuko Ohishi; Ayuko Motoyama; Tomoyuki Aizu; Atsushi Enomoto; Koyuki Kondo; Sae Tanaka; Yuichiro Hara; Shigeyuki Koshikawa; Hiroshi Sagara; Toru Miura; Shin Ichi Yokobori; Kiyoshi Miyagawa; Yutaka Suzuki; Takeo Kubo; Masaaki Oyama; Yuji Kohara; Asao Fujiyama; Kazuharu Arakawa; Toshiaki Katayama; Atsushi Toyoda; Takekazu Kunieda

doi:10.1038/ncomms12808

Extremotolerant tardigrade genome and improved radiotolerance of human cultured cells by tardigrade-unique protein

Takuma Hashimoto, Daiki D. Horikawa, Yuki Saito, Hirokazu Kuwahara, Hiroko Kozuka-Hata, Tadasu Shin-I, Yohei Minakuchi, Kazuko Ohishi, Ayuko Motoyama, Tomoyuki Aizu, Atsushi Enomoto, Koyuki Kondo, Sae Tanaka, Yuichiro Hara, Shigeyuki Koshikawa, Hiroshi Sagara, Toru Miura, Shin Ichi Yokobori, Kiyoshi Miyagawa, Yutaka SuzukiTakeo Kubo, Masaaki Oyama, Yuji Kohara, Asao Fujiyama, Kazuharu Arakawa, Toshiaki Katayama, Atsushi Toyoda, Takekazu Kunieda

Research output: Contribution to journal › Article › peer-review

172 Citations (Scopus)

Abstract

Tardigrades, also known as water bears, are small aquatic animals. Some tardigrade species tolerate almost complete dehydration and exhibit extraordinary tolerance to various physical extremes in the dehydrated state. Here we determine a high-quality genome sequence of Ramazzottius varieornatus, one of the most stress-tolerant tardigrade species. Precise gene repertoire analyses reveal the presence of a small proportion (1.2% or less) of putative foreign genes, loss of gene pathways that promote stress damage, expansion of gene families related to ameliorating damage, and evolution and high expression of novel tardigrade-unique proteins. Minor changes in the gene expression profiles during dehydration and rehydration suggest constitutive expression of tolerance-related genes. Using human cultured cells, we demonstrate that a tardigrade-unique DNA-associating protein suppresses X-ray-induced DNA damage by ∼40% and improves radiotolerance. These findings indicate the relevance of tardigrade-unique proteins to tolerability and tardigrades could be a bountiful source of new protection genes and mechanisms.

Original language	English
Article number	12808
Journal	Nature communications
Volume	7
DOIs	https://doi.org/10.1038/ncomms12808
Publication status	Published - 2016 Sept 20
Externally published	Yes

ASJC Scopus subject areas

Chemistry(all)
Biochemistry, Genetics and Molecular Biology(all)
Physics and Astronomy(all)

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10.1038/ncomms12808

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Hashimoto, T., Horikawa, D. D., Saito, Y., Kuwahara, H., Kozuka-Hata, H., Shin-I, T., Minakuchi, Y., Ohishi, K., Motoyama, A., Aizu, T., Enomoto, A., Kondo, K., Tanaka, S., Hara, Y., Koshikawa, S., Sagara, H., Miura, T., Yokobori, S. I., Miyagawa, K., ... Kunieda, T. (2016). Extremotolerant tardigrade genome and improved radiotolerance of human cultured cells by tardigrade-unique protein. Nature communications, 7, [12808]. https://doi.org/10.1038/ncomms12808

Hashimoto, T, Horikawa, DD, Saito, Y, Kuwahara, H, Kozuka-Hata, H, Shin-I, T, Minakuchi, Y, Ohishi, K, Motoyama, A, Aizu, T, Enomoto, A, Kondo, K, Tanaka, S, Hara, Y, Koshikawa, S, Sagara, H, Miura, T, Yokobori, SI, Miyagawa, K, Suzuki, Y, Kubo, T, Oyama, M, Kohara, Y, Fujiyama, A, Arakawa, K, Katayama, T, Toyoda, A & Kunieda, T 2016, 'Extremotolerant tardigrade genome and improved radiotolerance of human cultured cells by tardigrade-unique protein', Nature communications, vol. 7, 12808. https://doi.org/10.1038/ncomms12808

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title = "Extremotolerant tardigrade genome and improved radiotolerance of human cultured cells by tardigrade-unique protein",

abstract = "Tardigrades, also known as water bears, are small aquatic animals. Some tardigrade species tolerate almost complete dehydration and exhibit extraordinary tolerance to various physical extremes in the dehydrated state. Here we determine a high-quality genome sequence of Ramazzottius varieornatus, one of the most stress-tolerant tardigrade species. Precise gene repertoire analyses reveal the presence of a small proportion (1.2% or less) of putative foreign genes, loss of gene pathways that promote stress damage, expansion of gene families related to ameliorating damage, and evolution and high expression of novel tardigrade-unique proteins. Minor changes in the gene expression profiles during dehydration and rehydration suggest constitutive expression of tolerance-related genes. Using human cultured cells, we demonstrate that a tardigrade-unique DNA-associating protein suppresses X-ray-induced DNA damage by ∼40% and improves radiotolerance. These findings indicate the relevance of tardigrade-unique proteins to tolerability and tardigrades could be a bountiful source of new protection genes and mechanisms.",

author = "Takuma Hashimoto and Horikawa, {Daiki D.} and Yuki Saito and Hirokazu Kuwahara and Hiroko Kozuka-Hata and Tadasu Shin-I and Yohei Minakuchi and Kazuko Ohishi and Ayuko Motoyama and Tomoyuki Aizu and Atsushi Enomoto and Koyuki Kondo and Sae Tanaka and Yuichiro Hara and Shigeyuki Koshikawa and Hiroshi Sagara and Toru Miura and Yokobori, {Shin Ichi} and Kiyoshi Miyagawa and Yutaka Suzuki and Takeo Kubo and Masaaki Oyama and Yuji Kohara and Asao Fujiyama and Kazuharu Arakawa and Toshiaki Katayama and Atsushi Toyoda and Takekazu Kunieda",

note = "Funding Information: This work was supported by JSPS/MEXT KAKENHI Grant Numbers 25281016, 16H02951, 16H01632, 20017010, 16064101 and 221S0002. T.H. received a Grant-in-Aid for JSPS Fellows (No. 25-1805) from the Japan Society for the Promotion of Science. Publisher Copyright: {\textcopyright} 2016 The Author(s).",

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doi = "10.1038/ncomms12808",

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T1 - Extremotolerant tardigrade genome and improved radiotolerance of human cultured cells by tardigrade-unique protein

AU - Hashimoto, Takuma

AU - Horikawa, Daiki D.

AU - Saito, Yuki

AU - Kuwahara, Hirokazu

AU - Kozuka-Hata, Hiroko

AU - Shin-I, Tadasu

AU - Minakuchi, Yohei

AU - Ohishi, Kazuko

AU - Motoyama, Ayuko

AU - Aizu, Tomoyuki

AU - Enomoto, Atsushi

AU - Kondo, Koyuki

AU - Tanaka, Sae

AU - Hara, Yuichiro

AU - Koshikawa, Shigeyuki

AU - Sagara, Hiroshi

AU - Miura, Toru

AU - Yokobori, Shin Ichi

AU - Miyagawa, Kiyoshi

AU - Suzuki, Yutaka

AU - Kubo, Takeo

AU - Oyama, Masaaki

AU - Kohara, Yuji

AU - Fujiyama, Asao

AU - Arakawa, Kazuharu

AU - Katayama, Toshiaki

AU - Toyoda, Atsushi

AU - Kunieda, Takekazu

N1 - Funding Information: This work was supported by JSPS/MEXT KAKENHI Grant Numbers 25281016, 16H02951, 16H01632, 20017010, 16064101 and 221S0002. T.H. received a Grant-in-Aid for JSPS Fellows (No. 25-1805) from the Japan Society for the Promotion of Science. Publisher Copyright: © 2016 The Author(s).

PY - 2016/9/20

Y1 - 2016/9/20

N2 - Tardigrades, also known as water bears, are small aquatic animals. Some tardigrade species tolerate almost complete dehydration and exhibit extraordinary tolerance to various physical extremes in the dehydrated state. Here we determine a high-quality genome sequence of Ramazzottius varieornatus, one of the most stress-tolerant tardigrade species. Precise gene repertoire analyses reveal the presence of a small proportion (1.2% or less) of putative foreign genes, loss of gene pathways that promote stress damage, expansion of gene families related to ameliorating damage, and evolution and high expression of novel tardigrade-unique proteins. Minor changes in the gene expression profiles during dehydration and rehydration suggest constitutive expression of tolerance-related genes. Using human cultured cells, we demonstrate that a tardigrade-unique DNA-associating protein suppresses X-ray-induced DNA damage by ∼40% and improves radiotolerance. These findings indicate the relevance of tardigrade-unique proteins to tolerability and tardigrades could be a bountiful source of new protection genes and mechanisms.

AB - Tardigrades, also known as water bears, are small aquatic animals. Some tardigrade species tolerate almost complete dehydration and exhibit extraordinary tolerance to various physical extremes in the dehydrated state. Here we determine a high-quality genome sequence of Ramazzottius varieornatus, one of the most stress-tolerant tardigrade species. Precise gene repertoire analyses reveal the presence of a small proportion (1.2% or less) of putative foreign genes, loss of gene pathways that promote stress damage, expansion of gene families related to ameliorating damage, and evolution and high expression of novel tardigrade-unique proteins. Minor changes in the gene expression profiles during dehydration and rehydration suggest constitutive expression of tolerance-related genes. Using human cultured cells, we demonstrate that a tardigrade-unique DNA-associating protein suppresses X-ray-induced DNA damage by ∼40% and improves radiotolerance. These findings indicate the relevance of tardigrade-unique proteins to tolerability and tardigrades could be a bountiful source of new protection genes and mechanisms.

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JO - Nature Communications

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Extremotolerant tardigrade genome and improved radiotolerance of human cultured cells by tardigrade-unique protein

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