The dynamic genome of Hydra

Jarrod A. Chapman; Ewen F. Kirkness; Oleg Simakov; Steven E. Hampson; Therese Mitros; Thomas Weinmaier; Thomas Rattei; Prakash G. Balasubramanian; Jon Borman; Dana Busam; Kathryn Disbennett; Cynthia Pfannkoch; Nadezhda Sumin; Granger G. Sutton; Lakshmi Devi Viswanathan; Brian Walenz; David M. Goodstein; Uffe Hellsten; Takeshi Kawashima; Simon E. Prochnik; Nicholas H. Putnam; Shengquiang Shu; Bruce Blumberg; Catherine E. Dana; Lydia Gee; Dennis F. Kibler; Lee Law; Dirk Lindgens; Daniel E. Martinez; Jisong Peng; Philip A. Wigge; Bianca Bertulat; Corina Guder; Yukio Nakamura; Suat Ozbek; Hiroshi Watanabe; Konstantin Khalturin; Georg Hemmrich; André Franke; René Augustin; Sebastian Fraune; Eisuke Hayakawa; Shiho Hayakawa; Mamiko Hirose; Jung Shan Hwang; Kazuho Ikeo; Chiemi Nishimiya-Fujisawa; Atshushi Ogura; Toshio Takahashi; Patrick R.H. Steinmetz; Xiaoming Zhang; Roland Aufschnaiter; Marie Kristin Eder; Anne Kathrin Gorny; Willi Salvenmoser; Alysha M. Heimberg; Benjamin M. Wheeler; Kevin J. Peterson; Angelika Böttger; Patrick Tischler; Alexander Wolf; Takashi Gojobori; Karin A. Remington; Robert L. Strausberg; J. Craig Venter; Ulrich Technau; Bert Hobmayer; Thomas C.G. Bosch; Thomas W. Holstein; Toshitaka Fujisawa; Hans R. Bode; Charles N. David; Daniel S. Rokhsar; Robert E. Steele

doi:10.1038/nature08830

The dynamic genome of Hydra

Jarrod A. Chapman, Ewen F. Kirkness, Oleg Simakov, Steven E. Hampson, Therese Mitros, Thomas Weinmaier, Thomas Rattei, Prakash G. Balasubramanian, Jon Borman, Dana Busam, Kathryn Disbennett, Cynthia Pfannkoch, Nadezhda Sumin, Granger G. Sutton, Lakshmi Devi Viswanathan, Brian Walenz, David M. Goodstein, Uffe Hellsten, Takeshi Kawashima, Simon E. ProchnikNicholas H. Putnam, Shengquiang Shu, Bruce Blumberg, Catherine E. Dana, Lydia Gee, Dennis F. Kibler, Lee Law, Dirk Lindgens, Daniel E. Martinez, Jisong Peng, Philip A. Wigge, Bianca Bertulat, Corina Guder, Yukio Nakamura, Suat Ozbek, Hiroshi Watanabe, Konstantin Khalturin, Georg Hemmrich, André Franke, René Augustin, Sebastian Fraune, Eisuke Hayakawa, Shiho Hayakawa, Mamiko Hirose, Jung Shan Hwang, Kazuho Ikeo, Chiemi Nishimiya-Fujisawa, Atshushi Ogura, Toshio Takahashi, Patrick R.H. Steinmetz, Xiaoming Zhang, Roland Aufschnaiter, Marie Kristin Eder, Anne Kathrin Gorny, Willi Salvenmoser, Alysha M. Heimberg, Benjamin M. Wheeler, Kevin J. Peterson, Angelika Böttger, Patrick Tischler, Alexander Wolf, Takashi Gojobori, Karin A. Remington, Robert L. Strausberg, J. Craig Venter, Ulrich Technau, Bert Hobmayer, Thomas C.G. Bosch, Thomas W. Holstein, Toshitaka Fujisawa, Hans R. Bode, Charles N. David, Daniel S. Rokhsar, Robert E. Steele

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Abstract

The freshwater cnidarian Hydra was first described in 1702 and has been the object of study for 300 years. Experimental studies of Hydra between 1736 and 1744 culminated in the discovery of asexual reproduction of an animal by budding, the first description of regeneration in an animal, and successful transplantation of tissue between animals. Today, Hydra is an important model for studies of axial patterning, stem cell biology and regeneration. Here we report the genome of Hydra magnipapillata and compare it to the genomes of the anthozoan Nematostella vectensis and other animals. The Hydra genome has been shaped by bursts of transposable element expansion, horizontal gene transfer, trans-splicing, and simplification of gene structure and gene content that parallel simplification of the Hydra life cycle. We also report the sequence of the genome of a novel bacterium stably associated with H. magnipapillata. Comparisons of the Hydra genome to the genomes of other animals shed light on the evolution of epithelia, contractile tissues, developmentally regulated transcription factors, the Spemann-Mangold organizer, pluripotency genes and the neuromuscular junction.

Original language	English (US)
Pages (from-to)	592-596
Number of pages	5
Journal	NATURE
Volume	464
Issue number	7288
DOIs	https://doi.org/10.1038/nature08830
State	Published - Mar 25 2010
Externally published	Yes

Bibliographical note

Funding Information:
Acknowledgements We are grateful to S. Clifton, R. Wilson and the EST sequencing group at the Genome Sequencing Center at the Washington University School of Medicine for their efforts in generating the Hydra ESTs and to the National Science Foundation for its support of the Hydra EST project (grant number IBN-0120591). Funding for the sequencing of the Hydra genome was provided by the National Human Genome Research Institute. We thank J. Gerhart who, as co-chair of the National Human Genome Research Institute Working Group on Comparative Genome Evolution, advocated sequencing of the Hydra genome. The septate junction electron micrograph in Fig. 3 was provided by G. Rieger. K.J.P. thanks N. Margulis for technical assistance and the NSF for support (grant number DEB-0716960). U.T. was supported by the Austrian Science Fund and the Norwegian Research Council. B.H. was supported by Austrian Science Fund grants FWF P16685 and FWF P20734. D.S.R. was supported by R. Melmon and the Gordon and Betty Moore Foundation. Work at the US Department of Energy Joint Genome Institute was supported by the Office of Science of the US Department of Energy under Contract No. DE-AC02-05CH11231. T.F. and T.G. were supported by Grants-In-Aid for Scientific Research from the Ministry of Education, Culture, Sports, Science, and Technology of Japan. T.C.G.B. was supported by grants from the Deutsche Forschungsgemeinschaft (DFG SFB617-A1) and from the DFG Cluster of Excellence programs ‘The Future Ocean’ and ‘Inflammation at Interfaces’. T.W.H. was supported by grants from the Deutsche Forschungsgemeinschaft including SFB488-A12 and the DFG Cluster of Excellence program ‘CellNetworks’. Support for H.W. was provided by the TOYOBO Biotechnology Foundation and the Alexander von Humboldt Foundation. Support for A.B., B.B., C.G., C.N.D., H.W., P.G.B., S.O., T.F. (Mercator Professor) and Y.N. was provided by the Deutsche Forschungsgemeinschaft.

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10.1038/nature08830

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Chapman, J. A., Kirkness, E. F., Simakov, O., Hampson, S. E., Mitros, T., Weinmaier, T., Rattei, T., Balasubramanian, P. G., Borman, J., Busam, D., Disbennett, K., Pfannkoch, C., Sumin, N., Sutton, G. G., Viswanathan, L. D., Walenz, B., Goodstein, D. M., Hellsten, U., Kawashima, T., ... Steele, R. E. (2010). The dynamic genome of Hydra. NATURE, 464(7288), 592-596. https://doi.org/10.1038/nature08830

@article{5feb64c3164a425eb32c91612f5ebd8d,

title = "The dynamic genome of Hydra",

abstract = "The freshwater cnidarian Hydra was first described in 1702 and has been the object of study for 300 years. Experimental studies of Hydra between 1736 and 1744 culminated in the discovery of asexual reproduction of an animal by budding, the first description of regeneration in an animal, and successful transplantation of tissue between animals. Today, Hydra is an important model for studies of axial patterning, stem cell biology and regeneration. Here we report the genome of Hydra magnipapillata and compare it to the genomes of the anthozoan Nematostella vectensis and other animals. The Hydra genome has been shaped by bursts of transposable element expansion, horizontal gene transfer, trans-splicing, and simplification of gene structure and gene content that parallel simplification of the Hydra life cycle. We also report the sequence of the genome of a novel bacterium stably associated with H. magnipapillata. Comparisons of the Hydra genome to the genomes of other animals shed light on the evolution of epithelia, contractile tissues, developmentally regulated transcription factors, the Spemann-Mangold organizer, pluripotency genes and the neuromuscular junction.",

author = "Chapman, {Jarrod A.} and Kirkness, {Ewen F.} and Oleg Simakov and Hampson, {Steven E.} and Therese Mitros and Thomas Weinmaier and Thomas Rattei and Balasubramanian, {Prakash G.} and Jon Borman and Dana Busam and Kathryn Disbennett and Cynthia Pfannkoch and Nadezhda Sumin and Sutton, {Granger G.} and Viswanathan, {Lakshmi Devi} and Brian Walenz and Goodstein, {David M.} and Uffe Hellsten and Takeshi Kawashima and Prochnik, {Simon E.} and Putnam, {Nicholas H.} and Shengquiang Shu and Bruce Blumberg and Dana, {Catherine E.} and Lydia Gee and Kibler, {Dennis F.} and Lee Law and Dirk Lindgens and Martinez, {Daniel E.} and Jisong Peng and Wigge, {Philip A.} and Bianca Bertulat and Corina Guder and Yukio Nakamura and Suat Ozbek and Hiroshi Watanabe and Konstantin Khalturin and Georg Hemmrich and Andr{\'e} Franke and Ren{\'e} Augustin and Sebastian Fraune and Eisuke Hayakawa and Shiho Hayakawa and Mamiko Hirose and Hwang, {Jung Shan} and Kazuho Ikeo and Chiemi Nishimiya-Fujisawa and Atshushi Ogura and Toshio Takahashi and Steinmetz, {Patrick R.H.} and Xiaoming Zhang and Roland Aufschnaiter and Eder, {Marie Kristin} and Gorny, {Anne Kathrin} and Willi Salvenmoser and Heimberg, {Alysha M.} and Wheeler, {Benjamin M.} and Peterson, {Kevin J.} and Angelika B{\"o}ttger and Patrick Tischler and Alexander Wolf and Takashi Gojobori and Remington, {Karin A.} and Strausberg, {Robert L.} and Venter, {J. Craig} and Ulrich Technau and Bert Hobmayer and Bosch, {Thomas C.G.} and Holstein, {Thomas W.} and Toshitaka Fujisawa and Bode, {Hans R.} and David, {Charles N.} and Rokhsar, {Daniel S.} and Steele, {Robert E.}",

note = "Funding Information: Acknowledgements We are grateful to S. Clifton, R. Wilson and the EST sequencing group at the Genome Sequencing Center at the Washington University School of Medicine for their efforts in generating the Hydra ESTs and to the National Science Foundation for its support of the Hydra EST project (grant number IBN-0120591). Funding for the sequencing of the Hydra genome was provided by the National Human Genome Research Institute. We thank J. Gerhart who, as co-chair of the National Human Genome Research Institute Working Group on Comparative Genome Evolution, advocated sequencing of the Hydra genome. The septate junction electron micrograph in Fig. 3 was provided by G. Rieger. K.J.P. thanks N. Margulis for technical assistance and the NSF for support (grant number DEB-0716960). U.T. was supported by the Austrian Science Fund and the Norwegian Research Council. B.H. was supported by Austrian Science Fund grants FWF P16685 and FWF P20734. D.S.R. was supported by R. Melmon and the Gordon and Betty Moore Foundation. Work at the US Department of Energy Joint Genome Institute was supported by the Office of Science of the US Department of Energy under Contract No. DE-AC02-05CH11231. T.F. and T.G. were supported by Grants-In-Aid for Scientific Research from the Ministry of Education, Culture, Sports, Science, and Technology of Japan. T.C.G.B. was supported by grants from the Deutsche Forschungsgemeinschaft (DFG SFB617-A1) and from the DFG Cluster of Excellence programs {\textquoteleft}The Future Ocean{\textquoteright} and {\textquoteleft}Inflammation at Interfaces{\textquoteright}. T.W.H. was supported by grants from the Deutsche Forschungsgemeinschaft including SFB488-A12 and the DFG Cluster of Excellence program {\textquoteleft}CellNetworks{\textquoteright}. Support for H.W. was provided by the TOYOBO Biotechnology Foundation and the Alexander von Humboldt Foundation. Support for A.B., B.B., C.G., C.N.D., H.W., P.G.B., S.O., T.F. (Mercator Professor) and Y.N. was provided by the Deutsche Forschungsgemeinschaft.",

year = "2010",

month = mar,

day = "25",

doi = "10.1038/nature08830",

language = "English (US)",

volume = "464",

pages = "592--596",

journal = "NATURE",

issn = "0028-0836",

publisher = "Nature Research",

number = "7288",

}

Chapman, JA, Kirkness, EF, Simakov, O, Hampson, SE, Mitros, T, Weinmaier, T, Rattei, T, Balasubramanian, PG, Borman, J, Busam, D, Disbennett, K, Pfannkoch, C, Sumin, N, Sutton, GG, Viswanathan, LD, Walenz, B, Goodstein, DM, Hellsten, U, Kawashima, T, Prochnik, SE, Putnam, NH, Shu, S, Blumberg, B, Dana, CE, Gee, L, Kibler, DF, Law, L, Lindgens, D, Martinez, DE, Peng, J, Wigge, PA, Bertulat, B, Guder, C, Nakamura, Y, Ozbek, S, Watanabe, H, Khalturin, K, Hemmrich, G, Franke, A, Augustin, R, Fraune, S, Hayakawa, E, Hayakawa, S, Hirose, M, Hwang, JS, Ikeo, K, Nishimiya-Fujisawa, C, Ogura, A, Takahashi, T, Steinmetz, PRH, Zhang, X, Aufschnaiter, R, Eder, MK, Gorny, AK, Salvenmoser, W, Heimberg, AM, Wheeler, BM, Peterson, KJ, Böttger, A, Tischler, P, Wolf, A, Gojobori, T, Remington, KA, Strausberg, RL, Venter, JC, Technau, U, Hobmayer, B, Bosch, TCG, Holstein, TW, Fujisawa, T, Bode, HR, David, CN, Rokhsar, DS & Steele, RE 2010, 'The dynamic genome of Hydra', NATURE, vol. 464, no. 7288, pp. 592-596. https://doi.org/10.1038/nature08830

TY - JOUR

T1 - The dynamic genome of Hydra

AU - Chapman, Jarrod A.

AU - Kirkness, Ewen F.

AU - Simakov, Oleg

AU - Hampson, Steven E.

AU - Mitros, Therese

AU - Weinmaier, Thomas

AU - Rattei, Thomas

AU - Balasubramanian, Prakash G.

AU - Borman, Jon

AU - Busam, Dana

AU - Disbennett, Kathryn

AU - Pfannkoch, Cynthia

AU - Sumin, Nadezhda

AU - Sutton, Granger G.

AU - Viswanathan, Lakshmi Devi

AU - Walenz, Brian

AU - Goodstein, David M.

AU - Hellsten, Uffe

AU - Kawashima, Takeshi

AU - Prochnik, Simon E.

AU - Putnam, Nicholas H.

AU - Shu, Shengquiang

AU - Blumberg, Bruce

AU - Dana, Catherine E.

AU - Gee, Lydia

AU - Kibler, Dennis F.

AU - Law, Lee

AU - Lindgens, Dirk

AU - Martinez, Daniel E.

AU - Peng, Jisong

AU - Wigge, Philip A.

AU - Bertulat, Bianca

AU - Guder, Corina

AU - Nakamura, Yukio

AU - Ozbek, Suat

AU - Watanabe, Hiroshi

AU - Khalturin, Konstantin

AU - Hemmrich, Georg

AU - Franke, André

AU - Augustin, René

AU - Fraune, Sebastian

AU - Hayakawa, Eisuke

AU - Hayakawa, Shiho

AU - Hirose, Mamiko

AU - Hwang, Jung Shan

AU - Ikeo, Kazuho

AU - Nishimiya-Fujisawa, Chiemi

AU - Ogura, Atshushi

AU - Takahashi, Toshio

AU - Steinmetz, Patrick R.H.

AU - Zhang, Xiaoming

AU - Aufschnaiter, Roland

AU - Eder, Marie Kristin

AU - Gorny, Anne Kathrin

AU - Salvenmoser, Willi

AU - Heimberg, Alysha M.

AU - Wheeler, Benjamin M.

AU - Peterson, Kevin J.

AU - Böttger, Angelika

AU - Tischler, Patrick

AU - Wolf, Alexander

AU - Gojobori, Takashi

AU - Remington, Karin A.

AU - Strausberg, Robert L.

AU - Venter, J. Craig

AU - Technau, Ulrich

AU - Hobmayer, Bert

AU - Bosch, Thomas C.G.

AU - Holstein, Thomas W.

AU - Fujisawa, Toshitaka

AU - Bode, Hans R.

AU - David, Charles N.

AU - Rokhsar, Daniel S.

AU - Steele, Robert E.

N1 - Funding Information: Acknowledgements We are grateful to S. Clifton, R. Wilson and the EST sequencing group at the Genome Sequencing Center at the Washington University School of Medicine for their efforts in generating the Hydra ESTs and to the National Science Foundation for its support of the Hydra EST project (grant number IBN-0120591). Funding for the sequencing of the Hydra genome was provided by the National Human Genome Research Institute. We thank J. Gerhart who, as co-chair of the National Human Genome Research Institute Working Group on Comparative Genome Evolution, advocated sequencing of the Hydra genome. The septate junction electron micrograph in Fig. 3 was provided by G. Rieger. K.J.P. thanks N. Margulis for technical assistance and the NSF for support (grant number DEB-0716960). U.T. was supported by the Austrian Science Fund and the Norwegian Research Council. B.H. was supported by Austrian Science Fund grants FWF P16685 and FWF P20734. D.S.R. was supported by R. Melmon and the Gordon and Betty Moore Foundation. Work at the US Department of Energy Joint Genome Institute was supported by the Office of Science of the US Department of Energy under Contract No. DE-AC02-05CH11231. T.F. and T.G. were supported by Grants-In-Aid for Scientific Research from the Ministry of Education, Culture, Sports, Science, and Technology of Japan. T.C.G.B. was supported by grants from the Deutsche Forschungsgemeinschaft (DFG SFB617-A1) and from the DFG Cluster of Excellence programs ‘The Future Ocean’ and ‘Inflammation at Interfaces’. T.W.H. was supported by grants from the Deutsche Forschungsgemeinschaft including SFB488-A12 and the DFG Cluster of Excellence program ‘CellNetworks’. Support for H.W. was provided by the TOYOBO Biotechnology Foundation and the Alexander von Humboldt Foundation. Support for A.B., B.B., C.G., C.N.D., H.W., P.G.B., S.O., T.F. (Mercator Professor) and Y.N. was provided by the Deutsche Forschungsgemeinschaft.

PY - 2010/3/25

Y1 - 2010/3/25

N2 - The freshwater cnidarian Hydra was first described in 1702 and has been the object of study for 300 years. Experimental studies of Hydra between 1736 and 1744 culminated in the discovery of asexual reproduction of an animal by budding, the first description of regeneration in an animal, and successful transplantation of tissue between animals. Today, Hydra is an important model for studies of axial patterning, stem cell biology and regeneration. Here we report the genome of Hydra magnipapillata and compare it to the genomes of the anthozoan Nematostella vectensis and other animals. The Hydra genome has been shaped by bursts of transposable element expansion, horizontal gene transfer, trans-splicing, and simplification of gene structure and gene content that parallel simplification of the Hydra life cycle. We also report the sequence of the genome of a novel bacterium stably associated with H. magnipapillata. Comparisons of the Hydra genome to the genomes of other animals shed light on the evolution of epithelia, contractile tissues, developmentally regulated transcription factors, the Spemann-Mangold organizer, pluripotency genes and the neuromuscular junction.

AB - The freshwater cnidarian Hydra was first described in 1702 and has been the object of study for 300 years. Experimental studies of Hydra between 1736 and 1744 culminated in the discovery of asexual reproduction of an animal by budding, the first description of regeneration in an animal, and successful transplantation of tissue between animals. Today, Hydra is an important model for studies of axial patterning, stem cell biology and regeneration. Here we report the genome of Hydra magnipapillata and compare it to the genomes of the anthozoan Nematostella vectensis and other animals. The Hydra genome has been shaped by bursts of transposable element expansion, horizontal gene transfer, trans-splicing, and simplification of gene structure and gene content that parallel simplification of the Hydra life cycle. We also report the sequence of the genome of a novel bacterium stably associated with H. magnipapillata. Comparisons of the Hydra genome to the genomes of other animals shed light on the evolution of epithelia, contractile tissues, developmentally regulated transcription factors, the Spemann-Mangold organizer, pluripotency genes and the neuromuscular junction.

UR - http://www.scopus.com/inward/record.url?scp=77950080387&partnerID=8YFLogxK

U2 - 10.1038/nature08830

DO - 10.1038/nature08830

M3 - Article

C2 - 20228792

AN - SCOPUS:77950080387

SN - 0028-0836

VL - 464

SP - 592

EP - 596

JO - NATURE

JF - NATURE

IS - 7288

ER -

The dynamic genome of Hydra

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