The dynamic genome of Hydra

Journal name:
Nature
Volume:
464,
Pages:
592–596
Date published:
DOI:
doi:10.1038/nature08830
Received
Accepted
Published online

The freshwater cnidarian Hydra was first described in 17021 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 animals2. Today, Hydra is an important model for studies of axial patterning3, stem cell biology4 and regeneration5. Here we report the genome of Hydra magnipapillata and compare it to the genomes of the anthozoan Nematostella vectensis6 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.

At a glance

Figures

  1. Dynamics of transposable element expansion in Hydra reveals several periods of transposon activity.
    Figure 1: Dynamics of transposable element expansion in Hydra reveals several periods of transposon activity.

    a, The top panel shows phylogenetic relationships between four Hydra species based on ESTs (using Nei-Gojobori synonymous substitution rates; see Supplementary Fig. 8). The bottom panel shows the fraction of the genome that is occupied by a specific repeat class at a given divergence from the repeat consensus generated by the ReAS (recovery of ancestral sequences) algorithm (see Supplementary Information section 9). Substitution levels are corrected for multiple substitutions using the Jukes–Cantor formula K = -3/4ln(1-i4/3), where i is per cent dissimilarity on the nucleotide level from the repeat consensus. This substitution level for transposons is equivalent to Nei-Gojobori synonymous substitution rates in the ESTs. Three element expansions are inferred, the most distinct are the most ancient at ~0.4 and the most recent at 0.05 divergence levels. The middle expansion at about ~0.2 is not well synchronized and is more clearly seen for individual element classes in Supplementary Figs 5 and 6. b, c, Example of periods of activity of a single Hydra CR1 retrotransposon family (b) and the maximum likelihood phylogeny of the family (c).

  2. The neuromuscular junction in Hydra.
    Figure 2: The neuromuscular junction in Hydra.

    a, Electron micrograph of a nerve synapsing on a Hydra epitheliomuscular cell. emc, epitheliomuscular cell; nv, nerve cell. Three vesicles are located in the nerve cell at the site of contact with the epitheliomuscular cell. Scale bar, 200nm. b, Schematic diagram of a canonical neuromuscular junction. Yellow indicates presence in Hydra. Choline acetyltransferase (ChAT) is shown in red because it is not clear whether Hydra has an enzyme that prefers choline (Ch) as a substrate. Acetylcholine (ACh) molecules are shown as blue circles. The nicotinic acetylcholine receptor (nAChR) is shown in the open state with acetylcholine bound (left), and in the closed state in the absence of bound acetylcholine (right). AChE, acetylcholinesterase; ChT, choline transporter; MuSK, muscle-specific kinase; VAChT, vesicular acetylcholine transporter.

  3. Hydra cell junctions.
    Figure 3: Hydra cell junctions.

    a, Schematic diagram of the positions of cell–cell and cell–matrix contacts in Hydra epitheliomuscular cells. Septate junction, red; gap junctions, green; spot desmosomes, blue; hemidesmosome-like cell–matrix contact, yellow. Ecto, ectodermal cell; Endo, endodermal cell; M, mesoglea. For simplicity the nervous system has been omitted. be, Electron micrographs of cell–cell and cell–matrix contacts in Hydra. b, Apical septate junction. c, Spot desmosome between basal muscle processes. d, Gap junction in the lateral cell membrane. e, Hemidesmosome-like cell–mesoglea contact site. Scale bars in be indicate 100nm. f, Phylogenetic distribution of cell–cell and cell–substrate contact proteins. A filled box indicates the presence of an orthologue from the corresponding protein family as identified by SMART/Pfam analysis or conserved cysteine patterns. See Supplementary Information section 17 and Supplementary Table 21 for details.

Author information

  1. These authors contributed equally to this work.

    • Jarrod A. Chapman,
    • Ewen F. Kirkness &
    • Oleg Simakov

Affiliations

  1. US Department of Energy Joint Genome Institute, Walnut Creek, California 94598, USA

    • Jarrod A. Chapman,
    • David M. Goodstein,
    • Uffe Hellsten,
    • Simon E. Prochnik,
    • Nicholas H. Putnam,
    • Shengquiang Shu &
    • Daniel S. Rokhsar
  2. The J. Craig Venter Institute, Rockville, Maryland 20850, USA

    • Ewen F. Kirkness,
    • Jon Borman,
    • Dana Busam,
    • Kathryn Disbennett,
    • Cynthia Pfannkoch,
    • Nadezhda Sumin,
    • Granger G. Sutton,
    • Lakshmi Devi Viswanathan,
    • Brian Walenz,
    • Karin A. Remington &
    • Robert L. Strausberg
  3. Institute of Zoology, Department of Molecular Evolution and Genomics, University of Heidelberg, D-69120 Heidelberg, Germany

    • Oleg Simakov,
    • Prakash G. Balasubramanian,
    • Bianca Bertulat,
    • Corina Guder,
    • Yukio Nakamura,
    • Suat Ozbek,
    • Hiroshi Watanabe &
    • Thomas W. Holstein
  4. Center for Integrative Genomics, Department of Molecular and Cell Biology, University of California, Berkeley, California 94720, USA

    • Oleg Simakov,
    • Therese Mitros,
    • Takeshi Kawashima,
    • Nicholas H. Putnam &
    • Daniel S. Rokhsar
  5. Department of Computer Science, University of California, Irvine, California 92697-3435, USA

    • Steven E. Hampson &
    • Dennis F. Kibler
  6. Department of Genome-Oriented Bioinformatics, Technische Universität München, D-85354 Freising, Germany

    • Thomas Weinmaier,
    • Thomas Rattei &
    • Patrick Tischler
  7. Department of Developmental and Cell Biology,

    • Bruce Blumberg,
    • Lydia Gee,
    • Lee Law,
    • Dirk Lindgens,
    • Jisong Peng &
    • Hans R. Bode
  8. Developmental Biology Center, University of California, Irvine, California 92697-2275, USA

    • Bruce Blumberg,
    • Catherine E. Dana,
    • Lydia Gee,
    • Lee Law,
    • Dirk Lindgens,
    • Jisong Peng,
    • Hans R. Bode &
    • Robert E. Steele
  9. Department of Biological Chemistry, University of California, Irvine, California 92697-1700, USA

    • Catherine E. Dana &
    • Robert E. Steele
  10. Department of Biology, Pomona College, Claremont, California 91711, USA

    • Daniel E. Martinez
  11. The Salk Institute, La Jolla, California 92037, USA

    • Philip A. Wigge
  12. Zoologisches Institüt, Christian-Albrechts-University, D-24098 Kiel, Germany

    • Konstantin Khalturin,
    • Georg Hemmrich,
    • André Franke,
    • René Augustin,
    • Sebastian Fraune &
    • Thomas C. G. Bosch
  13. National Institute of Genetics, Yata 1, 111, Mishima 411-8540, Japan

    • Eisuke Hayakawa,
    • Shiho Hayakawa,
    • Mamiko Hirose,
    • Jung Shan Hwang,
    • Kazuho Ikeo,
    • Chiemi Nishimiya-Fujisawa,
    • Atshushi Ogura,
    • Takashi Gojobori &
    • Toshitaka Fujisawa
  14. Suntory Institute for Bioorganic Research, Osaka 618-8503, Japan

    • Toshio Takahashi
  15. Department of Molecular Evolution and Development, University of Vienna, A-1090 Vienna, Austria

    • Patrick R. H. Steinmetz &
    • Ulrich Technau
  16. Department of Anatomy and Cell Biology, The University of Kansas Medical Center, Kansas City, Kansas 66160, USA

    • Xiaoming Zhang
  17. Institute of Zoology and Center for Molecular Biosciences, University of Innsbruck, A-6020 Innsbruck, Austria

    • Roland Aufschnaiter,
    • Marie-Kristin Eder,
    • Anne-Kathrin Gorny,
    • Willi Salvenmoser &
    • Bert Hobmayer
  18. Department of Biological Sciences, Dartmouth College, Hanover, New Hampshire 03755, USA

    • Alysha M. Heimberg &
    • Kevin J. Peterson
  19. Department of Computer Science, North Carolina State University, Raleigh, North Carolina 27695, USA

    • Benjamin M. Wheeler
  20. Department of Biology II, Ludwig-Maximilians-University, D-82152 Planegg-Martinsried, Germany

    • Angelika Böttger,
    • Alexander Wolf &
    • Charles N. David
  21. Deceased.

    • Steven E. Hampson
  22. Present addresses: Department of Cell and Developmental Biology, John Innes Centre, Norwich NR4 7UH, UK (P.A.W.); Institute of Human Genetics, University of Heidelberg, D-69120 Heidelberg, Germany (A.-K.G.); Center for Bioinformatics and Computational Biology, National Institute of General Medical Sciences, Bethesda, Maryland 20892-6200, USA (K.A.R.); Department of Ecology and Evolutionary Biology, Rice University, Houston, Texas 77251-1892, USA (N.H.P.); Ochadai Academic Production, Ochanomizu University, Ohtsuka, Bunkyo, 1128610 Tokyo, Japan (A.O.).

    • Nicholas H. Putnam,
    • Philip A. Wigge,
    • Atshushi Ogura,
    • Anne-Kathrin Gorny &
    • Karin A. Remington

Corresponding authors

Correspondence to:

Two different assemblies of the Hydra magnipapillata strain 105 genome were generated and deposited in GenBank under accession numbers ABRM00000000 and ACZU00000000. The Curvibacter sp. genome sequence has been deposited in GenBank under accession numbers FN543101, FN543102, FN543103, FN543104, FN543105, FN543106, FN543107 and FN543108.

Author details

Supplementary information

PDF files

  1. Supplementary Information (7.5M)

    This file contains Supplementary Sections S1-S18, Supplementary Tables S1-21, Supplementary Figures S1-S19 with legends, and Supplementary References.

Additional data