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.

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).

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, 200 nm. 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.

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. b–e, 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 b–e indicate 100 nm. 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.