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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.

SUBMITTER: Chapman JA

PROVIDER: S-EPMC4479502 | biostudies-literature | 2010 Mar

REPOSITORIES: biostudies-literature

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The dynamic genome of Hydra.

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

Nature 20100314 7288

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 ...[more]

PMID: 20228792

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Project description:BACKGROUND: Animal mitochondrial (mt) genomes are characteristically circular molecules of approximately 16-20 kb. Medusozoa (Cnidaria excluding Anthozoa) are exceptional in that their mt genomes are linear and sometimes subdivided into two to presumably four different molecules. In the genus Hydra, the mt genome comprises one or two mt chromosomes. Here, we present the whole mt genome sequence from the hydrozoan Hydra magnipapillata, comprising the first sequence of a fragmented metazoan mt genome encoded on two linear mt chromosomes (mt1 and mt2). RESULTS: The H. magnipapillata mt chromosomes contain the typical metazoan set of 13 genes for respiratory proteins, the two rRNA genes and two tRNA genes. All genes are unidirectionally oriented on mt1 and mt2, and several genes overlap. The gene arrangement suggests that the two mt chromosomes originated from one linear molecule that separated between nd5 and rns. Strong correlations between the AT content of rRNA genes (rns and rnl) and the AT content of protein-coding genes among 24 cnidarian genomes imply that base composition is mainly determined by mt genome-wide constraints. We show that identical inverted terminal repeats (ITR) occur on both chromosomes; these ITR contain a partial copy or part of the 3' end of cox1 (54 bp). Additionally, both mt chromosomes possess identical oriented sequences (IOS) at the 5' and 3' ends (5' and 3' IOS) adjacent to the ITR. The 5' IOS contains trnM and non-coding sequences (119 bp), whereas the 3' IOS comprises a larger part (mt2) with a larger partial copy of cox1 (243 bp). CONCLUSION: ITR are also documented in the two other available medusozoan mt genomes (Aurelia aurita and Hydra oligactis). In H. magnipapillata, the arrangement of ITR and 5' IOS and 3' IOS suggest that these regions are crucial for mt DNA replication and/or transcription initiation. An analogous organization occurs in a highly fragmented ichthyosporean mt genome. With our data, we can reject a model of mt replication that has previously been proposed for Hydra. This raises new questions regarding replication mechanisms probably employed by all medusozoans, and also has general implications for the expected organization of fragmented linear mt chromosomes of other taxa.

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The dynamic genome of Hydra.

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The dynamic genome of Hydra.

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