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Comparative genomics of the tardigrades Hypsibius dujardini and Ramazzottius varieornatus

Yuki Yoshida, Georgios Koutsovoulos, Dominik R. Laetsch, Lewis Stevens, Sujai Kumar, Daiki D. Horikawa, Kyoko Ishino, Shiori Komine, Takekazu Kunieda, Masaru Tomita, Mark Blaxter, Kazuharu Arakawa
doi: https://doi.org/10.1101/112664
Yuki Yoshida
1Institute for Advanced Biosciences, Keio University, Kakuganji 246-2, Mizukami, Tsuruoka City Yamagata, Japan
2Systems Biology Program, Graduate School of Media and Governance, Keio University, 5322, Endo, Fujisawa City, Kanagawa, Japan
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Georgios Koutsovoulos
3Institute of Evolutionary Biology, School of Biological Sciences, University of Edinburgh EH9 4JT UK
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Dominik R. Laetsch
3Institute of Evolutionary Biology, School of Biological Sciences, University of Edinburgh EH9 4JT UK
4The James Hutton Institute, Dundee DD2 5DA, United Kingdom
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Lewis Stevens
3Institute of Evolutionary Biology, School of Biological Sciences, University of Edinburgh EH9 4JT UK
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Sujai Kumar
3Institute of Evolutionary Biology, School of Biological Sciences, University of Edinburgh EH9 4JT UK
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Daiki D. Horikawa
1Institute for Advanced Biosciences, Keio University, Kakuganji 246-2, Mizukami, Tsuruoka City Yamagata, Japan
2Systems Biology Program, Graduate School of Media and Governance, Keio University, 5322, Endo, Fujisawa City, Kanagawa, Japan
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Kyoko Ishino
1Institute for Advanced Biosciences, Keio University, Kakuganji 246-2, Mizukami, Tsuruoka City Yamagata, Japan
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Shiori Komine
1Institute for Advanced Biosciences, Keio University, Kakuganji 246-2, Mizukami, Tsuruoka City Yamagata, Japan
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Takekazu Kunieda
5Department of Biological Sciences, Graduate School of Science, University of Tokyo, Hongo 7-3-1, Bunkyo-ku, Tokyo, Japan
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Masaru Tomita
1Institute for Advanced Biosciences, Keio University, Kakuganji 246-2, Mizukami, Tsuruoka City Yamagata, Japan
2Systems Biology Program, Graduate School of Media and Governance, Keio University, 5322, Endo, Fujisawa City, Kanagawa, Japan
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Mark Blaxter
3Institute of Evolutionary Biology, School of Biological Sciences, University of Edinburgh EH9 4JT UK
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Kazuharu Arakawa
1Institute for Advanced Biosciences, Keio University, Kakuganji 246-2, Mizukami, Tsuruoka City Yamagata, Japan
2Systems Biology Program, Graduate School of Media and Governance, Keio University, 5322, Endo, Fujisawa City, Kanagawa, Japan
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ABSTRACT

Tardigrada, a phylum of meiofaunal organisms, have been at the center of discussions of the evolution of Metazoa, the biology of survival in extreme environments, and the role of horizontal gene transfer in animal evolution. Tardigrada are placed as sisters to Arthropoda and Onychophora (velvet worms) in the superphylum Ecdysozoa by morphological analyses, but many molecular phylogenies fail to recover this relationship. This tension between molecular and morphological understanding may be very revealing of the mode and patterns of evolution of major groups. Similar to bdelloid rotifers, nematodes and other animals of the water film, limno-terrestrial tardigrades display extreme cryptobiotic abilities, including anhydrobiosis and cryobiosis. These extremophile behaviors challenge understanding of normal, aqueous physiology: how does a multicellular organism avoid lethal cellular collapse in the absence of liquid water? Meiofaunal species have been reported to have elevated levels of HGT events, but how important this is in evolution, and in particular in the evolution of extremophile physiology, is unclear. To address these questions, we resequenced and reassembled the genome of Hypsibius dujardini, a limno-terrestrial tardigrade that can undergo anhydrobiosis only after extensive pre-exposure to drying conditions, and compared it to the genome of Ramazzottius varieornatus, a related species with tolerance to rapid desiccation. The two species had contrasting gene expression responses to anhydrobiosis, with major transcriptional change in H. dujardini but limited regulation in R. varieornatus. We identified few horizontally transferred genes, but some of these were shown to be involved in entry into anhydrobiosis. Whole-genome molecular phylogenies supported a Tardigrada+Nematoda relationship over Tardigrada+Arthropoda, but rare genomic changes tended to support Tardigrada+Arthropoda.

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-ND 4.0 International license.
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Posted March 01, 2017.
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Comparative genomics of the tardigrades Hypsibius dujardini and Ramazzottius varieornatus
Yuki Yoshida, Georgios Koutsovoulos, Dominik R. Laetsch, Lewis Stevens, Sujai Kumar, Daiki D. Horikawa, Kyoko Ishino, Shiori Komine, Takekazu Kunieda, Masaru Tomita, Mark Blaxter, Kazuharu Arakawa
bioRxiv 112664; doi: https://doi.org/10.1101/112664
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Comparative genomics of the tardigrades Hypsibius dujardini and Ramazzottius varieornatus
Yuki Yoshida, Georgios Koutsovoulos, Dominik R. Laetsch, Lewis Stevens, Sujai Kumar, Daiki D. Horikawa, Kyoko Ishino, Shiori Komine, Takekazu Kunieda, Masaru Tomita, Mark Blaxter, Kazuharu Arakawa
bioRxiv 112664; doi: https://doi.org/10.1101/112664

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