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The genome of the water strider Gerris buenoi reveals expansions of gene repertoires associated with adaptations to life on the water

View ORCID ProfileDavid Armisén, Rajendhran Rajakumar, View ORCID ProfileMarkus Friedrich, View ORCID ProfileJoshua B Benoit, Hugh M. Robertson, View ORCID ProfileKristen A. Panfilio, View ORCID ProfileSeung-Joon Ahn, View ORCID ProfileMonica F. Poelchau, Hsu Chao, View ORCID ProfileHuyen Dinh, View ORCID ProfileHarshaVardhan Doddapaneni, View ORCID ProfileShannon Dugan, Richard A. Gibbs, Daniel S.T. Hughes, View ORCID ProfileYi Han, Sandra L. Lee, Shwetha C. Murali, View ORCID ProfileDonna M. Muzny, View ORCID ProfileJiaxin Qu, View ORCID ProfileKim C. Worley, View ORCID ProfileMonica Munoz-Torres, Ehab Abouheif, François Bonneton, Travis Chen, Li-Mei Chiang, Christopher P. Childers, View ORCID ProfileAndrew Graham Cridge, View ORCID ProfileAntonin Jean Johan Crumière, Amelie Decaras, Elise M. Didion, View ORCID ProfileElizabeth Duncan, Elena N. Elpidina, Marie-Julie Favé, Cédric Finet, View ORCID ProfileChris G.C. Jacobs, Alys Jarvela, Emily J. Jennings, Jeffery W. Jones, Maryna P. Lesoway, Mackenzie Lovegrove, Alexander Martynov, Brenda Oppert, Angelica Lillico-Ouachour, Arjuna Rajakumar, Peter Nagui Refki, View ORCID ProfileAndrew J. Rosendale, Maria Emilia Santos, William Toubiana, View ORCID ProfileMaurijn van der Zee, Iris M. Vargas Jentzsch, Aidamalia Vargas Lowman, Severine Viala, View ORCID ProfileStephen Richards, View ORCID ProfileAbderrahman Khila
doi: https://doi.org/10.1101/242230
David Armisén
1Institut de Génomique Fonctionnelle de Lyon, Université de Lyon, Université Claude Bernard Lyon 1, CNRS UMR 5242, Ecole Normale Supérieure de Lyon, 46, allée d’Italie, 69364 Lyon Cedex 07, France
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Rajendhran Rajakumar
2Department of Molecular Genetics & Microbiology and UF Genetics Institute, University of Florida, 2033 Mowry Road, Gainesville, Florida 32610-3610, USA
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Markus Friedrich
3Department of Biological Sciences, Wayne State University, Detroit, Michigan 48202, USA
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Joshua B Benoit
4Department of Biological Sciences, McMicken College of Arts and Sciences, University of Cincinnati, 318 College Drive, Cincinnati OH 45221-0006 USA
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Hugh M. Robertson
5Department of Entomology, University of Illinois at Urbana-Champaign, Urbana, Illinois 61801, USA
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Kristen A. Panfilio
6Institute for Zoology: Developmental Biology, University of Cologne, Zülpicher Str. 47b, 50674 Cologne, Germany
7School of Life Sciences, University of Warwick, Gibbet Hill Campus, Coventry CV4 7AL, UK
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Seung-Joon Ahn
8USDA-ARS Horticultural Crops Research Unit, 3420 NW Orchard Avenue, Corvallis, OR 97330, USA
9Department of Crop and Soil Science, Oregon State University, 3050 SW Campus Way, Corvallis, OR 97331, USA
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Monica F. Poelchau
10USDA Agricultural Research Service, National Agricultural Library, Beltsville, MD 20705, USA
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  • ORCID record for Monica F. Poelchau
Hsu Chao
11Human Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, Texas 77030, USA
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Huyen Dinh
11Human Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, Texas 77030, USA
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HarshaVardhan Doddapaneni
11Human Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, Texas 77030, USA
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Shannon Dugan
11Human Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, Texas 77030, USA
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Richard A. Gibbs
11Human Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, Texas 77030, USA
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Daniel S.T. Hughes
11Human Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, Texas 77030, USA
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Yi Han
11Human Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, Texas 77030, USA
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Sandra L. Lee
11Human Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, Texas 77030, USA
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Shwetha C. Murali
12Howard Hughes Medical Institute, University of Washington, Seattle, WA 98195, USA
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Donna M. Muzny
11Human Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, Texas 77030, USA
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Jiaxin Qu
11Human Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, Texas 77030, USA
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Kim C. Worley
11Human Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, Texas 77030, USA
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Monica Munoz-Torres
13Lawrence Berkeley National Laboratory, Berkeley, California, USA;
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Ehab Abouheif
14McGill University, Department of Biology, 1205 Avenue Docteur Penfield Avenue, Montréal, Québec H3A 1B1, Canada
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François Bonneton
1Institut de Génomique Fonctionnelle de Lyon, Université de Lyon, Université Claude Bernard Lyon 1, CNRS UMR 5242, Ecole Normale Supérieure de Lyon, 46, allée d’Italie, 69364 Lyon Cedex 07, France
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Travis Chen
14McGill University, Department of Biology, 1205 Avenue Docteur Penfield Avenue, Montréal, Québec H3A 1B1, Canada
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Li-Mei Chiang
10USDA Agricultural Research Service, National Agricultural Library, Beltsville, MD 20705, USA
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Christopher P. Childers
10USDA Agricultural Research Service, National Agricultural Library, Beltsville, MD 20705, USA
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Andrew Graham Cridge
15Laboratory for Evolution and Development, Department of Biochemistry, University of Otago, P.O. Box 56, Dunedin, Aotearoa-New Zealand
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Antonin Jean Johan Crumière
1Institut de Génomique Fonctionnelle de Lyon, Université de Lyon, Université Claude Bernard Lyon 1, CNRS UMR 5242, Ecole Normale Supérieure de Lyon, 46, allée d’Italie, 69364 Lyon Cedex 07, France
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Amelie Decaras
1Institut de Génomique Fonctionnelle de Lyon, Université de Lyon, Université Claude Bernard Lyon 1, CNRS UMR 5242, Ecole Normale Supérieure de Lyon, 46, allée d’Italie, 69364 Lyon Cedex 07, France
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Elise M. Didion
4Department of Biological Sciences, McMicken College of Arts and Sciences, University of Cincinnati, 318 College Drive, Cincinnati OH 45221-0006 USA
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Elizabeth Duncan
15Laboratory for Evolution and Development, Department of Biochemistry, University of Otago, P.O. Box 56, Dunedin, Aotearoa-New Zealand
16School of Biology, Faculty of Biological Sciences, University of Leeds, Leeds LS2 9JT, United Kingdom
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Elena N. Elpidina
17A.N. Belozersky Institute of Physico-Chemical Biology, Moscow State University, Moscow 119991, Russia
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Marie-Julie Favé
14McGill University, Department of Biology, 1205 Avenue Docteur Penfield Avenue, Montréal, Québec H3A 1B1, Canada
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Cédric Finet
1Institut de Génomique Fonctionnelle de Lyon, Université de Lyon, Université Claude Bernard Lyon 1, CNRS UMR 5242, Ecole Normale Supérieure de Lyon, 46, allée d’Italie, 69364 Lyon Cedex 07, France
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Chris G.C. Jacobs
18Institute of Biology, Leiden University, Sylviusweg 72, 2333 BE Leiden, Netherlands
19Max Planck Institute for Chemical Ecology, Hans-Knöll Strasse 8, 07745 Jena, Germany
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Alys Jarvela
20University of Maryland, College Park, 4291 Fieldhouse Dr., Plant Sciences Building, Rm. 4112, College Park, MD 20742, USA
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Emily J. Jennings
4Department of Biological Sciences, McMicken College of Arts and Sciences, University of Cincinnati, 318 College Drive, Cincinnati OH 45221-0006 USA
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Jeffery W. Jones
3Department of Biological Sciences, Wayne State University, Detroit, Michigan 48202, USA
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Maryna P. Lesoway
14McGill University, Department of Biology, 1205 Avenue Docteur Penfield Avenue, Montréal, Québec H3A 1B1, Canada
21Smithsonian Tropical Research Institute, Naos Island Laboratories, Apartado Postal 084-303092, Balboa, Ancon, Republic of Panama.
22Department of Cell and Developmental Biology, University of Illinois, Urbana, IL.
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Mackenzie Lovegrove
9Department of Crop and Soil Science, Oregon State University, 3050 SW Campus Way, Corvallis, OR 97331, USA
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Alexander Martynov
23Center for Data-Intensive Biomedicine and Biotechnology, Skolkovo Institute of Science and Technology, Skolkovo 143025 Russia
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Brenda Oppert
24USDA Agricultural Research Service, Center for Grain and Animal Health Research, 1515 College Ave., Manhattan, KS, 66502 USA
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Angelica Lillico-Ouachour
14McGill University, Department of Biology, 1205 Avenue Docteur Penfield Avenue, Montréal, Québec H3A 1B1, Canada
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Arjuna Rajakumar
14McGill University, Department of Biology, 1205 Avenue Docteur Penfield Avenue, Montréal, Québec H3A 1B1, Canada
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Peter Nagui Refki
1Institut de Génomique Fonctionnelle de Lyon, Université de Lyon, Université Claude Bernard Lyon 1, CNRS UMR 5242, Ecole Normale Supérieure de Lyon, 46, allée d’Italie, 69364 Lyon Cedex 07, France
25Max-Planck-Institut für Evolutionsbiologie. Department of Evolutionary Genetics. August-Thienemann-Straße 2, 24306 Plön, Germany
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Andrew J. Rosendale
4Department of Biological Sciences, McMicken College of Arts and Sciences, University of Cincinnati, 318 College Drive, Cincinnati OH 45221-0006 USA
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Maria Emilia Santos
1Institut de Génomique Fonctionnelle de Lyon, Université de Lyon, Université Claude Bernard Lyon 1, CNRS UMR 5242, Ecole Normale Supérieure de Lyon, 46, allée d’Italie, 69364 Lyon Cedex 07, France
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William Toubiana
1Institut de Génomique Fonctionnelle de Lyon, Université de Lyon, Université Claude Bernard Lyon 1, CNRS UMR 5242, Ecole Normale Supérieure de Lyon, 46, allée d’Italie, 69364 Lyon Cedex 07, France
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Maurijn van der Zee
18Institute of Biology, Leiden University, Sylviusweg 72, 2333 BE Leiden, Netherlands
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  • ORCID record for Maurijn van der Zee
Iris M. Vargas Jentzsch
6Institute for Zoology: Developmental Biology, University of Cologne, Zülpicher Str. 47b, 50674 Cologne, Germany
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Aidamalia Vargas Lowman
1Institut de Génomique Fonctionnelle de Lyon, Université de Lyon, Université Claude Bernard Lyon 1, CNRS UMR 5242, Ecole Normale Supérieure de Lyon, 46, allée d’Italie, 69364 Lyon Cedex 07, France
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Severine Viala
1Institut de Génomique Fonctionnelle de Lyon, Université de Lyon, Université Claude Bernard Lyon 1, CNRS UMR 5242, Ecole Normale Supérieure de Lyon, 46, allée d’Italie, 69364 Lyon Cedex 07, France
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Stephen Richards
11Human Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, Texas 77030, USA
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Abderrahman Khila
1Institut de Génomique Fonctionnelle de Lyon, Université de Lyon, Université Claude Bernard Lyon 1, CNRS UMR 5242, Ecole Normale Supérieure de Lyon, 46, allée d’Italie, 69364 Lyon Cedex 07, France
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Abstract

The semi-aquatic bugs conquered water surfaces worldwide and occupy ponds, streams, lakes, mangroves, and even open oceans. As such, they inspired a range of scientific studies from ecology and evolution to developmental genetics and hydrodynamics of fluid locomotion. However, the lack of a representative water strider genome hinders thorough investigations of the mechanisms underlying the processes of adaptation and diversification in this group. Here we report the sequencing and manual annotation of the Gerris buenoi (G. buenoi) genome, the first water strider genome to be sequenced so far. G. buenoi genome is about 1 000Mb and the sequencing effort recovered 20 949 predicted protein-coding genes. Manual annotation uncovered a number of local (tandem and proximal) gene duplications and expansions of gene families known for their importance in a variety of processes associated with morphological and physiological adaptations to water surface lifestyle. These expansions affect key processes such as growth, vision, desiccation resistance, detoxification, olfaction and epigenetic components. Strikingly, the G. buenoi genome contains three Insulin Receptors, a unique case among metazoans, suggesting key changes in the rewiring and function of the insulin pathway. Other genomic changes include wavelength sensitivity shifts in opsin proteins likely in association with the requirements of vision in water habitats. Our findings suggest that local gene duplications might have had an important role during the evolution of water striders. These findings along with the G. buenoi genome open exciting research opportunities to understand adaptation and genome evolution of this unique hemimetabolous insect.

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The genome of the water strider Gerris buenoi reveals expansions of gene repertoires associated with adaptations to life on the water
David Armisén, Rajendhran Rajakumar, Markus Friedrich, Joshua B Benoit, Hugh M. Robertson, Kristen A. Panfilio, Seung-Joon Ahn, Monica F. Poelchau, Hsu Chao, Huyen Dinh, HarshaVardhan Doddapaneni, Shannon Dugan, Richard A. Gibbs, Daniel S.T. Hughes, Yi Han, Sandra L. Lee, Shwetha C. Murali, Donna M. Muzny, Jiaxin Qu, Kim C. Worley, Monica Munoz-Torres, Ehab Abouheif, François Bonneton, Travis Chen, Li-Mei Chiang, Christopher P. Childers, Andrew Graham Cridge, Antonin Jean Johan Crumière, Amelie Decaras, Elise M. Didion, Elizabeth Duncan, Elena N. Elpidina, Marie-Julie Favé, Cédric Finet, Chris G.C. Jacobs, Alys Jarvela, Emily J. Jennings, Jeffery W. Jones, Maryna P. Lesoway, Mackenzie Lovegrove, Alexander Martynov, Brenda Oppert, Angelica Lillico-Ouachour, Arjuna Rajakumar, Peter Nagui Refki, Andrew J. Rosendale, Maria Emilia Santos, William Toubiana, Maurijn van der Zee, Iris M. Vargas Jentzsch, Aidamalia Vargas Lowman, Severine Viala, Stephen Richards, Abderrahman Khila
bioRxiv 242230; doi: https://doi.org/10.1101/242230
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The genome of the water strider Gerris buenoi reveals expansions of gene repertoires associated with adaptations to life on the water
David Armisén, Rajendhran Rajakumar, Markus Friedrich, Joshua B Benoit, Hugh M. Robertson, Kristen A. Panfilio, Seung-Joon Ahn, Monica F. Poelchau, Hsu Chao, Huyen Dinh, HarshaVardhan Doddapaneni, Shannon Dugan, Richard A. Gibbs, Daniel S.T. Hughes, Yi Han, Sandra L. Lee, Shwetha C. Murali, Donna M. Muzny, Jiaxin Qu, Kim C. Worley, Monica Munoz-Torres, Ehab Abouheif, François Bonneton, Travis Chen, Li-Mei Chiang, Christopher P. Childers, Andrew Graham Cridge, Antonin Jean Johan Crumière, Amelie Decaras, Elise M. Didion, Elizabeth Duncan, Elena N. Elpidina, Marie-Julie Favé, Cédric Finet, Chris G.C. Jacobs, Alys Jarvela, Emily J. Jennings, Jeffery W. Jones, Maryna P. Lesoway, Mackenzie Lovegrove, Alexander Martynov, Brenda Oppert, Angelica Lillico-Ouachour, Arjuna Rajakumar, Peter Nagui Refki, Andrew J. Rosendale, Maria Emilia Santos, William Toubiana, Maurijn van der Zee, Iris M. Vargas Jentzsch, Aidamalia Vargas Lowman, Severine Viala, Stephen Richards, Abderrahman Khila
bioRxiv 242230; doi: https://doi.org/10.1101/242230

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