Genetic tool development in marine protists: emerging model organisms for experimental cell biology

Drahomíra Faktorová1, R Ellen R Nisbet2,3, José A Fernández Robledo4, Elena Casacuberta5, Lisa Sudek6, Andrew E Allen7,8, Manuel Ares Jr9, Cristina Aresté5, Cecilia Balestreri10, Adrian C Barbrook2, Patrick Beardslee11, Sara Bender12, David S Booth13, François-Yves Bouget14, Chris Bowler15, Susana A Breglia16, Colin Brownlee10, Gertraud Burger17, Heriberto Cerutti11, Rachele Cesaroni18, Miguel A Chiurillo19, Thomas Clemente11, Duncan B Coles4, Jackie L Collier20, Elizabeth C Cooney21, Kathryn Coyne22, Roberto Docampo19, Christopher L Dupont8, Virginia Edgcomb23, Elin Einarsson2, Pía A Elustondo16,24, Fernan Federici25, Veronica Freire-Beneitez26,27, Nastasia J Freyria4, Kodai Fukuda28, Paulo A García29, Peter R Girguis30, Fatma Gomaa30, Sebastian G Gornik31, Jian Guo6,9, Vladimír Hampl32, Yutaka Hanawa33, Esteban R Haro-Contreras16, Elisabeth Hehenberger21, Andrea Highfield10, Yoshihisa Hirakawa33, Amanda Hopes34, Christopher J Howe2, Ian Hu2, Jorge Ibañez25, Nicholas A T Irwin21, Yuu Ishii35, Natalia Ewa Janowicz32, Adam C Jones12, Ambar Kachale36, Konomi Fujimura-Kamada37, Binnypreet Kaur36, Jonathan Z Kaye12, Eleanna Kazana26,27, Patrick J Keeling21, Nicole King13, Lawrence A Klobutcher38, Noelia Lander19, Imen Lassadi2, Zhuhong Li19, Senjie Lin38, Jean-Claude Lozano14, Fulei Luan11, Shinichiro Maruyama35, Tamara Matute25, Cristina Miceli39, Jun Minagawa37,40, Mark Moosburner7,8, Sebastián R Najle5,41, Deepak Nanjappa22, Isabel C Nimmo2, Luke Noble42,43, Anna M G Novák Vanclová32, Mariusz Nowacki18, Isaac Nuñez25, Arnab Pain44,45, Angela Piersanti39, Sandra Pucciarelli39, Jan Pyrih26,32, Joshua S Rest46, Mariana Rius20, Deborah Robertson47, Albane Ruaud25,48, Iñaki Ruiz-Trillo5,49,50, Monika A Sigg13, Pamela A Silver51,52, Claudio H Slamovits16, G Jason Smith53, Brittany N Sprecher38, Rowena Stern10, Estienne C Swart18,48, Anastasios D Tsaousis26,27, Lev Tsypin54,55, Aaron Turkewitz54, Jernej Turnšek7,8,51,52, Matus Valach17, Valérie Vergé14, Peter von Dassow25,56, Tobias von der Haar26, Ross F Waller2, Lu Wang57, Xiaoxue Wen11, Glen Wheeler10, April Woods53, Huan Zhang38, Thomas Mock58, Alexandra Z Worden59,60, Julius Lukeš61

  1. Institute of Parasitology, Biology Centre, Czech Academy of Sciences and Faculty of Sciences, University of South Bohemia, České Budějovice, Czech Republic. dranov@paru.cas.cz.
  2. Department of Biochemistry, University of Cambridge, Cambridge, UK.
  3. School of Biosciences, University of Nottingham, Sutton Bonington, UK.
  4. Bigelow Laboratory for Ocean Sciences, East Boothbay, ME, USA.
  5. Institut de Biologia Evolutiva, CSIC-Universitat Pompeu Fabra, Barcelona, Spain.
  6. Monterey Bay Aquarium Research Institute, Moss Landing, CA, USA.
  7. Integrative Oceanography Division, Scripps Institution of Oceanography, University of California, San Diego, CA, USA.
  8. Microbial and Environmental Genomics, J. Craig Venter Institute, La Jolla, CA, USA.
  9. Molecular, Cell and Developmental Biology, University of California, Santa Cruz, CA, USA.
  10. The Marine Biological Association, Plymouth and School of Ocean and Earth Sciences, University of Southampton, Southampton, UK.
  11. School of Biological Sciences, University of Nebraska, Lincoln, NE, USA.
  12. Gordon and Betty Moore Foundation, Palo Alto, CA, USA.
  13. Department of Molecular and Cell Biology, University of California, Berkeley, CA, USA.
  14. Sorbonne Université, CNRS UMR7621, Observatoire Océanologique, Banyuls sur Mer, France.
  15. Institut de Biologie de l'Ecole Normale Supérieure (IBENS), Ecole Normale Supérieure, CNRS, INSERM, Université PSL, Paris, France.
  16. Centre for Comparative Genomics and Evolutionary Bioinformatics, Dalhousie University, Halifax, Nova Scotia, Canada.
  17. Department of Biochemistry and Robert-Cedergren Centre for Bioinformatics and Genomics, Université de Montréal, Montreal, Quebec, Canada.
  18. Institute of Cell Biology, University of Bern, Bern, Switzerland.
  19. Center for Tropical and Emerging Global Diseases, University of Georgia, Athens, GA, USA.
  20. School of Marine and Atmospheric Sciences, Stony Brook University, Stony Brook, NY, USA.
  21. Department of Botany, University of British Columbia, Vancouver, British Columbia, Canada.
  22. University of Delaware College of Earth, Ocean and Environment, Lewes, DE, USA.
  23. Woods Hole Oceanographic Institution, Woods Hole, MA, USA.
  24. AGADA Biosciences Inc., Halifax, Nova Scotia, Canada.
  25. Facultad Ciencias Biológicas, Pontificia Universidad Católica de Chile, Fondo de Desarrollo de Areas Prioritarias, Center for Genome Regulation and Millennium Institute for Integrative Biology (iBio), Santiago de Chile, Chile.
  26. School of Biosciences, University of Kent, Canterbury, Kent, UK.
  27. Laboratory of Molecular and Evolutionary Parasitology, University of Kent, Kent, UK.
  28. Graduate School of Life and Environmental Sciences, University of Tsukuba, Ibaraki, Japan.
  29. Department of Mechanical Engineering, Massachusetts Institute of Technology, Boston, MA, USA.
  30. Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, MA, USA.
  31. Centre for Organismal Studies, University of Heidelberg, Heidelberg, Germany.
  32. Department of Parasitology, Faculty of Science, Charles University, BIOCEV, Vestec, Czech Republic.
  33. Faculty of Life and Environmental Sciences, University of Tsukuba, Ibaraki, Japan.
  34. School of Environmental Sciences, University of East Anglia, Norwich, UK.
  35. Graduate School of Life Sciences, Tohoku University, Sendai, Miyagi, Japan.
  36. Institute of Parasitology, Biology Centre, Czech Academy of Sciences and Faculty of Sciences, University of South Bohemia, České Budějovice, Czech Republic.
  37. Division of Environmental Photobiology, National Institute for Basic Biology, Okazaki, Aichi, Japan.
  38. Department of Marine Sciences, University of Connecticut , Groton, CT, USA.
  39. School of Biosciences and Veterinary Medicine, University of Camerino, Camerino, Italy.
  40. Department of Basic Biology, School of Life Science, Graduate University for Advanced Studies, Okazaki, Aichi, Japan.
  41. Instituto de Biología Molecular y Celular, CONICET, and Facultad de Ciencias Bioquímicas y Farmacéuticas, Universidad Nacional de Rosario, Rosario, Argentina.
  42. Center for Genomics and Systems Biology, New York University, New York, NY, USA.
  43. Institute de Biologie de l'ENS, Département de biologie, École Normale Supérieure, CNRS, INSERM, Paris, France.
  44. Biological and Environmental Science and Engineering Division, King Abdullah University of Science and Technology, Thuwal, Saudi Arabia.
  45. Center for Zoonosis Control, Global Institution for Collaborative Research and Education, Hokkaido University, Sapporo, Japan.
  46. Department of Ecology and Evolution, Stony Brook University, Stony Brook, NY, USA.
  47. Lasry Center for Biosciences, Clark University, Worcester, MA, USA.
  48. Max Planck Institute for Developmental Biology, Tübingen, Germany.
  49. Departament de Genètica Microbiologia i Estadıśtica, Universitat de Barcelona, Barcelona, Spain.
  50. Catalan Institution for Research and Advanced Studies, Barcelona, Spain.
  51. Department of Systems Biology, Harvard Medical School, Boston, MA, USA.
  52. Wyss Institute for Biologically Inspired Engineering, Harvard University, Boston, MA, USA.
  53. Department of Environmental Biotechnology, Moss Landing Marine Laboratories, Moss Landing, CA, USA.
  54. Department of Molecular Genetics and Cell Biology, University of Chicago, Chicago, IL, USA.
  55. Department of Biology, California Institute of Technology, Pasadena, CA, USA.
  56. Instituto Milenio de Oceanografia de Chile, Concepción, Chile.
  57. Institute of Oceanography, Minjiang University, Fuzhou, China.
  58. School of Environmental Sciences, University of East Anglia, Norwich, UK. t.mock@uea.ac.uk.
  59. Monterey Bay Aquarium Research Institute, Moss Landing, CA, USA. azworden@geomar.de.
  60. Ocean EcoSystems Biology Unit, Marine Ecology Division, Helmholtz Centre for Ocean Research, Kiel, Germany. azworden@geomar.de.
  61. Institute of Parasitology, Biology Centre, Czech Academy of Sciences and Faculty of Sciences, University of South Bohemia, České Budějovice, Czech Republic. jula@paru.cas.cz.

Abstract

Diverse microbial ecosystems underpin life in the sea. Among these microbes are many unicellular eukaryotes that span the diversity of the eukaryotic tree of life. However, genetic tractability has been limited to a few species, which do not represent eukaryotic diversity or environmentally relevant taxa. Here, we report on the development of genetic tools in a range of protists primarily from marine environments. We present evidence for foreign DNA delivery and expression in 13 species never before transformed and for advancement of tools for eight other species, as well as potential reasons for why transformation of yet another 17 species tested was not achieved. Our resource in genetic manipulation will provide insights into the ancestral eukaryotic lifeforms, general eukaryote cell biology, protein diversification and the evolution of cellular pathways.

Presented By Drahomíra Faktorová | ORCID iD

Genetics & Genome Biology, BiotechnologyNicholas Liao2020-05 (May)