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Nat Methods. 2020 Apr 6. doi: 10.1038/s41592-020-0796-x. [Epub ahead of print]

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

Faktorová D1, Nisbet RER2,3, Fernández Robledo JA4, Casacuberta E5, Sudek L6, Allen AE7,8, Ares M Jr9, Aresté C5, Balestreri C10, Barbrook AC2, Beardslee P11, Bender S12, Booth DS13, Bouget FY14, Bowler C15, Breglia SA16, Brownlee C10, Burger G17, Cerutti H11, Cesaroni R18, Chiurillo MA19, Clemente T11, Coles DB4, Collier JL20, Cooney EC21, Coyne K22, Docampo R19, Dupont CL8, Edgcomb V23, Einarsson E2, Elustondo PA16,24, Federici F25, Freire-Beneitez V26,27, Freyria NJ4, Fukuda K28, García PA29, Girguis PR30, Gomaa F30, Gornik SG31, Guo J6,9, Hampl V32, Hanawa Y33, Haro-Contreras ER16, Hehenberger E21, Highfield A10, Hirakawa Y33, Hopes A34, Howe CJ2, Hu I2, Ibañez J25, Irwin NAT21, Ishii Y35, Janowicz NE32, Jones AC12, Kachale A36, Fujimura-Kamada K37, Kaur B36, Kaye JZ12, Kazana E26,27, Keeling PJ21, King N13, Klobutcher LA38, Lander N19, Lassadi I2, Li Z19, Lin S38, Lozano JC14, Luan F11, Maruyama S35, Matute T25, Miceli C39, Minagawa J37,40, Moosburner M7,8, Najle SR5,41, Nanjappa D22, Nimmo IC2, Noble L42,43, Novák Vanclová AMG32, Nowacki M18, Nuñez I25, Pain A44,45, Piersanti A39, Pucciarelli S39, Pyrih J26,32, Rest JS46, Rius M20, Robertson D47, Ruaud A25,48, Ruiz-Trillo I5,49,50, Sigg MA13, Silver PA51,52, Slamovits CH16, Jason Smith G53, Sprecher BN38, Stern R10, Swart EC18,48, Tsaousis AD26,27, Tsypin L54,55, Turkewitz A54, Turnšek J7,8,51,52, Valach M17, Vergé V14, von Dassow P25,56, von der Haar T26, Waller RF2, Wang L57, Wen X11, Wheeler G10, Woods A53, Zhang H38, Mock T58, Worden AZ59,60, Lukeš J61.

Author information

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.

PMID:
32251396
DOI:
10.1038/s41592-020-0796-x

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