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A short history of picoplankton... with some shades of green. Daniel Vaulot JAMS Symposium, Sydney - 2019-03-20

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Outline Eukaryotic picoplankton Green picoplankton Mamiellophyceae What's next ? 2 / 30

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Eukaryotic picoplankton 3 / 30

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Diatoms and dino agellates: 20-200 µm 4 / 30

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Oceanic deserts 5 / 30

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1982 - Tiny eukaryotes John Sieburth - Electron microscopy Electron microscopy Johnson, P.W. & Sieburth, J.M. 1982. J. Phycol. 18:318–27. 6 / 30

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Pico-phytoplankton diversity Not, F., Siano, R., Kooistra, W.H.C.F., Simon, N., Vaulot, D. & Probert, I. 2012. In Piganeau, G. [Ed.] Genomic Insights Gained into the Diversity, Biology and Evolution of Microbial Photosynthetic Eukaryotes. Elsevier. 7 / 30

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Pico-phytoplankton diversity Not, F., Siano, R., Kooistra, W.H.C.F., Simon, N., Vaulot, D. & Probert, I. 2012. In Piganeau, G. [Ed.] Genomic Insights Gained into the Diversity, Biology and Evolution of Microbial Photosynthetic Eukaryotes. Elsevier. 8 / 30

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1990 - Bathycoccus Isolated from 100 m off Naples 1.5 µm Eikrem, W. & Throndsen, J. 1990. Phycologia. 29:344–50. 9 / 30

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1995 - Ostreococcus Isolated from Thau lagoon (oyster production) The smallest photosynthetic eukaryote (0.8 µm) Chrétiennot-Dinet, M.-J., Courties, C., Vaquer, A., Neveux, J., Claustre, H., Lautier, J. & Machado, M.C. 1995. Phycologia. 34:285–92. 10 / 30

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1999 - Bolidomonas 1.5 µm Close to diatoms phylogenetically 11 / 30

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1999 - Bolidomonas 1.5 µm Close to diatoms phylogenetically 2011 - Triparma Group known since 1980 First isolate in 2008 Covered with silica as diatoms Confirm filiation of Bolidomonas Guillou, L., Chrétiennot-Dinet, M.-J., Medlin, L.K., Claustre, H., Loiseaux-de Goër, S. & Vaulot, D. 1999. J. Phycol. 35:368–81. Ichinomiya, M., Yoshikawa, S., Kamiya, M., Ohki, K., Takaichi, S. & Kuwata, A. 2011. J. Phycol. 47:144–51. 11 / 30

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Green picoplankton 12 / 30

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Green vs. Red lineages Falkowski, P.G., Katz, M.E., Knoll, A.H., Quigg, A., Raven, J.A., Schofield, O. & Taylor, F.J. 2004. Science. 305:354–60. 13 / 30

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What is the color of the ocean ? 1. Why did the green lineage rapidly decline in ecological importance during the early Mesozoic? 2. Why have terrestrial photoautotrophs not followed similar trajectories following the end-Permian extinction? 14 / 30

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What is the color of the ocean ? 1. Why did the green lineage rapidly decline in ecological importance during the early Mesozoic? 2. Why have terrestrial photoautotrophs not followed similar trajectories following the end-Permian extinction? But maybe the question should be: Is the ocean really red ? Falkowski, P.G., Schofield, O., Katz, M.E., van de Schootbrugge, B. & Knoll, A. 2004. In Thierstein, H. & Young, J. Eds. Coccolithophorids. Springer-Verlag, Berlin, pp. 429–53. 14 / 30

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150 stations 1 million sequences Ocean sampling day (OSD) > > 15 / 30

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40 stations Depths: 2 Fractions: 4 sequences Tara Oceans de Vargas, C., Audic, S., Henry, N., Decelle, J., Mahe, F., Logares, R., Lara, E. et al. 2015. Science. 348:1261605. > > 5.10 6 16 / 30

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Build a reference database 18S rRNA GenBank sequences Tragin, M., Lopes dos Santos, A., Christen, R. & Vaulot, D. 2016. Perspect. Phycol. 3:141–54. 17 / 30

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Data from OSD The green lineage represents 25% of marine phytoplankton 18 / 30

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Data from OSD Up to 94% ... The green lineage represents 25% of marine phytoplankton 18 / 30

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Data from OSD Up to 94% ... The green lineage represents 25% of marine phytoplankton Next question: What are the shade of green ? Tragin, M. & Vaulot, D. 2018. Sci. Rep. 8:14020. 18 / 30

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Green algae: Oceanic vs. Coastal Lopes dos Santos, A., Gourvil, P., Tragin, M., Noël, M.-H., Decelle, J., Romac, S. & Vaulot, D. 2017. ISME J. 11:512–28. 19 / 30

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Mamiellophyceae 20 / 30

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Mamiellophyceae Present everywhere in coastal waters, no obvious patterns. Tragin, M. & Vaulot, D. 2018. Sci. Rep. 8:14020. 21 / 30

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Four major genera Tragin, M. & Vaulot, D. 2019. Sci. Rep. in press. 22 / 30

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Species: Four described M. pusilla M. commoda M. bravo M. polaris Two "candidate" sp. 1 sp. 2 Micromonas Simon, N., Foulon, E., Grulois, D., Six, C., Desdevises, Y., Latimier, M., Le Gall, F. et al. 2017. Protist. 168:612–35. 23 / 30

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Metabarcodes: Nine clades/species M. pusilla M. commoda A1-A2 M. bravo B1-B2 M. polaris clades B3-B5 Micromonas Tragin, M. & Vaulot, D. 2019. Sci. Rep. in press. 24 / 30

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M. polaris only found in polar waters Micromonas 25 / 30

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M. polaris only found in polar waters B5 only found in tropical waters Micromonas Tragin, M. & Vaulot, D. 2019. Sci. Rep. in press 25 / 30

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What is next ? 26 / 30

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Genomic adaptation to the environment Bathycoccus Bathycoccus 27 / 30

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Dispensable genes ? Genomic adaptation to the environment Bathycoccus Bathycoccus Moreau, H., Verhelst, B., Couloux, A., Derelle, E., Rombauts, S., Grimsley, N., Van Bel, M. et al. 2012. Genome Biol. 13:R74. Vannier, T., ..., Vaulot, D. et al. 2016. Sci. Rep. 6:37900. 27 / 30

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Interactions Gérikas Ribeiro, C., Lopes dos Santos, A., Marie, D., Pereira Brandini, F. & Vaulot, D. 2018. ISME J. 12:1360–74. 28 / 30

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Take home messages Green algae 25% of phytoplankton Mamiellophyceae vs. Chloropicophyceae Patterns emerge at species/clade level What's next ? Link genomes and environmental adaptation Study interactions 29 / 30

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Acknowledgments EU projects PICODIV MicroB3 MACUMBA ANR projects MALINA Green Edge Phytopol CNRS Sorbonne Université Nanyang Technological University 30 / 30