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Genomics-Enabled Exploration of Marine Diatoms

Permanent staff
Chris Bowler (CNRS Research Director, Head of the Plant and Diatom Genomics laboratory) +33 (0)1 44 32 35 25
Lucie Zinger (Associate Professor, Ecole Normale Supérieure)
Helena Cruz de Carvalho (Associate Professor, HDR, UPEC)
Martine Boccara (Professor, Sorbonne Université)

Non-permanent staff
Anna Novak Vanclova (Post-Doc)
Antoine Hoguin (Doctorant)
Elena Kazamia (Post-doc Marie Curie)
Fabio Rocha Jimenez Vieira (Post-Doc)
Federico Ibarbalz (Post-Doc)
Florent Charton (Doctorant)
Juan J. Pierella Karlusich (Post-doc)
Lorenzo Concia (Post-Doc)
Nathalie Joli (Post-Doc)
Ouardia Ait-Mohamed (Ingénieur de Recherche)
Priscillia Pierre-Elies (Ingénieur d’Etude)
Richard Dorrell (Chercheur CNRS Momentum)
Roy Elhourany (Post-Doc, Centre national d’études spatiales - CNES)
Shun Liu (Doctorante)
Théo Sciandra (Doctorant, Cotutell Université Paris Sud et Université Laval, Quebec)
Xia GAO (Doctorant de l’Université Paris Sud)

Diatoms are one of the most important components of marine phytoplankton ecosystems and are the main players in the biological carbon pump (sequestration of CO2 from the atmosphere to the ocean depths).

Figure 1. A centric diatom from Patagonia (image from Christian Sardet, Tara Oceans).

Recently completed whole genome sequences from two species, Thalassiosira pseudonana and Phaeodactylum tricornutum, have revealed a wealth of information about the evolutionary origins and metabolic adaptations that may have led to their ecological success (Armbrust et al, 2004, Bowler 2008). A major finding is that they have acquired genes both from their endosymbiotic ancestors and by horizontal gene transfer from marine bacteria (Bowler et al, 2008 ; Moustafa et al, 2009 ; Dorrell et al, 2017)).

Figure 2. The melting pot diatom genome, derived from multiple sources during diatom evolution.

This unique melting pot of genes encodes novel capacities for metabolic management, for example allowing the integration of a urea cycle into a photosynthetic cell (Allen et al, 2011). Our studies focus on P. tricornutum and exploit the availability of techniques for reverse genetics (Tirichine et al, 2017 ; Rastogi et al, 2018), digital gene expression profiling-, genome and epigenome maps, ecotypes with differential capacities to adapt to different conditions (De Martino et al, 2011), and distinct morphotypes that can be induced to change shape in response to ecologically relevant stimuli (Bowler et al, Cur. Op. 2010 ; Tirichine et al, 2017).

Figure 3. The polymorphic diatom Phaeodactylum tricornutum (Image from Alessandra De Martino).

Using these resources we explore both the physiological functions of diatom gene products, e.g., in response to iron and nitrate availability (Allen et al, 2011 ; Morrissey et al, 2018 ; Kazamia et al, 2018), and the evolutionary mechanisms that have led to diatom success in contemporary oceans (Bailleul et al, 2015 ; Benoisto et al, 2017 ; Treguer et al, 2018).

Specific research topics that we are currently addressing are :

1. How has diatom evolution enabled interactions between chloroplasts and mitochondria that have provided diatoms with physiological and metabolic innovations ?

2. What are the molecular mechanisms underlying the ability of diatoms to survive long periods of nutrient starvation and to benefit preferentially from periodic nutrient shift-up events ?

3. What are the relative contributions of DNA sequence variation and epigenetic processes in diatom adaptive dynamics ?

The laboratory is also one of the founding members of the Tara Oceans consortium (Karsenti 2011). During this four year expedition, from 2009-2013, 40,000 samples have been collected both from surface waters and from the deep chlorophyll maxima (DCM) at 210 sampling sites defined by a wide range of diverse physico-chemical features (Bork et al, 2015).

Figure 4. The Tara Oceans Expeditions 2009-2013.

We are using these for microscopy observations, both onboard using live samples and on land using fixed samples, in order to characterize diatom populations at the species level (Colin et al, 2017.

Figure 5. A selection of diatoms collected during the Tara Oceans expedition and stained with FITC-silane (images from Atsuko Tanaka).

In parallel, nucleic acids are also being extracted and sequenced at Genoscope in order to quantify species abundance at the molecular level, define diversity and community structure, and metagenomics and metatranscriptomics approaches are being used to reveal diatom gene expression profiles in different oceanic contexts (Malviya et al, 2016 ; Carraded et al, 2018 ; Leblanc et al, 2018 ; Lewitus et al, 2018 ; Vincent et al, 2018).

Our general objective is to perform a global evaluation of diatom communities and diatom gene expression profiles in a range of different oceanic contexts. The results will provide a basis for understanding how diatom communities are structured and how they will be affected by climate change-induced phenomena in the future.

Selected publications from 2012

• Ibarbalz FM, Henry N, Brandão MC, Martini S, Busseni G, Byrne H, Coelho LP, Endo H, Gasol JM, Gregory AC, Mahé F, Rigonato J, Royo-Llonch M, Salazar G, Sanz-Sáez I, Scalco E, Soviadan D, Zayed AA, Zingone A, Labadie K, Ferland J, Marec C, Kandels S, Picheral M, Dimier C, Poulain J, Pisarev S, Carmichael M, Pesant S ; Tara Oceans Coordinators, Babin M, Boss E, Iudicone D, Jaillon O, Acinas SG, Ogata H, Pelletier E, Stemmann L, Sullivan MB, Sunagawa S, Bopp L, de Vargas C, Karp-Boss L, Wincker P, Lombard F, Bowler C, Zinger L. (2020) Global Trends in Marine Plankton Diversity across Kingdoms of Life. Cell 2019 Nov 14 ;179(5):1084-1097.

• Carradec, Q., Pelletier, E., Da Silva, C., Alberti, A., Seeleuthner, Y., Blanc-Mathieu, R., Lima-Mendez, G., Rocha, F., Tirichine, L., Labadie, K., Kirilovsky, A., Bertrand, A., Engelen, S., Madoui, M. A., Méheust, R., Poulain, J., Romac, S., Richter, D. J., Yoshikawa, G., Dimier, C., Kandels-Lewis, S., Picheral, M., Searson, S. Tara Oceans Coordinators, Jaillon, O., Aury, J. M., Karsenti, E., Sullivan, M. B., Sunagawa, S., Bork, P., Not, F., Hingamp, P., Raes, J., Guidi, L., Ogata, H., de Vargas, C., Iudicone, D., Bowler, C. and Wincker, P. (2018) A global ocean atlas of eukaryotic genes. Nat. Commun. 9 : 373

• Leblanc, K., Quéguiner, B., Diaz, F., Cornet, V., Michel-Rodriguez, M., Durrieu de Madron, X., Bowler, C., Malviya, S., Thyssen, M., Grégori, G., Rembauville, M., Grosso, O., Poulain, J., de Vargas, C., Pujo-Pay, M. and Conan, P. (2018) Nanoplanktonic diatoms are globally overlooked but play a role in spring blooms and carbon export. Nat. Commun. 9 : 953

• Kazamia, E., Sutak, R., Paz-Yepes, J., Dorrell, R. G., Rocha Jimenez Vieira, F., Mach, J., Morrissey, J., Leon, S., Lam, F., Pelletier, E., Camadro, J.-M., Bowler, C. and Lesuisse, E. (2018) Endocytosis-mediated siderophore uptake as a strategy for Fe acquisition in diatoms. Sci. Adv. 4 : eaar4536

• Rastogi, A., Maheswari, U., Dorrell, R. G., Vieira, F. R. J., Maumus, F., Kustka, A., McCarthy, J., Allen, A. E., Kersey, P., Bowler, C. and Tirichine, L. (2018) Integrative analysis of large scale transcriptome data draws a comprehensive landscape of Phaeodactylum tricornutum genome and evolutionary origin of diatoms. Sci. Rep . 8 : 4834

• Tréguer, P., Bowler, C., Moriceau, B., Dutkiewicz, S., Gehlen, M., Aumont, O., Bittner, L., Dugdale, R., Finkel, Z., Iudicone, D., Jahn, O., Guidi, L., Lasbleiz, M., Leblanc, K., Levy, M. and Pondaven, P. (2018) Influence of diatom diversity on the ocean biological carbon pump. Nature Geosci . 11 : 27-37

• Vincent, F. J., Colin, S., Romac, S., Scalco, E., Bittner, L., Garcia, Y., Lopes, R. M., Dolan, J. R., Zingone, A., de Vargas, C. and Bowler, C. (2018) The epibiotic life of the cosmopolitan diatom Fragilariopsis doliolus on heterotrophic ciliates in the open ocean. ISME J. 12 : 1094-1108

• Dorrell, R.G., Klinger, C.M., Newby, R.J., Richardson, E., Butterfield, E.R., Dacks, J.B., Howe, C.J., Nisbet, R.E.R., Bowler, C. (2017) Progressive and biased divergent evolution underpins the origin and diversification of peridinin dinoflagellate plastids. MBE 34 : 361-379

• Dorrell, R.G., Gile, G.H., Méheust, R., Bapteste, E.P., McCallum, G., Klinger, C.M., Brillet-Gueguén, L., Freeman, K., Richter, D.J., Bowler, C. (2017) Chimeric origins of ochrophyte and haptophyte plastids revealed through an ancient plastid proteome. ELife 6 : 23717

• Tirichine, L., Rastogi, A. and Bowler, C. (2017) Recent progress in diatom genomics and epigenomics. Curr. Op. Plant Biol. 36 : 46-55

• Benoiston, A. S., Ibarbalz, F. M., Bittner, L., Guidi, L., Jahn, O., Dutkiewicz, S. and Bowler, C. (2017) The evolution of diatoms and their biogeochemical functions. Phil. Trans. R. Soc. Lond. B Biol. Sci . 372 : 1728

• Colin, S., Coelho, L. P., Sunagawa, S., Bowler, C., Karsenti, E., Bork, P., Pepperkok, R. and de Vargas, C. (2017) Quantitative 3D-imaging for cell biology and ecology of environmental microbial eukaryotes. eLife 6 : e26066

• Rastogi A, Murik O, Bowler C, Tirichine L. (2016) PhytoCRISP-Ex : a web-based and stand-alone application to find specific target sequences for CRISPR/CAS editing. BMC Bioinformatics 17(1):261. doi : 10.1186/s12859-016-1143-1

• Malviya, S., Scalco, E., Audic, S., Vincent, F., Veluchamy, A., Poulain, J., Wincker, P., Iudicone, D., de Vargas, C., Bittner, L., Zingone, A. and Bowler, C. (2016) Insights into global diatom distribution and diversity in the world’s ocean. Proc. Natl. Acad. Sci. USA 113 : E1516-25

• Bork, P., Bowler, C., de Vargas, C., Gorsky, G., Karsenti, E. and Wincker, P. (2015) Tara Oceans studies plankton at planetary scale. Science 348 : 873

• Bailleul, B., Berne, N., Murik, O., Petroutsos, D., Prihoda, J, Tanaka, A., Villanova, V., Bligny, R., Flori, S., Falconet, D., Krieger-Liszkay, A., Santabarbara, S., Rappaport, F., Joliot, P., Tirichine, L., Falkowski, P. G., Cardol, P., Bowler, C. and Finazzi, G. (2015) Energetic coupling between plastids and mitochondria drives CO2 assimilation in diatoms. Nature. 524 : 366-369.

• Veluchamy A, Rastogi A, Lin X, Lombard B, Murik O, Thomas Y, Dingli F, Rivarola M1, Ott S, Liu X, Sun Y, Rabinowicz PD, McCarthy J, Allen AE1, Loew D, Bowler C, Tirichine L. (2015) An integrative analysis of post-translational histone modifications in the marine diatom Phaeodactylum tricornutum. Genome Biol.. May 20 ;16(1):102

• Morrissey J, Sutak R, Paz-Yepes J, Tanaka A, Moustafa A, Veluchamy A, Thomas Y, Botebol H, Bouget FY, McQuaid JB, Tirichine L, Allen AE, Lesuisse E, Bowler C. (2015) A novel protein, ubiquitous in marine phytoplankton, concentrates iron at the cell surface and facilitates uptake. Curr. Biol.. 25 : 364-71

• Veluchamy, A., Lin, X., Maumus, F., Rivarola, M., Bhavsar, J., Creasy, T., O’Brien, K., Sengamalay, N. A., Tallon, L. J., Smith, A. D., Rayko, E., Ahmed, I., Le Crom, S., Farrant, G. K., Sgro, J.-Y., Olson, S. A., Splinter Bondurant, S., Allen, A., Rabinowicz, P. D., Sussman, M. R., Bowler, C. and Tirichine, L. (2013) Insights into the role of DNA methylation in diatoms by genome-wide profiling in Phaeodactylum tricornutum. Nature Comm.. 4 : 2091

•Allen AE, Moustafa A, Montsant A, Eckert A, Kroth PG, Bowler C. (2012) Evolution and functional diversification of fructose bisphosphate aldolase genes in photosynthetic marine diatoms. Mol Biol Evol. 1 : 367-379