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Genomics-Enabled Exploration of Marine Diatoms

Genomics-Enabled Exploration of Marine Diatoms

Research staff
Chris Bowler (CNRS Research Director, Head of the Plant and Diatom Genomics laboratory) +33 (0)1 44 32 35 25

Anne-Flore Deton-Cabanillas (Research Assistant, CNRS)
Antoine Hoguin (PhD student) +33 (0)1 44 32 35 34
Catherine Cantrel (Research Assistant, CNRS) +33 (0)1 44 32 35 34
Elena Kazamia (Post-doc, Marie Curie Research Fellow)
Fabio Rocha Jimenez Vieira (Post-Doc)
Federico Ibarbalz (Post-Doc)
Flora Vincent (PhD student)
Imen Mestiri (Post-doc, CNRS)
Juan J. Pierella Karlusich (Post-doc)
Leila Tirichine Delacour (Research Director, CNRS +33 (0)1 44 32 35 34
Lucie Zinger (Assistant Professor, Ecole Normale Supérieure) +33 (0)1 44 32 35 28
Maria Helena Cruz de Carvalho (Assistant Professor, HDR, UPEC)
Martine Boccara (Professor, UPMC)
Nathalie Joli (Post-Doc)
Ouardia Ait-Mohamed (Research Ingeneer)
Richard Dorrell (Post-doc) +33 (0)1 44 32 35 34
Xue Zhao (PhD student) +33 (0)1 44 32 35 34

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 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 2008, Moustafa 2009).

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 2006, 2011). Our studies focus on P. tricornutum and exploit the availability of techniques for reverse genetics (Siaut 2007, De Riso 2009), digital gene expression profiling, genome and epigenome maps, ecotypes with differential capacities to adapt to different conditions (De Martino 2011), and distinct morphotypes that can be induced to change shape in response to ecologically relevant stimuli (Bowler Curr Op 2010).

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 2008, Allen 2011), and the evolutionary mechanisms that have led to diatom success in contemporary oceans (Bowler Ann Rev 2010).

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, 3,500 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.
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.
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.

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

• Progressive and biased divergent evolution underpins the origin and diversification of peridinin dinoflagellate plastids, 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., MBE (2017) 34 : 361-379.

• Chimeric origins of ochrophyte and haptophyte plastids revealed through an ancient plastid proteome, 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., ELife (2017) 6 : 23717

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

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

• 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. A novel protein, ubiquitous in marine phytoplankton, concentrates iron at the cell surface and facilitates uptake. Curr Biol. (2015) 25 : 364-71.

• Huysman MJ, Fortunato AE, Matthijs M, Costa BS, Vanderhaeghen R, Van den Daele H, Sachse M, Inzé D, Bowler C, Kroth PG, Wilhelm C, Falciatore A, Vyverman W, De Veylder L. AUREOCHROME1a-Mediated Induction of the Diatom-Specific Cyclin dsCYC2 Controls the Onset of Cell Division in Diatoms (Phaeodactylum tricornutum). Plant Cell. (2013).

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

• Fernie AR, Obata T, Allen AE, Araújo WL, Bowler C. Leveraging metabolomics for functional investigations in sequenced marine diatoms. Trends Plant Sci.. (2012) 17 : 395-403.

• Allen AE, Dupont CL, Oborník M, Horák A, Nunes-Nesi A, McCrow JP, Zheng H, Johnson DA, Hu H, Fernie AR, Bowler C. Evolution and metabolic significance of the urea cycle in photosynthetic diatoms. Nature. (2011) 473 : 203-207.

• Bowler C, et al. The Phaeodactylum genome reveals the evolutionary history of diatom genomes. Nature. (2008) 456 : 239-244.