Publications by authors named "Chris Bowler"

169 Publications

Iron metabolism strategies in diatoms.

J Exp Bot 2021 Mar;72(6):2165-2180

Institut de Biologie de l'ENS (IBENS), Département de Biologie, École Normale Supérieure, CNRS, INSERM, Université PSL, 75005 Paris, France.

Diatoms are one of the most successful group of photosynthetic eukaryotes in the contemporary ocean. They are ubiquitously distributed and are the most abundant primary producers in polar waters. Equally remarkable is their ability to tolerate iron deprivation and respond to periodic iron fertilization. Despite their relatively large cell sizes, diatoms tolerate iron limitation and frequently dominate iron-stimulated phytoplankton blooms, both natural and artificial. Here, we review the main iron use strategies of diatoms, including their ability to assimilate and store a range of iron sources, and the adaptations of their photosynthetic machinery and architecture to iron deprivation. Our synthesis relies on published literature and is complemented by a search of 82 diatom transcriptomes, including information collected from seven representatives of the most abundant diatom genera in the world's oceans.
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http://dx.doi.org/10.1093/jxb/eraa575DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7966952PMC
March 2021

Complex Response of the Chlorarachniophyte Bigelowiella natans to Iron Availability.

mSystems 2021 Feb 9;6(1). Epub 2021 Feb 9.

Department of Parasitology, Faculty of Science, Charles University, BIOCEV, Vestec, Czech Republic

The productivity of the ocean is largely dependent on iron availability, and marine phytoplankton have evolved sophisticated mechanisms to cope with chronically low iron levels in vast regions of the open ocean. By analyzing the metabarcoding data generated from the Oceans expedition, we determined how the global distribution of the model marine chlorarachniophyte varies across regions with different iron concentrations. We performed a comprehensive proteomics analysis of the molecular mechanisms underpinning the adaptation of to iron scarcity and report on the temporal response of cells to iron enrichment. Our results highlight the role of phytotransferrin in iron homeostasis and indicate the involvement of CREG1 protein in the response to iron availability. Analysis of the Oceans metagenomes and metatranscriptomes also points to a similar role for CREG1, which is found to be widely distributed among marine plankton but to show a strong bias in gene and transcript abundance toward iron-deficient regions. Our analyses allowed us to define a new subfamily of the CobW domain-containing COG0523 putative metal chaperones which are involved in iron metabolism and are restricted to only a few phytoplankton lineages in addition to At the physiological level, we elucidated the mechanisms allowing a fast recovery of PSII photochemistry after resupply of iron. Collectively, our study demonstrates that is well adapted to dynamically respond to a changing iron environment and suggests that CREG1 and COG0523 are important components of iron homeostasis in and other phytoplankton. Despite low iron availability in the ocean, marine phytoplankton require considerable amounts of iron for their growth and proliferation. While there is a constantly growing knowledge of iron uptake and its role in the cellular processes of the most abundant marine photosynthetic groups, there are still largely overlooked branches of the eukaryotic tree of life, such as the chlorarachniophytes. In the present work, we focused on the model chlorarachniophyte , integrating physiological and proteomic analyses in culture conditions with the mining of omics data generated by the Oceans expedition. We provide unique insight into the complex responses of to iron availability, including novel links to iron metabolism conserved in other phytoplankton lineages.
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http://dx.doi.org/10.1128/mSystems.00738-20DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7883536PMC
February 2021

Genome-wide analysis of allele-specific expression of genes in the model diatom Phaeodactylum tricornutum.

Sci Rep 2021 Feb 3;11(1):2954. Epub 2021 Feb 3.

Institut de Biologie de l'Ecole Normale Supérieure (IBENS), Ecole Normale Supérieure, CNRS, INSERM, PSL Université Paris, 75005, Paris, France.

Recent advances in next generation sequencing technologies have allowed the discovery of widespread autosomal allele-specific expression (aASE) in mammals and plants with potential phenotypic effects. Extensive numbers of genes with allele-specific expression have been described in the diatom Fragilariopsis cylindrus in association with adaptation to external cues, as well as in Fistulifera solaris in the context of natural hybridization. However, the role of aASE and its extent in diatoms remain elusive. In this study, we investigate allele-specific expression in the model diatom Phaeodactylum tricornutum by the re-analysis of previously published whole genome RNA sequencing data and polymorphism calling. We found that 22% of P. tricornutum genes show moderate bias in allelic expression while 1% show nearly complete monoallelic expression. Biallelic expression associates with genes encoding components of protein metabolism while moderately biased genes associate with functions in catabolism and protein transport. We validated candidate genes by pyrosequencing and found that moderate biases in allelic expression were less stable than monoallelically expressed genes that showed consistent bias upon experimental validations at the population level and in subcloning experiments. Our approach provides the basis for the analysis of aASE in P. tricornutum and could be routinely implemented to test for variations in allele expression under different environmental conditions.
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http://dx.doi.org/10.1038/s41598-021-82529-1DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7859220PMC
February 2021

Genome wide natural variation of H3K27me3 selectively marks genes predicted to be important for cell differentiation in Phaeodactylum tricornutum.

New Phytol 2021 03 31;229(6):3208-3220. Epub 2020 Dec 31.

Institut de Biologie de l'ENS (IBENS), Département de Biologie, École Normale Supérieure, CNRS, INSERM, Université PSL, Paris, 75005, France.

In multicellular organisms, Polycomb Repressive Complex2 (PRC2) is known to deposit tri-methylation of lysine 27 of histone H3 (H3K27me3) to establish and maintain gene silencing, critical for developmentally regulated processes. The PRC2 complex is absent in both widely studied model yeasts, which initially suggested that PRC2 arose with the emergence of multicellularity. However, its discovery in several unicellular species including microalgae questions its role in unicellular eukaryotes. Here, we use Phaeodactylum tricornutum enhancer of zeste E(z) knockouts and show that P. tricornutum E(z) is responsible for di- and tri-methylation of lysine 27 of histone H3. H3K27me3 depletion abolishes cell morphology in P. tricornutum providing evidence for its role in cell differentiation. Genome-wide profiling of H3K27me3 in fusiform and triradiate cells further revealed genes that may specify cell identity. These results suggest a role for PRC2 and its associated mark in cell differentiation in unicellular species, and highlight their ancestral function in a broader evolutionary context than currently is appreciated.
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http://dx.doi.org/10.1111/nph.17129DOI Listing
March 2021

Phylogenomic fingerprinting of tempo and functions of horizontal gene transfer within ochrophytes.

Proc Natl Acad Sci U S A 2021 Jan;118(4)

Aix Marseille University, Universite de Toulon, CNRS, Institut de Recherche pour le Développement (IRD), Mediterranean Institute of Oceanography (MIO) UM 110, 13288 Marseille, France;

Horizontal gene transfer (HGT) is an important source of novelty in eukaryotic genomes. This is particularly true for the ochrophytes, a diverse and important group of algae. Previous studies have shown that ochrophytes possess a mosaic of genes derived from bacteria and eukaryotic algae, acquired through chloroplast endosymbiosis and from HGTs, although understanding of the time points and mechanisms underpinning these transfers has been restricted by the depth of taxonomic sampling possible. We harness an expanded set of ochrophyte sequence libraries, alongside automated and manual phylogenetic annotation, in silico modeling, and experimental techniques, to assess the frequency and functions of HGT across this lineage. Through manual annotation of thousands of single-gene trees, we identify continuous bacterial HGT as the predominant source of recently arrived genes in the model diatom Using a large-scale automated dataset, a multigene ochrophyte reference tree, and mathematical reconciliation of gene trees, we note a probable elevation of bacterial HGTs at foundational points in diatom evolution, following their divergence from other ochrophytes. Finally, we demonstrate that throughout ochrophyte evolutionary history, bacterial HGTs have been enriched in genes encoding secreted proteins. Our study provides insights into the sources and frequency of HGTs, and functional contributions that HGT has made to algal evolution.
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http://dx.doi.org/10.1073/pnas.2009974118DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7848541PMC
January 2021

PhaeoNet: A Holistic RNAseq-Based Portrait of Transcriptional Coordination in the Model Diatom .

Front Plant Sci 2020 16;11:590949. Epub 2020 Oct 16.

Institut de Biologie de l'Ecole Normale Supérieure (IBENS), Ecole Normale Supérieure, CNRS, INSERM, Université PSL, Paris, France.

Transcriptional coordination is a fundamental component of prokaryotic and eukaryotic cell biology, underpinning the cell cycle, physiological transitions, and facilitating holistic responses to environmental stress, but its overall dynamics in eukaryotic algae remain poorly understood. Better understanding of transcriptional partitioning may provide key insights into the primary metabolism pathways of eukaryotic algae, which frequently depend on intricate metabolic associations between the chloroplasts and mitochondria that are not found in plants. Here, we exploit 187 publically available RNAseq datasets generated under varying nitrogen, iron and phosphate growth conditions to understand the co-regulatory principles underpinning transcription in the model diatom . Using WGCNA (Weighted Gene Correlation Network Analysis), we identify 28 merged modules of co-expressed genes in the genome, which show high connectivity and correlate well with previous microarray-based surveys of gene co-regulation in this species. We use combined functional, subcellular localization and evolutionary annotations to reveal the fundamental principles underpinning the transcriptional co-regulation of genes implicated in chloroplast and mitochondrial metabolism, as well as the functions of diverse transcription factors underpinning this co-regulation. The resource is publically available as PhaeoNet, an advanced tool to understand diatom gene co-regulation.
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http://dx.doi.org/10.3389/fpls.2020.590949DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7596299PMC
October 2020

Biogeography of marine giant viruses reveals their interplay with eukaryotes and ecological functions.

Nat Ecol Evol 2020 12 7;4(12):1639-1649. Epub 2020 Sep 7.

Bioinformatics Center, Institute for Chemical Research, Kyoto University, Uji, Japan.

Nucleocytoplasmic large DNA viruses (NCLDVs) are ubiquitous in marine environments and infect diverse eukaryotes. However, little is known about their biogeography and ecology in the ocean. By leveraging the Tara Oceans pole-to-pole metagenomic data set, we investigated the distribution of NCLDVs across size fractions, depths and biomes, as well as their associations with eukaryotic communities. Our analyses reveal a heterogeneous distribution of NCLDVs across oceans, and a higher proportion of unique NCLDVs in the polar biomes. The community structures of NCLDV families correlate with specific eukaryotic lineages, including many photosynthetic groups. NCLDV communities are generally distinct between surface and mesopelagic zones, but at some locations they exhibit a high similarity between the two depths. This vertical similarity correlates to surface phytoplankton biomass but not to physical mixing processes, which suggests a potential role of vertical transport in structuring mesopelagic NCLDV communities. These results underscore the importance of the interactions between NCLDVs and eukaryotes in biogeochemical processes in the ocean.
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http://dx.doi.org/10.1038/s41559-020-01288-wDOI Listing
December 2020

Global identification of a marine diatom long noncoding natural antisense transcripts (NATs) and their response to phosphate fluctuations.

Sci Rep 2020 08 24;10(1):14110. Epub 2020 Aug 24.

Institut de Biologie de L'Ecole normale supérieure (IBENS), Ecole normale supérieure, CNRS, INSERM, Université PSL, 75005, Paris, France.

Often ignored and regarded as mere transcriptional noise, long noncoding RNAs (lncRNAs) are starting to be considered key regulators of gene expression across the Eukarya domain of life. In the model diatom Phaeodactylum tricornutum, we have previously reported the occurrence of 1,510 intergenic lncRNAs (lincRNAs), many of which displaying specific patterns of expression under phosphate fluctuation (Pi). Using strand-specific RNA-sequencing data we now expand the repertoire of P. tricornutum lncRNAs by identifying 2,628 novel natural antisense transcripts (NATs) that cover 21.5% of the annotated genomic loci. We found that NAT expression is tightly regulated by phosphate depletion and other naturally occurring environmental stresses. Furthermore, we identified 121 phosphate stress responsive NAT-mRNA pairs, the great majority of which showing a positive correlation (concordant pairs) and a small fraction with negative correlation (discordant pairs). Taken together our results show that NATs are highly abundant transcripts in P. tricornutum and that their expression is under tight regulation by nutrient and environmental stresses. Furthermore, our results suggest that in P. tricornutum Pi stress response NAT pairs predominantly regulate positively the expression of their cognate sense genes, the latter being involved in several biological processes underlying the control of cellular homeostasis under stress.
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http://dx.doi.org/10.1038/s41598-020-71002-0DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7445176PMC
August 2020

Genome-enabled phylogenetic and functional reconstruction of an araphid pennate diatom Plagiostriata sp. CCMP470, previously assigned as a radial centric diatom, and its bacterial commensal.

Sci Rep 2020 06 10;10(1):9449. Epub 2020 Jun 10.

Stazione Zoologica Anton Dohrn, Villa Comunale, 80121, Napoli, Italy.

Diatoms are an ecologically fundamental and highly diverse group of algae, dominating marine primary production in both open-water and coastal communities. The diatoms include both centric species, which may have radial or polar symmetry, and the pennates, which include raphid and araphid species and arose within the centric lineage. Here, we use combined microscopic and molecular information to reclassify a diatom strain CCMP470, previously annotated as a radial centric species related to Leptocylindrus danicus, as an araphid pennate species in the staurosiroid lineage, within the genus Plagiostriata. CCMP470 shares key ultrastructural features with Plagiostriata taxa, such as the presence of a sternum with parallel striae, and the presence of a highly reduced labiate process on its valve; and this evolutionary position is robustly supported by multigene phylogenetic analysis. We additionally present a draft genome of CCMP470, which is the first genome available for a staurosiroid lineage. 270 Pfams (19%) found in the CCMP470 genome are not known in other diatom genomes, which otherwise does not hold big novelties compared to genomes of non-staurosiroid diatoms. Notably, our DNA library contains the genome of a bacterium within the Rhodobacterales, an alpha-proteobacterial lineage known frequently to associate with algae. We demonstrate the presence of commensal alpha-proteobacterial sequences in other published algal genome and transcriptome datasets, which may indicate widespread and persistent co-occurrence.
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http://dx.doi.org/10.1038/s41598-020-65941-xDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7287063PMC
June 2020

Tara Oceans: towards global ocean ecosystems biology.

Nat Rev Microbiol 2020 08 12;18(8):428-445. Epub 2020 May 12.

Research Federation for the Study of Global Ocean Systems Ecology and Evolution, FR2022/Tara GOSEE, Paris, France.

A planetary-scale understanding of the ocean ecosystem, particularly in light of climate change, is crucial. Here, we review the work of Tara Oceans, an international, multidisciplinary project to assess the complexity of ocean life across comprehensive taxonomic and spatial scales. Using a modified sailing boat, the team sampled plankton at 210 globally distributed sites at depths down to 1,000 m. We describe publicly available resources of molecular, morphological and environmental data, and discuss how an ecosystems biology approach has expanded our understanding of plankton diversity and ecology in the ocean as a planetary, interconnected ecosystem. These efforts illustrate how global-scale concepts and data can help to integrate biological complexity into models and serve as a baseline for assessing ecosystem changes and the future habitability of our planet in the Anthropocene epoch.
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http://dx.doi.org/10.1038/s41579-020-0364-5DOI Listing
August 2020

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

Authors:
Drahomíra Faktorová R Ellen R Nisbet José A Fernández Robledo Elena Casacuberta Lisa Sudek Andrew E Allen Manuel Ares Cristina Aresté Cecilia Balestreri Adrian C Barbrook Patrick Beardslee Sara Bender David S Booth François-Yves Bouget Chris Bowler Susana A Breglia Colin Brownlee Gertraud Burger Heriberto Cerutti Rachele Cesaroni Miguel A Chiurillo Thomas Clemente Duncan B Coles Jackie L Collier Elizabeth C Cooney Kathryn Coyne Roberto Docampo Christopher L Dupont Virginia Edgcomb Elin Einarsson Pía A Elustondo Fernan Federici Veronica Freire-Beneitez Nastasia J Freyria Kodai Fukuda Paulo A García Peter R Girguis Fatma Gomaa Sebastian G Gornik Jian Guo Vladimír Hampl Yutaka Hanawa Esteban R Haro-Contreras Elisabeth Hehenberger Andrea Highfield Yoshihisa Hirakawa Amanda Hopes Christopher J Howe Ian Hu Jorge Ibañez Nicholas A T Irwin Yuu Ishii Natalia Ewa Janowicz Adam C Jones Ambar Kachale Konomi Fujimura-Kamada Binnypreet Kaur Jonathan Z Kaye Eleanna Kazana Patrick J Keeling Nicole King Lawrence A Klobutcher Noelia Lander Imen Lassadi Zhuhong Li Senjie Lin Jean-Claude Lozano Fulei Luan Shinichiro Maruyama Tamara Matute Cristina Miceli Jun Minagawa Mark Moosburner Sebastián R Najle Deepak Nanjappa Isabel C Nimmo Luke Noble Anna M G Novák Vanclová Mariusz Nowacki Isaac Nuñez Arnab Pain Angela Piersanti Sandra Pucciarelli Jan Pyrih Joshua S Rest Mariana Rius Deborah Robertson Albane Ruaud Iñaki Ruiz-Trillo Monika A Sigg Pamela A Silver Claudio H Slamovits G Jason Smith Brittany N Sprecher Rowena Stern Estienne C Swart Anastasios D Tsaousis Lev Tsypin Aaron Turkewitz Jernej Turnšek Matus Valach Valérie Vergé Peter von Dassow Tobias von der Haar Ross F Waller Lu Wang Xiaoxue Wen Glen Wheeler April Woods Huan Zhang Thomas Mock Alexandra Z Worden Julius Lukeš

Nat Methods 2020 05;17(5):551

Institute of Parasitology, Biology Centre, Czech Academy of Sciences and Faculty of Sciences, University of South Bohemia, České Budějovice, Czech Republic.

An amendment to this paper has been published and can be accessed via a link at the top of the paper.
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http://dx.doi.org/10.1038/s41592-020-0828-6DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7200595PMC
May 2020

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

Authors:
Drahomíra Faktorová R Ellen R Nisbet José A Fernández Robledo Elena Casacuberta Lisa Sudek Andrew E Allen Manuel Ares Cristina Aresté Cecilia Balestreri Adrian C Barbrook Patrick Beardslee Sara Bender David S Booth François-Yves Bouget Chris Bowler Susana A Breglia Colin Brownlee Gertraud Burger Heriberto Cerutti Rachele Cesaroni Miguel A Chiurillo Thomas Clemente Duncan B Coles Jackie L Collier Elizabeth C Cooney Kathryn Coyne Roberto Docampo Christopher L Dupont Virginia Edgcomb Elin Einarsson Pía A Elustondo Fernan Federici Veronica Freire-Beneitez Nastasia J Freyria Kodai Fukuda Paulo A García Peter R Girguis Fatma Gomaa Sebastian G Gornik Jian Guo Vladimír Hampl Yutaka Hanawa Esteban R Haro-Contreras Elisabeth Hehenberger Andrea Highfield Yoshihisa Hirakawa Amanda Hopes Christopher J Howe Ian Hu Jorge Ibañez Nicholas A T Irwin Yuu Ishii Natalia Ewa Janowicz Adam C Jones Ambar Kachale Konomi Fujimura-Kamada Binnypreet Kaur Jonathan Z Kaye Eleanna Kazana Patrick J Keeling Nicole King Lawrence A Klobutcher Noelia Lander Imen Lassadi Zhuhong Li Senjie Lin Jean-Claude Lozano Fulei Luan Shinichiro Maruyama Tamara Matute Cristina Miceli Jun Minagawa Mark Moosburner Sebastián R Najle Deepak Nanjappa Isabel C Nimmo Luke Noble Anna M G Novák Vanclová Mariusz Nowacki Isaac Nuñez Arnab Pain Angela Piersanti Sandra Pucciarelli Jan Pyrih Joshua S Rest Mariana Rius Deborah Robertson Albane Ruaud Iñaki Ruiz-Trillo Monika A Sigg Pamela A Silver Claudio H Slamovits G Jason Smith Brittany N Sprecher Rowena Stern Estienne C Swart Anastasios D Tsaousis Lev Tsypin Aaron Turkewitz Jernej Turnšek Matus Valach Valérie Vergé Peter von Dassow Tobias von der Haar Ross F Waller Lu Wang Xiaoxue Wen Glen Wheeler April Woods Huan Zhang Thomas Mock Alexandra Z Worden Julius Lukeš

Nat Methods 2020 05 6;17(5):481-494. Epub 2020 Apr 6.

Institute of Parasitology, Biology Centre, Czech Academy of Sciences and Faculty of Sciences, University of South Bohemia, České Budějovice, Czech Republic.

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.
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http://dx.doi.org/10.1038/s41592-020-0796-xDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7200600PMC
May 2020

Diatoms Are Selective Segregators in Global Ocean Planktonic Communities.

mSystems 2020 Jan 21;5(1). Epub 2020 Jan 21.

lnstitut de Biologie de l'ENS, Département de Biologie, École Normale Supérieure, CNRS, INSERM, Université PSL, Paris, France

Diatoms are a major component of phytoplankton, believed to be responsible for around 20% of the annual primary production on Earth. As abundant and ubiquitous organisms, they are known to establish biotic interactions with many other members of plankton. Through analyses of cooccurrence networks derived from the Oceans expedition that take into account both biotic and abiotic factors in shaping the spatial distributions of species, we show that only 13% of diatom pairwise associations are driven by environmental conditions; the vast majority are independent of abiotic factors. In contrast to most other plankton groups, on a global scale, diatoms display a much higher proportion of negative correlations with other organisms, particularly toward potential predators and parasites, suggesting that their biogeography is constrained by top-down pressure. Genus-level analyses indicate that abundant diatoms are not necessarily the most connected and that species-specific abundance distribution patterns lead to negative associations with other organisms. In order to move forward in the biological interpretation of cooccurrence networks, an open-access extensive literature survey of diatom biotic interactions was compiled, of which 18.5% were recovered in the computed network. This result reveals the extent of what likely remains to be discovered in the field of planktonic biotic interactions, even for one of the best-known organismal groups. Diatoms are key phytoplankton in the modern ocean that are involved in numerous biotic interactions, ranging from symbiosis to predation and viral infection, which have considerable effects on global biogeochemical cycles. However, despite recent large-scale studies of plankton, we are still lacking a comprehensive picture of the diversity of diatom biotic interactions in the marine microbial community. Through the ecological interpretation of both inferred microbial association networks and available knowledge on diatom interactions compiled in an open-access database, we propose an ecosystems approach for exploring diatom interactions in the ocean.
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http://dx.doi.org/10.1128/mSystems.00444-19DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6977069PMC
January 2020

Phytoplankton in the Ocean.

Ann Rev Mar Sci 2020 01;12:233-265

Institut de Biologie de l'École Normale Supérieure (IBENS), Département de Biologie, École Normale Supérieure, CNRS, INSERM, Université de Recherche Paris Sciences et Lettres (Université PSL), 75005 Paris, France; email:

Photosynthesis evolved in the ocean more than 2 billion years ago and is now performed by a wide range of evolutionarily distinct organisms, including both prokaryotes and eukaryotes. Our appreciation of their abundance, distributions, and contributions to primary production in the ocean has been increasing since they were first discovered in the seventeenth century and has now been enhanced by data emerging from the Oceans project, which performed a comprehensive worldwide sampling of plankton in the upper layers of the ocean between 2009 and 2013. Largely using recent data from Oceans, here we review the geographic distributions of phytoplankton in the global ocean and their diversity, abundance, and standing stock biomass. We also discuss how omics-based information can be incorporated into studies of photosynthesis in the ocean and show the likely importance of mixotrophs and photosymbionts.
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http://dx.doi.org/10.1146/annurev-marine-010419-010706DOI Listing
January 2020

Intraspecific Diversity in the Cold Stress Response of Transposable Elements in the Diatom .

Genes (Basel) 2019 12 20;11(1). Epub 2019 Dec 20.

Stazione Zoologica Anton Dohrn, Villa Comunale, 80121 Napoli, Italy.

Transposable elements (TEs), activated as a response to unfavorable conditions, have been proposed to contribute to the generation of genetic and phenotypic diversity in diatoms. Here we explore the transcriptome of three warm water strains of the diatom , and the possible involvement of TEs in their response to changing temperature conditions. At low temperature (13 °C) several stress response proteins were overexpressed, confirming low temperature to be unfavorable for , while TE-related transcripts of the LTR retrotransposon superfamily were the most enriched transcripts. Their expression levels, as well as most of the stress-related proteins, were found to vary significantly among strains, and even within the same strains analysed at different times. The lack of overexpression after many months of culturing suggests a possible role of physiological plasticity in response to growth under controlled laboratory conditions. While further investigation on the possible central role of TEs in the diatom stress response is warranted, the strain-specific responses and possible role of in-culture evolution draw attention to the interplay between the high intraspecific variability and the physiological plasticity of diatoms, which can both contribute to the adaptation of a species to a wide range of conditions in the marine environment.
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http://dx.doi.org/10.3390/genes11010009DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7017206PMC
December 2019

Global Trends in Marine Plankton Diversity across Kingdoms of Life.

Cell 2019 11;179(5):1084-1097.e21

Institut de Biologie de l'École Normale Supérieure (IBENS), École Normale Supérieure, CNRS, INSERM, PSL Université Paris, 75005 Paris, France. Electronic address:

The ocean is home to myriad small planktonic organisms that underpin the functioning of marine ecosystems. However, their spatial patterns of diversity and the underlying drivers remain poorly known, precluding projections of their responses to global changes. Here we investigate the latitudinal gradients and global predictors of plankton diversity across archaea, bacteria, eukaryotes, and major virus clades using both molecular and imaging data from Tara Oceans. We show a decline of diversity for most planktonic groups toward the poles, mainly driven by decreasing ocean temperatures. Projections into the future suggest that severe warming of the surface ocean by the end of the 21 century could lead to tropicalization of the diversity of most planktonic groups in temperate and polar regions. These changes may have multiple consequences for marine ecosystem functioning and services and are expected to be particularly significant in key areas for carbon sequestration, fisheries, and marine conservation. VIDEO ABSTRACT.
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http://dx.doi.org/10.1016/j.cell.2019.10.008DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6912166PMC
November 2019

Gene Expression Changes and Community Turnover Differentially Shape the Global Ocean Metatranscriptome.

Cell 2019 Nov;179(5):1068-1083.e21

Department of Biology, Institute of Microbiology and Swiss Institute of Bioinformatics, ETH Zürich, Zürich 8093, Switzerland. Electronic address:

Ocean microbial communities strongly influence the biogeochemistry, food webs, and climate of our planet. Despite recent advances in understanding their taxonomic and genomic compositions, little is known about how their transcriptomes vary globally. Here, we present a dataset of 187 metatranscriptomes and 370 metagenomes from 126 globally distributed sampling stations and establish a resource of 47 million genes to study community-level transcriptomes across depth layers from pole-to-pole. We examine gene expression changes and community turnover as the underlying mechanisms shaping community transcriptomes along these axes of environmental variation and show how their individual contributions differ for multiple biogeochemically relevant processes. Furthermore, we find the relative contribution of gene expression changes to be significantly lower in polar than in non-polar waters and hypothesize that in polar regions, alterations in community activity in response to ocean warming will be driven more strongly by changes in organismal composition than by gene regulatory mechanisms. VIDEO ABSTRACT.
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http://dx.doi.org/10.1016/j.cell.2019.10.014DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6912165PMC
November 2019

Access to RNA-sequencing data from 1,173 plant species: The 1000 Plant transcriptomes initiative (1KP).

Gigascience 2019 10;8(10)

Department of Biological Sciences, University of Alberta, Edmonton, AB T6G 2E9, Canada.

Background: The 1000 Plant transcriptomes initiative (1KP) explored genetic diversity by sequencing RNA from 1,342 samples representing 1,173 species of green plants (Viridiplantae).

Findings: This data release accompanies the initiative's final/capstone publication on a set of 3 analyses inferring species trees, whole genome duplications, and gene family expansions. These and previous analyses are based on de novo transcriptome assemblies and related gene predictions. Here, we assess their data and assembly qualities and explain how we detected potential contaminations.

Conclusions: These data will be useful to plant and/or evolutionary scientists with interests in particular gene families, either across the green plant tree of life or in more focused lineages.
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http://dx.doi.org/10.1093/gigascience/giz126DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6808545PMC
October 2019

A genomics approach reveals the global genetic polymorphism, structure, and functional diversity of ten accessions of the marine model diatom Phaeodactylum tricornutum.

ISME J 2020 02 17;14(2):347-363. Epub 2019 Oct 17.

Institut de biologie de l'Ecole normale supérieure (IBENS), Ecole normale supérieure, CNRS, INSERM, PSL Université Paris, 75005, Paris, France.

Diatoms emerged in the Mesozoic period and presently constitute one of the main primary producers in the world's ocean and are of a major economic importance. In the current study, using whole genome sequencing of ten accessions of the model diatom Phaeodactylum tricornutum, sampled at broad geospatial and temporal scales, we draw a comprehensive landscape of the genomic diversity within the species. We describe strong genetic subdivisions of the accessions into four genetic clades (A-D) with constituent populations of each clade possessing a conserved genetic and functional makeup, likely a consequence of the limited dispersal of P. tricornutum in the open ocean. We further suggest dominance of asexual reproduction across all the populations, as implied by high linkage disequilibrium. Finally, we show limited yet compelling signatures of genetic and functional convergence inducing changes in the selection pressure on many genes and metabolic pathways. We propose these findings to have significant implications for understanding the genetic structure of diatom populations in nature and provide a framework to assess the genomic underpinnings of their ecological success and impact on aquatic ecosystems where they play a major role. Our work provides valuable resources for functional genomics and for exploiting the biotechnological potential of this model diatom species.
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http://dx.doi.org/10.1038/s41396-019-0528-3DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6976637PMC
February 2020

The Tara Pacific expedition-A pan-ecosystemic approach of the "-omics" complexity of coral reef holobionts across the Pacific Ocean.

PLoS Biol 2019 09 23;17(9):e3000483. Epub 2019 Sep 23.

Centre Scientifique de Monaco, Monte Carlo, Principality of Monaco.

Coral reefs are the most diverse habitats in the marine realm. Their productivity, structural complexity, and biodiversity critically depend on ecosystem services provided by corals that are threatened because of climate change effects-in particular, ocean warming and acidification. The coral holobiont is composed of the coral animal host, endosymbiotic dinoflagellates, associated viruses, bacteria, and other microeukaryotes. In particular, the mandatory photosymbiosis with microalgae of the family Symbiodiniaceae and its consequences on the evolution, physiology, and stress resilience of the coral holobiont have yet to be fully elucidated. The functioning of the holobiont as a whole is largely unknown, although bacteria and viruses are presumed to play roles in metabolic interactions, immunity, and stress tolerance. In the context of climate change and anthropogenic threats on coral reef ecosystems, the Tara Pacific project aims to provide a baseline of the "-omics" complexity of the coral holobiont and its ecosystem across the Pacific Ocean and for various oceanographically distinct defined areas. Inspired by the previous Tara Oceans expeditions, the Tara Pacific expedition (2016-2018) has applied a pan-ecosystemic approach on coral reefs throughout the Pacific Ocean, drawing an east-west transect from Panama to Papua New Guinea and a south-north transect from Australia to Japan, sampling corals throughout 32 island systems with local replicates. Tara Pacific has developed and applied state-of-the-art technologies in very-high-throughput genetic sequencing and molecular analysis to reveal the entire microbial and chemical diversity as well as functional traits associated with coral holobionts, together with various measures on environmental forcing. This ambitious project aims at revealing a massive amount of novel biodiversity, shedding light on the complex links between genomes, transcriptomes, metabolomes, organisms, and ecosystem functions in coral reefs and providing a reference of the biological state of modern coral reefs in the Anthropocene.
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http://dx.doi.org/10.1371/journal.pbio.3000483DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6776362PMC
September 2019

Metabolic Innovations Underpinning the Origin and Diversification of the Diatom Chloroplast.

Biomolecules 2019 07 30;9(8). Epub 2019 Jul 30.

Institut de Biologie de l'ENS (IBENS), Département de biologie, École normale supérieure, CNRS, INSERM, Université PSL, 75005 Paris, France.

Of all the eukaryotic algal groups, diatoms make the most substantial contributions to photosynthesis in the contemporary ocean. Understanding the biological innovations that have occurred in the diatom chloroplast may provide us with explanations to the ecological success of this lineage and clues as to how best to exploit the biology of these organisms for biotechnology. In this paper, we use multi-species transcriptome datasets to compare chloroplast metabolism pathways in diatoms to other algal lineages. We identify possible diatom-specific innovations in chloroplast metabolism, including the completion of tocopherol synthesis via a chloroplast-targeted tocopherol cyclase, a complete chloroplast ornithine cycle, and chloroplast-targeted proteins involved in iron acquisition and CO concentration not shared between diatoms and their closest relatives in the stramenopiles. We additionally present a detailed investigation of the chloroplast metabolism of the oil-producing diatom , which is of industrial interest for biofuel production. These include modified amino acid and pyruvate hub metabolism that might enhance acetyl-coA production for chloroplast lipid biosynthesis and the presence of a chloroplast-localised squalene synthesis pathway unknown in other diatoms. Our data provides valuable insights into the biological adaptations underpinning an ecologically critical lineage, and how chloroplast metabolism can change even at a species level in extant algae.
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http://dx.doi.org/10.3390/biom9080322DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6723447PMC
July 2019

Phaeodactylum tricornutum.

Trends Genet 2019 09 15;35(9):706-707. Epub 2019 Jul 15.

Institut de Biologie Physico-Chimique, Laboratoire du Biologie du Chloroplaste et Perception de la Lumière chez les Microalgues, UMR7141 CNRS, Sorbonne Université, Paris, France.

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http://dx.doi.org/10.1016/j.tig.2019.05.007DOI Listing
September 2019

Meta-omics reveals genetic flexibility of diatom nitrogen transporters in response to environmental changes.

Mol Biol Evol 2019 Jul 1. Epub 2019 Jul 1.

Stazione Zoologica Anton Dohrn, Villa Comunale, Naples, Italy.

Diatoms (Bacillariophyta), one of the most abundant and diverse groups of marine phytoplankton, respond rapidly to the supply of new nutrients, often out-competing other phytoplankton. Herein, we integrated analyses of the evolution, distribution and expression modulation of two gene families involved in diatom nitrogen uptake (DiAMT1 and DiNRT2), in order to infer the main drivers of divergence in a key functional trait of phytoplankton. Our results suggest that major steps in the evolution of the two gene families reflected key events triggering diatom radiation and diversification. Their expression is modulated in the contemporary ocean by seawater temperature, nitrate and iron concentrations. Moreover, the differences in diversity and expression of these gene families throughout the water column hint at a possible link with bacterial activity. This study represents a proof-of-concept of how a holistic approach may shed light on the functional biology of organisms in their natural environment.
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http://dx.doi.org/10.1093/molbev/msz157DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6805229PMC
July 2019

Arabidopsis S2Lb links AtCOMPASS-like and SDG2 activity in H3K4me3 independently from histone H2B monoubiquitination.

Genome Biol 2019 05 21;20(1):100. Epub 2019 May 21.

Institut de Biologie de l'Ecole Normale Supérieure (IBENS), Ecole Normale Supérieure, CNRS, INSERM, PSL University, 75005, Paris, France.

Background: The functional determinants of H3K4me3, their potential dependency on histone H2B monoubiquitination, and their contribution to defining transcriptional regimes are poorly defined in plant systems. Unlike in Saccharomyces cerevisiae, where a single SET1 protein catalyzes H3K4me3 as part of COMPlex of proteins ASsociated with Set1 (COMPASS), in Arabidopsis thaliana, this activity involves multiple histone methyltransferases. Among these, the plant-specific SET DOMAIN GROUP 2 (SDG2) has a prominent role.

Results: We report that SDG2 co-regulates hundreds of genes with SWD2-like b (S2Lb), a plant ortholog of the Swd2 axillary subunit of yeast COMPASS. We show that S2Lb co-purifies with the AtCOMPASS core subunit WDR5, and both S2Lb and SDG2 directly influence H3K4me3 enrichment over highly transcribed genes. S2Lb knockout triggers pleiotropic developmental phenotypes at the vegetative and reproductive stages, including reduced fertility and seed dormancy. However, s2lb seedlings display little transcriptomic defects as compared to the large repertoire of genes targeted by S2Lb, SDG2, or H3K4me3, suggesting that H3K4me3 enrichment is important for optimal gene induction during cellular transitions rather than for determining on/off transcriptional status. Moreover, unlike in budding yeast, most of the S2Lb and H3K4me3 genomic distribution does not rely on a trans-histone crosstalk with histone H2B monoubiquitination.

Conclusions: Collectively, this study unveils that the evolutionarily conserved COMPASS-like complex has been co-opted by the plant-specific SDG2 histone methyltransferase and mediates H3K4me3 deposition through an H2B monoubiquitination-independent pathway in Arabidopsis.
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http://dx.doi.org/10.1186/s13059-019-1705-4DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6528313PMC
May 2019

Marine DNA Viral Macro- and Microdiversity from Pole to Pole.

Cell 2019 05 25;177(5):1109-1123.e14. Epub 2019 Apr 25.

Department of Microbiology, The Ohio State University, Columbus, OH 43210, USA; Department of Civil, Environmental and Geodetic Engineering, The Ohio State University, Columbus, OH 43210, USA. Electronic address:

Microbes drive most ecosystems and are modulated by viruses that impact their lifespan, gene flow, and metabolic outputs. However, ecosystem-level impacts of viral community diversity remain difficult to assess due to classification issues and few reference genomes. Here, we establish an ∼12-fold expanded global ocean DNA virome dataset of 195,728 viral populations, now including the Arctic Ocean, and validate that these populations form discrete genotypic clusters. Meta-community analyses revealed five ecological zones throughout the global ocean, including two distinct Arctic regions. Across the zones, local and global patterns and drivers in viral community diversity were established for both macrodiversity (inter-population diversity) and microdiversity (intra-population genetic variation). These patterns sometimes, but not always, paralleled those from macro-organisms and revealed temperate and tropical surface waters and the Arctic as biodiversity hotspots and mechanistic hypotheses to explain them. Such further understanding of ocean viruses is critical for broader inclusion in ecosystem models.
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http://dx.doi.org/10.1016/j.cell.2019.03.040DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6525058PMC
May 2019

Principles of plastid reductive evolution illuminated by nonphotosynthetic chrysophytes.

Proc Natl Acad Sci U S A 2019 04 14;116(14):6914-6923. Epub 2019 Mar 14.

Graduate School of Human and Environmental Studies, Kyoto University, Kyoto 606-8501, Japan;

The division of life into producers and consumers is blurred by evolution. For example, eukaryotic phototrophs can lose the capacity to photosynthesize, although they may retain vestigial plastids that perform other essential cellular functions. Chrysophyte algae have undergone a particularly large number of photosynthesis losses. Here, we present a plastid genome sequence from a nonphotosynthetic chrysophyte, "" sp. NIES-1846, and show that it has retained a nearly identical set of plastid-encoded functions as apicomplexan parasites. Our transcriptomic analysis of 12 different photosynthetic and nonphotosynthetic chrysophyte lineages reveals remarkable convergence in the functions of these nonphotosynthetic plastids, along with informative lineage-specific retentions and losses. At one extreme, retains many photosynthesis-associated proteins, although it appears to have lost the reductive pentose phosphate pathway and most plastid amino acid metabolism pathways. At the other extreme, lacks plastid-targeted proteins associated with gene expression and all metabolic pathways that require plastid-encoded partners, indicating a complete loss of plastid DNA in this genus. Intriguingly, some of the nucleus-encoded proteins that once functioned in the expression of the plastid genome have been retained. These proteins were likely to have been dual targeted to the plastid and mitochondria of the chrysophyte ancestor, and are uniquely targeted to the mitochondria in Our comparative analyses provide insights into the process of functional reduction in nonphotosynthetic plastids.
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http://dx.doi.org/10.1073/pnas.1819976116DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6452693PMC
April 2019

Corrigendum: A Potential Role for Epigenetic Processes in the Acclimation Response to Elevated CO in the Model Diatom .

Front Microbiol 2019 8;10:158. Epub 2019 Feb 8.

State Key Laboratory of Marine Environmental Science, College of Ocean and Earth Sciences, Xiamen University, Xiamen, China.

[This corrects the article DOI: 10.3389/fmicb.2018.03342.].
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http://dx.doi.org/10.3389/fmicb.2019.00158DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6376209PMC
February 2019

A Potential Role for Epigenetic Processes in the Acclimation Response to Elevated CO in the Model Diatom .

Front Microbiol 2018 14;9:3342. Epub 2019 Jan 14.

State Key Laboratory of Marine Environmental Science,College of Ocean and Earth Sciences, Xiamen University, Xiamen, China.

Understanding of the molecular responses underpinning diatom responses to ocean acidification is fundamental for predicting how important primary producers will be shaped by the continuous rise in atmospheric CO. In this study, we have analyzed global transcriptomic changes of the model diatom following growth for 15 generations in elevated CO by strand-specific RNA sequencing (ssRNA-seq). Our results indicate that no significant effects of elevated CO and associated carbonate chemistry changes on the physiological performance of the cells were observed after 15 generations whereas the expression of genes encoding histones and other genes involved in chromatin structure were significantly down-regulated, while the expression of transposable elements (TEs) and genes encoding histone acetylation enzymes were significantly up-regulated. Furthermore, we identified a series of long non-protein coding RNAs (lncRNAs) specifically responsive to elevated CO, suggesting putative regulatory roles for these largely uncharacterized genome components. Taken together, our integrative analyses reveal that epigenetic elements such as TEs, histone modifications and lncRNAs may have important roles in the acclimation of diatoms to elevated CO over short time scales and thus may influence longer term adaptive processes in response to progressive ocean acidification.
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http://dx.doi.org/10.3389/fmicb.2018.03342DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6340190PMC
January 2019

Author Correction: Clade-specific diversification dynamics of marine diatoms since the Jurassic.

Nat Ecol Evol 2018 12;2(12):1993

Institut de Biologie de l'Ecole Normale Supérieure (IBENS), CNRS, INSERM, Université PSL, Paris, France.

In the version of this Article originally published, the authors did not give credit to David G. Mann for the four microscopic images used in Fig. 1a. This has now been amended in all versions of the Article.
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http://dx.doi.org/10.1038/s41559-018-0740-yDOI Listing
December 2018