Project

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Molecular evolution and ecology of Foraminifera and related protists

Applicant Pawlowski Jan Wojciech
Number 140766
Funding scheme Project funding (Div. I-III)
Research institution Département de Génétique et Evolution Faculté des Sciences Université de Genève
Institution of higher education University of Geneva - GE
Main discipline Zoology
Start/End 01.04.2012 - 31.03.2015
Approved amount 702'000.00
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All Disciplines (2)

Discipline
Zoology
Genetics

Keywords (10)

Eukaryotes; Fossil DNA; Phylogeny; DNA Barcoding; Foraminifera; Diversity; Evolution; Next Generation Sequencing; Protists; Systematics

Lay Summary (English)

Lead
Lay summary

Molecular evolution and ecology of Foraminifera and related protists

Foraminifera are a diverse group of single-cell eukaryotes particularly abundant in some marine ecosystems but present also in soil and freshwater habitats. Marine foraminifera have capacity to develop complex multi-chambered skeletons that are preserved in the sediments and formed a particularly rich fossil record. Until now, our knowledge of Foraminifera was based almost exclusively on study of foraminiferal tests (shells).

In our project we are using the modern tools of genetics and genomics to investigate the evolution and diversity of Foraminifera. In particular, we are taking advantage of the development of next-generation sequencing (NGS) technologies to gain insight into molecular processes involved in skeleton building and its diversification. We are also applying NGS to uncover the hidden richness of environmental foraminiferal lineages as well as to test the preservation of foraminiferal DNA in ancient sediments.

Our study will contribute to better understanding the process of diversification of foraminifera and other skeleton-bearing protists. It will provide new genetic tools to identify foraminiferal species and to characterize their assemblage. If successful, we will be able to use DNA fragments preserved in marine sediments to reconstruct the community of eukaryotes living in the past oceans.

Direct link to Lay Summary Last update: 21.02.2013

Responsible applicant and co-applicants

Employees

Publications

Publication
Accurate multiplexing and filtering for high-throughput amplicon-sequencing.
Esling Philippe, Lejzerowicz Franck, Pawlowski Jan (2015), Accurate multiplexing and filtering for high-throughput amplicon-sequencing., in Nucleic acids research, 43(5), 2513-24.
Molecular Phylogeny and Morphology of Leannia veloxifera n. gen. et sp. Unveils a New Lineage of Monothalamous Foraminifera.
Apothéloz-Perret-Gentil Laure, Pawlowski Jan (2015), Molecular Phylogeny and Morphology of Leannia veloxifera n. gen. et sp. Unveils a New Lineage of Monothalamous Foraminifera., in The Journal of eukaryotic microbiology, 62(3), 353-61.
Transcriptome analyses to investigate symbiotic relationships between marine protists.
Balzano Sergio, Corre Erwan, Decelle Johan, Sierra Roberto, Wincker Patrick, Da Silva Corinne, Poulain Julie, Pawlowski Jan, Not Fabrice (2015), Transcriptome analyses to investigate symbiotic relationships between marine protists., in Frontiers in microbiology, 6, 98-98.
A plea for DNA barcoding of Foraminifera
Pawlowski Jan, Holzmann Maria (2014), A plea for DNA barcoding of Foraminifera, in Journal Foraminiferal Research, 44(1), 62-67.
Ancient DNA sheds new light on the Svalbard foraminiferal fossil record of the last millennium.
Pawłowska J, Lejzerowicz F, Esling P, Szczuciński W, Zajączkowski M, Pawlowski J (2014), Ancient DNA sheds new light on the Svalbard foraminiferal fossil record of the last millennium., in Geobiology, 12(4), 277-88.
Environmental monitoring through protist next-generation sequencing metabarcoding: assessing the impact of fish farming on benthic foraminifera communities.
Pawlowski Jan, Esling Philippe, Lejzerowicz Franck, Cedhagen Tomas, Wilding Thomas A (2014), Environmental monitoring through protist next-generation sequencing metabarcoding: assessing the impact of fish farming on benthic foraminifera communities., in Molecular ecology resources, 14(6), 1129-40.
Patterns of rare and abundant marine microbial eukaryotes.
Logares Ramiro, Audic Stéphane, Bass David, Bittner Lucie, Boutte Christophe, Christen Richard, Claverie Jean-Michel, Decelle Johan, Dolan John R, Dunthorn Micah, Edvardsen Bente, Gobet Angélique, Kooistra Wiebe H C F, Mahé Frédéric, Not Fabrice, Ogata Hiroyuki, Pawlowski Jan, Pernice Massimo C, Romac Sarah, Shalchian-Tabrizi Kamran, Simon Nathalie, Stoeck Thorsten, Santini Sébastien, Siano Raffaele, Wincker Patrick (2014), Patterns of rare and abundant marine microbial eukaryotes., in Current biology : CB, 24(8), 813-21.
Phylogenetic position and molecular diversity of Carterinida
Pawlowski Jan, Holzmann Maria, Debenay Jean-Pierre (2014), Phylogenetic position and molecular diversity of Carterinida, in Journal Foraminiferal Research, 44(4), 440-450.
The genome of the foraminiferan Reticulomyxa filosa.
Glöckner Gernot, Hülsmann Norbert, Schleicher Michael, Noegel Angelika A, Eichinger Ludwig, Gallinger Christoph, Pawlowski Jan, Sierra Roberto, Euteneuer Ursula, Pillet Loic, Moustafa Ahmed, Platzer Matthias, Groth Marco, Szafranski Karol, Schliwa Manfred (2014), The genome of the foraminiferan Reticulomyxa filosa., in Current biology : CB, 24(1), 11-8.
The Marine Microbial Eukaryote Transcriptome Sequencing Project (MMETSP): illuminating the functional diversity of eukaryotic life in the oceans through transcriptome sequencing.
Keeling Patrick J, Burki Fabien, Wilcox Heather M, Allam Bassem, Allen Eric E, Amaral-Zettler Linda A, Armbrust E Virginia, Archibald John M, Bharti Arvind K, Bell Callum J, Beszteri Bank, Bidle Kay D, Cameron Connor T, Campbell Lisa, Caron David A, Cattolico Rose Ann, Collier Jackie L, Coyne Kathryn, Davy Simon K, Deschamps Phillipe, Dyhrman Sonya T, Edvardsen Bente, Gates Ruth D, Gobler Christopher J, Greenwood Spencer J (2014), The Marine Microbial Eukaryote Transcriptome Sequencing Project (MMETSP): illuminating the functional diversity of eukaryotic life in the oceans through transcriptome sequencing., in PLoS biology, 12(6), 1001889-1001889.
Toxisarcon taimyr sp.nov., (2014) a new large monothalamous foraminifer from the Kara Sea inner shelf.
Voltsky Ivan, Korsun Sergey, Pawlowski Jan (2014), Toxisarcon taimyr sp.nov., (2014) a new large monothalamous foraminifer from the Kara Sea inner shelf., in Marine Biodiversity, 44:213-221, 213-221.
Wide occurrence of SSU rDNA intragenomic polymorphism in foraminifera and its implications for molecular species identification.
Weber Alexandra Anh-Thu, Pawlowski Jan (2014), Wide occurrence of SSU rDNA intragenomic polymorphism in foraminifera and its implications for molecular species identification., in Protist, 165(5), 645-61.
Ancient DNA complements microfossil record in deep-sea subsurface sediments.
Lejzerowicz Franck, Esling Philippe, Majewski Wojciech, Szczuciński Witold, Decelle Johan, Obadia Cyril, Arbizu Pedro Martinez, Pawlowski Jan (2013), Ancient DNA complements microfossil record in deep-sea subsurface sediments., in Biology letters, 9(4), 20130283-20130283.
Arnoldiellina fluorescens gen. et sp. nov.--a new green autofluorescent foraminifer from the Gulf of Eilat (Israel).
Apothéloz-Perret-Gentil Laure, Holzmann Maria, Pawlowski Jan (2013), Arnoldiellina fluorescens gen. et sp. nov.--a new green autofluorescent foraminifer from the Gulf of Eilat (Israel)., in European journal of protistology, 49(2), 210-6.
Can abundance of protists be inferred from sequence data: a case study of foraminifera.
Weber Alexandra A-T, Pawlowski Jan (2013), Can abundance of protists be inferred from sequence data: a case study of foraminifera., in PloS one, 8(2), 56739-56739.
Deep relationships of Rhizaria revealed by phylogenomics: a farewell to Haeckel's Radiolaria.
Sierra Roberto, Matz Mikhail V, Aglyamova Galina, Pillet Loïc, Decelle Johan, Not Fabrice, de Vargas Colomban, Pawlowski Jan (2013), Deep relationships of Rhizaria revealed by phylogenomics: a farewell to Haeckel's Radiolaria., in Molecular phylogenetics and evolution, 67(1), 53-9.
Identifying active foraminifera in the Sea of Japan using metatrascriptomic approach.
Lejzerowicz Franck, Voltsky Ivan, Pawlowski Jan (2013), Identifying active foraminifera in the Sea of Japan using metatrascriptomic approach., in Deep-Sea Research, 86-87, 214-220.
Molecular evidence for Lessepsian invasion of soritids (larger symbiont bearing benthic foraminifera).
Merkado Gily, Holzmann Maria, Apothéloz-Perret-Gentil Laure, Pawlowski Jan, Abdu Uri, Almogi-Labin Ahuva, Hyams-Kaphzan Orit, Bakhrat Anna, Abramovich Sigal (2013), Molecular evidence for Lessepsian invasion of soritids (larger symbiont bearing benthic foraminifera)., in PloS one, 8(10), 77725-77725.
Molecular evidence for β-tubulin neofunctionalization in Retaria (Foraminifera and radiolarians).
Hou Yubo, Sierra Roberto, Bassen David, Banavali Nilesh K, Habura Andrea, Pawlowski Jan, Bowser Samuel S (2013), Molecular evidence for β-tubulin neofunctionalization in Retaria (Foraminifera and radiolarians)., in Molecular biology and evolution, 30(11), 2487-93.
New supraordinal classification of Foraminifera: molecules meet morphology
Pawlowski Jan, Holzmann Maria, Tyszka Jaroslaw (2013), New supraordinal classification of Foraminifera: molecules meet morphology, in Marine Micropaleontology, 100, 1-10.
Phylogenomics of the intracellular parasite Mikrocytos mackini reveals evidence for a mitosome in rhizaria.
Burki Fabien, Corradi Nicolas, Sierra Roberto, Pawlowski Jan, Meyer Gary R, Abbott Cathryn L, Keeling Patrick J (2013), Phylogenomics of the intracellular parasite Mikrocytos mackini reveals evidence for a mitosome in rhizaria., in Current biology : CB, 23(16), 1541-7.
The new micro-kingdoms of eukaryotes.
Pawlowski Jan (2013), The new micro-kingdoms of eukaryotes., in BMC biology, 11, 40-40.
The Protist Ribosomal Reference database (PR2): a catalog of unicellular eukaryote small sub-unit rRNA sequences with curated taxonomy.
Guillou Laure, Bachar Dipankar, Audic Stéphane, Bass David, Berney Cédric, Bittner Lucie, Boutte Christophe, Burgaud Gaétan, de Vargas Colomban, Decelle Johan, Del Campo Javier, Dolan John R, Dunthorn Micah, Edvardsen Bente, Holzmann Maria, Kooistra Wiebe H C F, Lara Enrique, Le Bescot Noan, Logares Ramiro, Mahé Frédéric, Massana Ramon, Montresor Marina, Morard Raphael, Not Fabrice, Pawlowski Jan (2013), The Protist Ribosomal Reference database (PR2): a catalog of unicellular eukaryote small sub-unit rRNA sequences with curated taxonomy., in Nucleic acids research, 41(Database i), 597-604.
Transcriptome analysis of foraminiferan Elphidium margaritaceum questions the role of gene transfer in kleptoplastidy.
Pillet Loïc, Pawlowski Jan (2013), Transcriptome analysis of foraminiferan Elphidium margaritaceum questions the role of gene transfer in kleptoplastidy., in Molecular biology and evolution, 30(1), 66-9.
CBOL protist working group: barcoding eukaryotic richness beyond the animal, plant, and fungal kingdoms.
Pawlowski Jan, Audic Stéphane, Adl Sina, Bass David, Belbahri Lassaâd, Berney Cédric, Bowser Samuel S, Cepicka Ivan, Decelle Johan, Dunthorn Micah, Fiore-Donno Anna Maria, Gile Gillian H, Holzmann Maria, Jahn Regine, Jirků Miloslav, Keeling Patrick J, Kostka Martin, Kudryavtsev Alexander, Lara Enrique, Lukeš Julius, Mann David G, Mitchell Edward A D, Nitsche Frank, Romeralo Maria, Saunders Gary W (2012), CBOL protist working group: barcoding eukaryotic richness beyond the animal, plant, and fungal kingdoms., in PLoS biology, 10(11), 1001419-1001419.
Intra-genomic ribosomal RNA polymorphism and morphological variation in Elphidium macellum suggests inter-specific hybridization in foraminifera.
Pillet Loïc, Fontaine Delia, Pawlowski Jan (2012), Intra-genomic ribosomal RNA polymorphism and morphological variation in Elphidium macellum suggests inter-specific hybridization in foraminifera., in PloS one, 7(2), 32373-32373.
The revised classification of eukaryotes.
Adl Sina M, Simpson Alastair G B, Lane Christopher E, Lukeš Julius, Bass David, Bowser Samuel S, Brown Matthew W, Burki Fabien, Dunthorn Micah, Hampl Vladimir, Heiss Aaron, Hoppenrath Mona, Lara Enrique, Le Gall Line, Lynn Denis H, McManus Hilary, Mitchell Edward A D, Mozley-Stanridge Sharon E, Parfrey Laura W, Pawlowski Jan, Rueckert Sonja, Shadwick Rueckert S, Shadwick Laura, Schoch Conrad L, Smirnov Alexey (2012), The revised classification of eukaryotes., in The Journal of eukaryotic microbiology, 59(5), 429-93.

Collaboration

Group / person Country
Types of collaboration
Dr. Wojciech Majewski, Institut of Paleobiology, Polish Academy of Sciences, Warszawa Poland (Europe)
- in-depth/constructive exchanges on approaches, methods or results
- Publication
Dr. Richard Christen, Université de Nice France (Europe)
- in-depth/constructive exchanges on approaches, methods or results
- Publication
Dr. Tomas Cedhagen, University of Aarhus Denmark (Europe)
- in-depth/constructive exchanges on approaches, methods or results
- Publication
Prof. Edward Mitchell, University Neuchâtel Switzerland (Europe)
- in-depth/constructive exchanges on approaches, methods or results
- Research Infrastructure
Dr. Thomas Wilding, SAMS Great Britain and Northern Ireland (Europe)
- in-depth/constructive exchanges on approaches, methods or results
- Publication
Dr. Colomban de Vargas, Station Biologique de Roscoff France (Europe)
- in-depth/constructive exchanges on approaches, methods or results
- Publication
Prof. Dr. P. Martinez Arbizu DZMB-Forschungsinstitut Senckenberg, Wilhelmshaven Germany (Europe)
- in-depth/constructive exchanges on approaches, methods or results
- Publication
Prof. Dr. Angelika Brandt, Zoological Museum, University of Hamburg Germany (Europe)
- in-depth/constructive exchanges on approaches, methods or results
Dr Samuel Bowser, Wadworth Center, Albany, NY United States of America (North America)
- in-depth/constructive exchanges on approaches, methods or results
- Publication
Dr. Fabien Burki, UBC, Vancouver Canada (North America)
- in-depth/constructive exchanges on approaches, methods or results
- Publication
Dr. Marek Zajaczkowski, IOPAN Sopot Poland (Europe)
- in-depth/constructive exchanges on approaches, methods or results
- Publication
Dr. Andrew Gooday, National Oceanographic Center, Southampton Great Britain and Northern Ireland (Europe)
- in-depth/constructive exchanges on approaches, methods or results
- Publication

Scientific events

Active participation

Title Type of contribution Title of article or contribution Date Place Persons involved
World Conference on Marine Biodiversity Talk given at a conference Next generation environmental DNA metabarcoding: a new tool for identification and assessment of deep-sea micro- and meiobenthic diversity. 12.10.2014 Qingdao, China Pawlowski Jan Wojciech;
Bioinformatique pour la Génomique Environmentale Talk given at a conference High-throughput molecular barcoding as a tool for assessment and monitoring the environmental impact associated with aquaculture 28.05.2014 Lyon, France Pawlowski Jan Wojciech;
Joint Aquatic Sciences Meeting Talk given at a conference Environmental barcoding as a tool for monitoring impact associated with salmon farming on community of benthic Foraminifera. 18.05.2014 Portland, United States of America Pawlowski Jan Wojciech;
Workshop Fundamental and Applied Protistology Talk given at a conference NGS applied to biomonitoring 15.04.2014 Neuchatel, Switzerland Pawlowski Jan Wojciech; Kuznetcov Ivan;
International Symposium on Foraminifera Talk given at a conference Towards a new classification of foraminifera: molecular contributions 24.01.2014 Concepcion, Chile Kuznetcov Ivan; Pawlowski Jan Wojciech; Sierra Miranda Roberto;
V Barcoding Conference Talk given at a conference Barcoding protists: the unseen eukaryotic majority 27.10.2013 Kunming, China Pawlowski Jan Wojciech;
International Congress of Protistology Talk given at a conference DNA barcoding and challenges of integrative taxonomy in protists 28.07.2013 Vancouver, Canada Pawlowski Jan Wojciech; Sierra Miranda Roberto;
Society for Molecular Biology and Evolution Symposium Talk given at a conference Deep relationships of Rhizaria 07.07.2013 Chicago, United States of America Pawlowski Jan Wojciech; Sierra Miranda Roberto;
32 Meeting of German Society of Protistology Talk given at a conference Protist metabarcoding: a new tool for environmental biomonitoring? 27.02.2013 Karthause Ittingen, Switzerland Pawlowski Jan Wojciech;
International Deep-Sea Biology Symposium Talk given at a conference Identifying active foraminiferans in the Sea of Japan using DNA and RNA-based metagenetics 03.12.2012 Wellington, New Zealand Pawlowski Jan Wojciech;
Society for Molecular Biology and Evolution Symposium Talk given at a conference Deep relationships of Rhizaria revealed by Phylogenomics 23.06.2012 Dublin, Ireland Pawlowski Jan Wojciech; Sierra Miranda Roberto;


Self-organised

Title Date Place
Eukaryotic -Omics: Exploring and testing with next-generation sequencing 24.04.2014 Genève, Switzerland

Communication with the public

Communication Title Media Place Year
Print (books, brochures, leaflets) The biology of the Southern Ocean: understanding its biodiversity and ecosystem. Italian-speaking Switzerland German-speaking Switzerland Western Switzerland 2015
New media (web, blogs, podcasts, news feeds etc.) A plea for high-throughput molecular monitoring of the deep-sea Deep-Sea Life 3:68 International 2014
Media relations: print media, online media Un diagnostic écologique pour les fermes salmonicoles Biofutur International 2014
Media relations: print media, online media Ancient DNA found hidden below sea floor news.sciencemag International 2013
Media relations: print media, online media Barcoding Protists - the unseen eukaryotic majority Barcode Bulletin International 2013
Media relations: print media, online media Jurassic Park au fond des océans Le Temps Western Switzerland 2013
Media relations: print media, online media Ocean floor holds ancient DNA The Scientist magazine International 2013
Talks/events/exhibitions La biodiversité en code-barres: rêve ou réalité? Western Switzerland 2012

Use-inspired outputs


Start-ups

Name Year
ID-Gene ecodiagnostics 2014

Associated projects

Number Title Start Funding scheme
125372 Molecular evolution and ecology of Foraminifera and related protists 01.04.2009 Project funding (Div. I-III)
150817 High-throughput sequencing for research on evolution and ecology of microeukaryotes 01.12.2013 R'EQUIP
159709 Molecular evolution and ecology of Foraminifera and related protists 01.04.2015 Project funding (Div. I-III)

Abstract

Recent development of next-generation sequencing (NGS) technologies provided a new tool to investigate the evolution and diversity of microeukaryotes. A remarkable progress has been achieved in understanding deep evolutionary relationships of eukaryotic phyla. On the other hand, environmental DNA studies led to the discovery of unexpected richness of microeukaryotes present in all sampled habitats, even the most hostile ones.In the present project, we will use NGS to explore the evolution and ecology of Foraminifera and related Rhizaria. This is a prolongation of a long-term project, whose aim is the collection and analysis of genetic data in order to infer evolutionary history, to describe the diversity and understand the biology of Foraminifera. Despite their ecological and evolutionary importance, our knowledge of foraminiferal genomics is still relatively poor. Our project aims to fill this gap by integrating different molecular approaches to investigate the evolution and diversity of this group.The project is divided into two parts. The first part is dedicated to a comparative analysis of NGS-generated transcriptomic data. We will complete the rhizarian transcriptomic database and test hypotheses concerning the phylogenetic position of Foraminifera and Radiolaria. We will also examine the deep phylogeny of foraminifera using selected genes obtained from transcriptomic data or by whole genome amplification approach. Finally, we will compare available transcriptomic data to identify and characterize the most common foraminiferal and rhizarian genes, with a special focus on genes involved in cell motility, biomineralization and development of multilocularity. In the second part of the project, we will use a molecular barcoding approach to identify foraminiferal species and assess their diversity in present and past environments. We will develop a comprehensive barcoding database comprising molecular and morphological data for all investigated foraminiferal species. We will use this database to analyse the worldwide distribution of deep-sea foraminifera inferred from NGS-based environmental studies. Furthermore, will test the preservation of foraminiferal DNA in subsurface sediment samples and evaluate the use of NGS technologies to infer past foraminiferal communities. Finally, we will develop a reverse taxonomy approach to identify and morphologically describe environmental lineages of Foraminifera that are known only by their sequences. The project will have a significant impact on our knowledge of evolution and diversity of protists. It will help inferring their evolutionary relationships and will contribute to a better understanding of fundamental cellular processes responsible for the outstanding diversification of Foraminifera and Radiolaria. It will also spur the development of new metagenetic tools to assess present and past foraminiferal richness and will thus shed light on their largely uncharted environmental diversity.
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