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Molecular evolution and ecology of Foraminifera and related protists

English title Molecular evolution and ecology of Foraminifera and related protists
Applicant Pawlowski Jan Wojciech
Number 179125
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 01.05.2018 - 31.10.2020
Approved amount 607'001.00
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All Disciplines (2)

Discipline
Zoology
Genetics

Keywords (9)

DNA Barcoding; Ancient DNA; Metabarcoding; Diversity; Eukaryotes; Evolution; Next Generation Sequencing; Foraminifera; Phylogeny

Lay Summary (French)

Lead
Les foraminifères sont des protistes (eucaryotes unicellulaires) dont les fossiles sont largement utilisés en paléontologie, mais dont la diversité actuelle reste encore très mal connue. Dans ce projet, nous utilisons divers techniques génomiques afin de mieux comprendre l’évolution, l’écologie et la diversité des ces organismes.
Lay summary

Contenu et objectifs du travail de recherche

Le projet s’inscrit dans le cadre des études phylogénomiques, métagénomiques et paléogénomiques dont l’objectif principal est de reconstruire l’histoire évolutive des espèces et d’examiner leur diversité à partir des données génomiques et transcriptomiques. Nos études précédentes ont permis de reconstruire l’arbre phylogénétique des foraminifères et découvrir une immense diversité des foraminifères modernes non-fossilisables. Dans le projet actuel nous utiliserons le séquençage à haut débit afin d’étudier les variations intra-spécifiques chez les foraminifères, explorer leurs relations avec d’autres microorganismes associés et identifier des espèces qui pourraient servir comme potentiels indicateurs des changements environnementaux. Nous allons aussi continuer à améliorer nos outils pour analyser les données de l’ADN environnemental afin de mieux les utiliser pour l’étude de la biodiversité.

Contexte scientifique et social du projet de recherche

Le projet contribuera à la recherche fondamentale sur l’évolution, l’écologie et la systématique des protistes. Il contribuera aussi à leur utilisation comme bioindicateurs pour évaluer l’état actuel des écosystèmes aquatiques ainsi que d’étudier leur histoire moderne à travers l’analyse des données paléogénomiques.

Mots-clés :

Séquençage à haut débit, code-barres génétiques, metabarcoding, ADN environnemental, ADN fossile, foraminifères, protistes, diversité, biomonitoring

Direct link to Lay Summary Last update: 09.04.2018

Responsible applicant and co-applicants

Employees

Publications

Publication
Planktonic foraminifera eDNA signature deposited on the seafloor remains preserved after burial in marine sediments
Barrenechea Angeles Inès, Lejzerowicz Franck, Cordier Tristan, Scheplitz Janin, Kucera Michal, Ariztegui Daniel, Pawlowski Jan, Morard Raphaël (2020), Planktonic foraminifera eDNA signature deposited on the seafloor remains preserved after burial in marine sediments, in Scientific Reports, 10(1), 20351-20351.
Planktonic foraminifera genomic variations reflect paleoceanographic changes in the Arctic: evidence from sedimentary ancient DNA
Pawłowska Joanna, Wollenburg Jutta E., Zajączkowski Marek, Pawlowski Jan (2020), Planktonic foraminifera genomic variations reflect paleoceanographic changes in the Arctic: evidence from sedimentary ancient DNA, in Scientific Reports, 10(1), 15102-15102.
Environmental DNA: What's behind the term? Clarifying the terminology and recommendations for its future use in biomonitoring
Pawlowski Jan, Apothéloz‐Perret‐Gentil Laure, Altermatt Florian (2020), Environmental DNA: What's behind the term? Clarifying the terminology and recommendations for its future use in biomonitoring, in Molecular Ecology, 29(22), 4258-4264.
Benthic monitoring of oil and gas offshore platforms in the North Sea using environmental DNA metabarcoding
Mauffrey Florian, Cordier Tristan, Apothéloz‐Perret‐Gentil Laure, Cermakova Kristina, Merzi Thomas, Delefosse Matthieu, Blanc Philippe, Pawlowski Jan (2020), Benthic monitoring of oil and gas offshore platforms in the North Sea using environmental DNA metabarcoding, in Molecular Ecology, mec.15698-mec.15698.
Benthic foraminiferal metabarcoding and morphology-based assessment around three offshore gas platforms: Congruence and complementarity
Frontalini Fabrizio, Cordier Tristan, Balassi Eszter, Armynot du Chatelet Eric, Cermakova Kristina, Apothéloz-Perret-Gentil Laure, Martins Maria Virginia Alves, Bucci Carla, Scantamburlo Enrico, Treglia Mauro, Bonamin Vladimiro, Pawlowski Jan (2020), Benthic foraminiferal metabarcoding and morphology-based assessment around three offshore gas platforms: Congruence and complementarity, in Environment International, 144, 106049-106049.
Broad sampling of monothalamids (Rhizaria, Foraminifera) gives further insight into diversity of non-marine Foraminifera
Siemensma Ferry, Holzmann Maria, Apothéloz-Perret-Gentil Laure, Clauß Steffen, Voelcker Eckhard, Bettighofer Wolfgang, Roshan Samira Khanipour, Walden Susanne, Dumack Kenneth, Pawlowski Jan (2020), Broad sampling of monothalamids (Rhizaria, Foraminifera) gives further insight into diversity of non-marine Foraminifera, in European Journal of Protistology, 125744-125744.
Xenophyophores (Rhizaria, Foraminifera), including four new species and two new genera, from the western Clarion-Clipperton Zone (abyssal equatorial Pacific)
Gooday Andrew J., Durden Jennifer M., Holzmann Maria, Pawlowski Jan, Smith Craig R. (2020), Xenophyophores (Rhizaria, Foraminifera), including four new species and two new genera, from the western Clarion-Clipperton Zone (abyssal equatorial Pacific), in European Journal of Protistology, 75, 125715-125715.
Ecosystems monitoring powered by environmental genomics: A review of current strategies with an implementation roadmap
Cordier Tristan, Alonso‐Sáez Laura, Apothéloz‐Perret‐Gentil Laure, Aylagas Eva, Bohan David A., Bouchez Agnès, Chariton Anthony, Creer Simon, Frühe Larissa, Keck François, Keeley Nigel, Laroche Olivier, Leese Florian, Pochon Xavier, Stoeck Thorsten, Pawlowski Jan, Lanzén Anders (2020), Ecosystems monitoring powered by environmental genomics: A review of current strategies with an implementation roadmap, in Molecular Ecology, mec.15472-mec.15472.
Dataset of foraminiferal sedimentary DNA (sedDNA) sequences from Svalbard
Pawłowska Joanna, Pawlowski Jan, Zajączkowski Marek (2020), Dataset of foraminiferal sedimentary DNA (sedDNA) sequences from Svalbard, in Data in Brief, 30, 105553-105553.
A meeting framework for inclusive and sustainable science
Blackman Rosetta C., Bruder Andreas, Burdon Francis J., Convey Peter, Funk W. Chris, Jähnig Sonja C., Kishe Mary Alphonce, Moretti Marcelo S., Natugonza Vianny, Pawlowski Jan, Stubbington Rachel, Zhang Xiaowei, Seehausen Ole, Altermatt Florian (2020), A meeting framework for inclusive and sustainable science, in Nature Ecology & Evolution, 4(5), 668-671.
Supervised machine learning is superior to indicator value inference in monitoring the environmental impacts of salmon aquaculture using eDNA metabarcodes
Frühe Larissa, Cordier Tristan, Dully Verena, Breiner Hans‐Werner, Lentendu Guillaume, Pawlowski Jan, Martins Catarina, Wilding Thomas A., Stoeck Thorsten (2020), Supervised machine learning is superior to indicator value inference in monitoring the environmental impacts of salmon aquaculture using eDNA metabarcodes, in Molecular Ecology, mec.15434-mec.15434.
Multiproxy evidence of the Neoglacial expansion of Atlantic Water to eastern Svalbard
Pawłowska Joanna, Łącka Magdalena, Kucharska Małgorzata, Pawlowski Jan, Zajączkowski Marek (2020), Multiproxy evidence of the Neoglacial expansion of Atlantic Water to eastern Svalbard, in Climate of the Past, 16(2), 487-501.
Insights into the ecology of epibenthic calcareous foraminifera from a colonization study at 4000 m (Station M) in the NE Pacific Ocean
Burkett Ashley, Rathburn Anthony, Pratt Robert Brandon, Holzmann Maria (2020), Insights into the ecology of epibenthic calcareous foraminifera from a colonization study at 4000 m (Station M) in the NE Pacific Ocean, in Deep Sea Research Part II: Topical Studies in Oceanography, 173, 104709-104709.
Reply to: Sources of C30 steroid biomarkers in Neoproterozoic–Cambrian rocks and oils
Hallmann Christian, Nettersheim Benjamin J., Brocks Jochen J., Schwelm Arne, Hope Janet M., Not Fabrice, Lomas Michael, Schmidt Christiane, Schiebel Ralf, Nowack Eva C. M., De Deckker Patrick, Pawlowski Jan, Bowser Samuel S., Bobrovskiy Ilya, Zonneveld Karin, Kucera Michal, Stuhr Marleen (2020), Reply to: Sources of C30 steroid biomarkers in Neoproterozoic–Cambrian rocks and oils, in Nature Ecology & Evolution, 4(1), 37-39.
Key Questions for Next-Generation Biomonitoring
Makiola Andreas, Compson Zacchaeus G., Baird Donald J., Barnes Matthew A., Boerlijst Sam P., Bouchez Agnès, Brennan Georgina, Bush Alex, Canard Elsa, Cordier Tristan, Creer Simon, Curry R. Allen, David Patrice, Dumbrell Alex J., Gravel Dominique, Hajibabaei Mehrdad, Hayden Brian, van der Hoorn Berry, Jarne Philippe, Jones J. Iwan, Karimi Battle, Keck Francois, Kelly Martyn, Knot Ineke E., et al. (2020), Key Questions for Next-Generation Biomonitoring, in Frontiers in Environmental Science, 7, 197.
SLIM: a flexible web application for the reproducible processing of environmental DNA metabarcoding data
Dufresne Yoann, Lejzerowicz Franck, Perret-Gentil Laure Apotheloz, Pawlowski Jan, Cordier Tristan (2019), SLIM: a flexible web application for the reproducible processing of environmental DNA metabarcoding data, in BMC Bioinformatics, 20(1), 88-88.
Benthic foraminiferal DNA metabarcodes significantly vary along a gradient from abyssal to hadal depths and between each side of the Kuril-Kamchatka trench
Cordier Tristan, Barrenechea Inès, Lejzerowicz Franck, Reo Emanuela, Pawlowski Jan (2019), Benthic foraminiferal DNA metabarcodes significantly vary along a gradient from abyssal to hadal depths and between each side of the Kuril-Kamchatka trench, in Progress in Oceanography, 178, 102175-102175.
Combined Molecular and Morphological Taxonomy of the Beccarii/T3 Group of the Foraminiferal Genus Ammonia
Hayward Bruce W., Holzmann Maria., Tsuchiya Masashi (2019), Combined Molecular and Morphological Taxonomy of the Beccarii/T3 Group of the Foraminiferal Genus Ammonia, in Journal of Foraminiferal Research, 49(4), 367-389.
Global Observing Needs in the Deep Ocean
Levin Lisa A., Bett Brian J., Gates Andrew R., Heimbach Patrick, Howe Bruce M., Janssen Felix, McCurdy Andrea, Ruhl Henry A., Snelgrove Paul, Stocks Karen I., Bailey David, Baumann-Pickering Simone, Beaverson Chris, Benfield Mark C., Booth David J., Carreiro-Silva Marina, Colaço Ana, Eblé Marie C., Fowler Ashley M., Gjerde Kristina M., Jones Daniel O. B., Katsumata K., Kelley Deborah, Le Bris Nadine, et al. (2019), Global Observing Needs in the Deep Ocean, in Frontiers in Marine Science, 6, 241.
Embracing Environmental Genomics and Machine Learning for Routine Biomonitoring
Cordier Tristan, Lanzén Anders, Apothéloz-Perret-Gentil Laure, Stoeck Thorsten, Pawlowski Jan (2019), Embracing Environmental Genomics and Machine Learning for Routine Biomonitoring, in Trends in Microbiology, 27(5), 387-397.
DNA metabarcoding—Need for robust experimental designs to draw sound ecological conclusions
Zinger Lucie, Bonin Aurélie, Alsos Inger G., Bálint Miklós, Bik Holly, Boyer Frédéric, Chariton Anthony A., Creer Simon, Coissac Eric, Deagle Bruce E., De Barba Marta, Dickie Ian A., Dumbrell Alex J., Ficetola Gentile Francesco, Fierer Noah, Fumagalli Luca, Gilbert M. Thomas P., Jarman Simon, Jumpponen Ari, Kauserud Håvard, Orlando Ludovic, Pansu Johan, Pawlowski Jan, Tedersoo Leho, et al. (2019), DNA metabarcoding—Need for robust experimental designs to draw sound ecological conclusions, in Molecular Ecology, 28(8), 1857-1862.
Putative sponge biomarkers in unicellular Rhizaria question an early rise of animals
Nettersheim Benjamin J., Brocks Jochen J., Schwelm Arne, Hope Janet M., Not Fabrice, Lomas Michael, Schmidt Christiane, Schiebel Ralf, Nowack Eva C. M., De Deckker Patrick, Pawlowski Jan, Bowser Samuel S., Bobrovskiy Ilya, Zonneveld Karin, Kucera Michal, Stuhr Marleen, Hallmann Christian (2019), Putative sponge biomarkers in unicellular Rhizaria question an early rise of animals, in Nature Ecology & Evolution, 3(4), 577-581.
Multi-marker eDNA metabarcoding survey to assess the environmental impact of three offshore gas platforms in the North Adriatic Sea (Italy)
Cordier Tristan, Frontalini Fabrizio, Cermakova Kristina, Apothéloz-Perret-Gentil Laure, Treglia Mauro, Scantamburlo Enrico, Bonamin Vladimiro, Pawlowski Jan (2019), Multi-marker eDNA metabarcoding survey to assess the environmental impact of three offshore gas platforms in the North Adriatic Sea (Italy), in Marine Environmental Research, 146, 24-34.
Responses of foraminifera communities to aquaculture‐derived organic enrichment as revealed by environmental DNA metabarcoding
He Xiaoping, Sutherland Terri F., Pawlowski Jan, Abbott Cathryn L. (2019), Responses of foraminifera communities to aquaculture‐derived organic enrichment as revealed by environmental DNA metabarcoding, in Molecular Ecology, 28(5), 1138-1153.
Revisions to the Classification, Nomenclature, and Diversity of Eukaryotes
Adl Sina M., Bass David, Lane Christopher E., Lukeš Julius, Schoch Conrad L., Smirnov Alexey, Agatha Sabine, Berney Cedric, Brown Matthew W., Burki Fabien, Cárdenas Paco, Čepička Ivan, Chistyakova Lyudmila, Campo Javier, Dunthorn Micah, Edvardsen Bente, Eglit Yana, Guillou Laure, Hampl Vladimír, Heiss Aaron A., Hoppenrath Mona, James Timothy Y., Karnkowska Anna, Karpov Sergey, et al. (2019), Revisions to the Classification, Nomenclature, and Diversity of Eukaryotes, in Journal of Eukaryotic Microbiology, 66(1), 4-119.
Xenophyophores (Rhizaria, Foraminifera) from the Eastern Clarion-Clipperton Zone (equatorial Pacific): the Genus Psammina
Gooday Andrew J., Holzmann Maria, Goineau Aurélie, Kamenskaya Olga, Melnik Vyacheslav F., Pearce Richard B., Weber Alexandra A.-T., Pawlowski Jan (2018), Xenophyophores (Rhizaria, Foraminifera) from the Eastern Clarion-Clipperton Zone (equatorial Pacific): the Genus Psammina, in Protist, 169(6), 926-957.
Supervised machine learning outperforms taxonomy-based environmental DNA metabarcoding applied to biomonitoring
Cordier Tristan, Forster Dominik, Dufresne Yoann, Martins Catarina I. M., Stoeck Thorsten, Pawlowski Jan (2018), Supervised machine learning outperforms taxonomy-based environmental DNA metabarcoding applied to biomonitoring, in Molecular Ecology Resources, 18(6), 1381-1391.
The future of biotic indices in the ecogenomic era: Integrating (e)DNA metabarcoding in biological assessment of aquatic ecosystems
Pawlowski Jan, Kelly-Quinn Mary, Altermatt Florian, Apothéloz-Perret-Gentil Laure, Beja Pedro, Boggero Angela, Borja Angel, Bouchez Agnès, Cordier Tristan, Domaizon Isabelle, Feio Maria Joao, Filipe Ana Filipa, Fornaroli Riccardo, Graf Wolfram, Herder Jelger, van der Hoorn Berry, Iwan Jones J., Sagova-Mareckova Marketa, Moritz Christian, Barquín Jose, Piggott Jeremy J., Pinna Maurizio, Rimet Frederic, Rinkevich Buki, et al. (2018), The future of biotic indices in the ecogenomic era: Integrating (e)DNA metabarcoding in biological assessment of aquatic ecosystems, in Science of The Total Environment, 637-638, 1295-1310.
Variable dispersal histories across the Drake Passage: The case of coastal benthic Foraminifera
Majda Aneta, Majewski Wojciech, Mamos Tomasz, Grabowski Michał, Godoi Maria Angelica, Pawłowski Jan (2018), Variable dispersal histories across the Drake Passage: The case of coastal benthic Foraminifera, in Marine Micropaleontology, 140, 81-94.

Datasets

Foraminifera metabarcodes

Author Cordier, Tristan
Publication date 12.07.2019
Persistent Identifier (PID) https://doi.org/10.1016/j.pocean.2019.102175
Repository NCBI
Abstract
Environmental genomics data from sediment samples collected during the KuramBio II (Kuril Kamchatka Biodiversity Studies II) expedition on RV Sonne in 2016

Eukaryotic metabarcodes for benthic monitoring

Author Cordier , Tristan
Publication date 21.02.2018
Persistent Identifier (PID) doi: 10.1111/1755-0998.12926
Repository NCBI
Abstract
The study compares the performance of five barcoding genes for ecological quality status inference in marine environments. The genes include one bacterial, one foraminiferal and three eukaryotes ones,

Eukaryotic metabarcodes from North Adriatic

Author Cordier, Tristan
Persistent Identifier (PID) doi: 10.1016/j.marenvres.2018.12.009
Repository NCBI
Abstract
Multi-marker eDNA metabarcoding survey around offshore gas platforms in the North Adriatic Sea

North Sea sediment DNA metabarcodes

Author Cordier, Tristan
Persistent Identifier (PID) doi: 10.1111/mec.15698
Repository NCBI
Abstract
This study aimed at evaluating the potential of metabarcoding to replace morphological identification for assessing the impact of oil drilling platform activities on sediments community.

Collaboration

Group / person Country
Types of collaboration
Technical University Kaiserlautern Germany (Europe)
- in-depth/constructive exchanges on approaches, methods or results
- Publication
- Research Infrastructure
MARUM Germany (Europe)
- in-depth/constructive exchanges on approaches, methods or results
- Publication
University of Urbino Italy (Europe)
- in-depth/constructive exchanges on approaches, methods or results
- Publication
National Oceanographic Center Great Britain and Northern Ireland (Europe)
- in-depth/constructive exchanges on approaches, methods or results
- Publication
IOPAN Poland (Europe)
- in-depth/constructive exchanges on approaches, methods or results
- Publication
Institute of Paleobiology, PAN Poland (Europe)
- in-depth/constructive exchanges on approaches, methods or results
- Publication
Eawag Switzerland (Europe)
- in-depth/constructive exchanges on approaches, methods or results
- Publication
Total SA France (Europe)
- in-depth/constructive exchanges on approaches, methods or results
- Publication
- Industry/business/other use-inspired collaboration

Scientific events

Active participation

Title Type of contribution Title of article or contribution Date Place Persons involved
Virtual workshop on Metabarcoding monitoring Talk given at a conference Environmental DNA metabarcoding – the future of biomonitoring 27.11.2020 Bogota, Colombia Pawlowski Jan Wojciech;
Naturalis - seminar Individual talk Foraminiferal eDNA metabarcoding and biomonitoring: promises and challenges 12.11.2020 Naturalis, Netherlands Pawlowski Jan Wojciech;
German Society for Protozoology meeting Talk given at a conference Protist metabarcoding and next-generation biomonitoring 05.03.2020 Kaiserlautern, Germany Pawlowski Jan Wojciech;
Polish Evolutionary Conference Individual talk Environmental DNA: a novel way to explore and monitor present and past biodiversity 17.09.2019 Gdansk, Poland Pawlowski Jan Wojciech;
Workshop on Environmental Biomonitoring Talk given at a conference Foraminiferal DNA metabarcoding – a new promising tool for benthic monitoring 13.05.2019 Sao Paolo, Brazil Pawlowski Jan Wojciech;
Stazione Zoologica di Napoli - seminar Individual talk Next-generation biomonitoring or how DNA metabarcording can help assessing human impacts on marine environments 18.10.2018 Napoli, Italy Pawlowski Jan Wojciech;


Communication with the public

Communication Title Media Place Year
Media relations: print media, online media Les unicellulaires dominent l'arbre du vivant Hotspot Italian-speaking Switzerland German-speaking Switzerland Western Switzerland 2020

Associated projects

Number Title Start Funding scheme
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

The evolutionary and ecological studies of microbial eukaryotes, or protists, have been completely transformed by accumulation of genomic and metagenomic data readily obtained from diverse biological and environmental material. The evolutionary history of protists has been profoundly revised by phylogenomics, while environmental genomics brought to light the immense diversity of the microeukaryotic biome and enhanced its ecological importance. Yet, unraveling the evolutionary and ecological information from extremely complex eukaryotic genomes and metagenomes is not always straightforward, and the transformation of this information into practical applications can be sometimes problematic.Here, we address some of the challenges raised by the deluge of high-throughput sequencing (HTS) data, focusing on molecular evolution and ecology of foraminifera and related protists. The project continues a long-term research that has been conducted by our group on protist phylogeny, taxonomy, and molecular ecology. The project is based on our extensive expertise in the field, the large databases accumulated over the years, and in-house built pipelines for their analyses. It also benefits of a large network of collaborations that facilitates the access to samples, assists in their processing and analyzing the obtained data.The project comprises two complementary parts. In the first part, we will use single-cell DNA and RNA-seq approaches in order to (1) complement the foraminiferal barcoding database, (2) revise the evolutionary relationships and identify foraminiferal mitochondrial genes, (3) assess the importance of intra-genomic variations, and (4) evaluate the role of bacterial microbiomes in the metabolism of foraminifera and their close relatives. In the second part, we will use environmental genomics in order to (5) assess the patterns of deep-sea benthic diversity, (6) expand the use of fossil eukaryotic DNA as paleoenvironmental proxy, and (7) search for species and genes that could be used as biosensors of environmental impacts. To facilitate the latter tasks, (8) we will develop bioinformatic tools for rapid and accurate analysis of environmental HTS data, focusing on machine learning and ecological network analyses applied to biomonitoring.The project has significance for both fundamental and applied science. Foraminifera are highly diversified both taxonomically and ecologically, and therefore represent a key model to improve our understanding of the origin and evolution of single-cell eukaryotes. The ubiquity, sensitivity and adaptability of foraminifera prompt their use as a proxy to infer global biodiversity patterns and to reconstruct paleoenvironments and paleoclimates using DNA preserved in the sediment. Finally, we will develop a novel category of DNA-based sensors to assess the environmental impacts of industrial activities.
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