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1. Simulation of bacterial populations with SLiM

Author

Cury, Jean, Haller, Benjamin C., Achaz, Guillaume, and Jay, Flora

Subjects
Archaeology, CC1-960, Science
Abstract

Simulation of genomic data is a key tool in population genetics, yet, to date, there is no forward-in-time simulator of bacterial populations that is both computationally efficient and adaptable to a wide range of scenarios. Here we demonstrate how to simulate bacterial populations with SLiM, a forward-in-time simulator built for eukaryotes. SLiM has gained many users in recent years, due to its speed and power, and has extensive documentation showcasing various scenarios that it can simulate. This paper focuses on a simple demographic scenario, to explore unique aspects of modeling bacteria in SLiM’s scripting language. In addition, we illustrate the flexibility of SLiM by simulating the growth of bacteria on a Petri dish with antibiotic. To foster the development of bacterial simulations based upon this recipe, we explain the inner workings of its code. We also validate the simulator, by extensively testing the results of simulations against existing simulators, and against theoretical expectations for some summary statistics. This protocol, with the flexibility and power of SLiM, will enable the community to simulate bacterial populations efficiently under a wide range of evolutionary scenarios.

Published
2022
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4. Expanding the stdpopsim species catalog, and lessons learned for realistic genome simulations

Author

Lauterbur, M Elise, Cavassim, Maria Izabel A, Gladstein, Ariella L, Gower, Graham, Pope, Nathaniel S, Tsambos, Georgia, Adrion, Jeffrey, Belsare, Saurabh, Biddanda, Arjun, Caudill, Victoria, Cury, Jean, Echevarria, Ignacio, Haller, Benjamin C, Hasan, Ahmed R, Huang, Xin, Iasi, Leonardo Nicola Martin, Noskova, Ekaterina, Obsteter, Jana, Pavinato, Vitor Antonio Correa, Pearson, Alice, Peede, David, Perez, Manolo F, Rodrigues, Murillo F, Smith, Chris CR, Spence, Jeffrey P, Teterina, Anastasia, Tittes, Silas, Unneberg, Per, Vazquez, Juan Manuel, Waples, Ryan K, Wohns, Anthony Wilder, Wong, Yan, Baumdicker, Franz, Cartwright, Reed A, Gorjanc, Gregor, Gutenkunst, Ryan N, Kelleher, Jerome, Kern, Andrew D, Ragsdale, Aaron P, Ralph, Peter L, Schrider, Daniel R, and Gronau, Ilan

Subjects
Genetics, Biotechnology, Human Genome, Generic health relevance, Software, Computer Simulation, Genome, Genetics, Population, Genomics, population genetics, simulations, open source, None, genetics, genomics, none, Biochemistry and Cell Biology
Abstract

Simulation is a key tool in population genetics for both methods development and empirical research, but producing simulations that recapitulate the main features of genomic datasets remains a major obstacle. Today, more realistic simulations are possible thanks to large increases in the quantity and quality of available genetic data, and the sophistication of inference and simulation software. However, implementing these simulations still requires substantial time and specialized knowledge. These challenges are especially pronounced for simulating genomes for species that are not well-studied, since it is not always clear what information is required to produce simulations with a level of realism sufficient to confidently answer a given question. The community-developed framework stdpopsim seeks to lower this barrier by facilitating the simulation of complex population genetic models using up-to-date information. The initial version of stdpopsim focused on establishing this framework using six well-characterized model species (Adrion et al., 2020). Here, we report on major improvements made in the new release of stdpopsim (version 0.2), which includes a significant expansion of the species catalog and substantial additions to simulation capabilities. Features added to improve the realism of the simulated genomes include non-crossover recombination and provision of species-specific genomic annotations. Through community-driven efforts, we expanded the number of species in the catalog more than threefold and broadened coverage across the tree of life. During the process of expanding the catalog, we have identified common sticking points and developed the best practices for setting up genome-scale simulations. We describe the input data required for generating a realistic simulation, suggest good practices for obtaining the relevant information from the literature, and discuss common pitfalls and major considerations. These improvements to stdpopsim aim to further promote the use of realistic whole-genome population genetic simulations, especially in non-model organisms, making them available, transparent, and accessible to everyone.

Published
2023

9. The immune modules conserved across the tree of life: Towards a definition of ancestral immunity.

Author

Bernheim, Aude, Cury, Jean, and Poirier, Enzo Z.

Subjects
*IMMUNITY, *PROKARYOTES, *PROTEIN domains
Abstract

Immune defence mechanisms exist across the tree of life in such diversity that prokaryotic antiviral responses have historically been considered unrelated to eukaryotic immunity. Mechanisms of defence in divergent eukaryotes were similarly believed to be largely clade specific. However, recent data indicate that a subset of modules (domains and proteins) from prokaryote defence systems are conserved in eukaryotes and populate many stages of innate immune pathways. In this Essay, we propose the notion of ancestral immunity, which corresponds to the set of immune modules conserved between prokaryotes and eukaryotes. After offering a typology of ancestral immunity, we speculate on the selective pressures that could have led to the differential conservation of specific immune modules across domains of life. The exploration of ancestral immunity is in its infancy and appears full of promises to illuminate immune evolution, and also to identify and decipher immune mechanisms of economic, ecological, and therapeutic importance. A subset of prokaryotic antiviral systems are conserved in eukaryotes and have crucial roles in immune pathways. This Essay introduces the concept of ancestral immunity, which refers to the set of immune modules (domains and proteins) conserved between prokaryotes and eukaryotes, discussing the topology of ancestral immunity and a putative evolutionary scenario for its existence. [ABSTRACT FROM AUTHOR]

Published
2024
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13. Expanding the stdpopsim species catalog, and lessons learned for realistic genome simulations

Author

Lauterbur, M Elise, primary, Cavassim, Maria Izabel A, additional, Gladstein, Ariella L, additional, Gower, Graham, additional, Pope, Nathaniel S, additional, Tsambos, Georgia, additional, Adrion, Jeffrey, additional, Belsare, Saurabh, additional, Biddanda, Arjun, additional, Caudill, Victoria, additional, Cury, Jean, additional, Echevarria, Ignacio, additional, Haller, Benjamin C, additional, Hasan, Ahmed R, additional, Huang, Xin, additional, Iasi, Leonardo Nicola Martin, additional, Noskova, Ekaterina, additional, Obsteter, Jana, additional, Pavinato, Vitor Antonio Correa, additional, Pearson, Alice, additional, Peede, David, additional, Perez, Manolo F, additional, Rodrigues, Murillo F, additional, Smith, Chris CR, additional, Spence, Jeffrey P, additional, Teterina, Anastasia, additional, Tittes, Silas, additional, Unneberg, Per, additional, Vazquez, Juan Manuel, additional, Waples, Ryan K, additional, Wohns, Anthony Wilder, additional, Wong, Yan, additional, Baumdicker, Franz, additional, Cartwright, Reed A, additional, Gorjanc, Gregor, additional, Gutenkunst, Ryan N, additional, Kelleher, Jerome, additional, Kern, Andrew D, additional, Ragsdale, Aaron P, additional, Ralph, Peter L, additional, Schrider, Daniel R, additional, and Gronau, Ilan, additional

Published
2023
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14. Expanding the stdpopsim species catalog, and lessons learned for realistic genome simulations

Author

Lauterbur, M. Elise, primary, Cavassim, Maria Izabel A., additional, Gladstein, Ariella L., additional, Gower, Graham, additional, Pope, Nathaniel S., additional, Tsambos, Georgia, additional, Adrion, Jeff, additional, Belsare, Saurabh, additional, Biddanda, Arjun, additional, Caudill, Victoria, additional, Cury, Jean, additional, Echevarria, Ignacio, additional, Haller, Benjamin C., additional, Hasan, Ahmed R., additional, Huang, Xin, additional, Iasi, Leonardo Nicola Martin, additional, Noskova, Ekaterina, additional, Obšteter, Jana, additional, Pavinato, Vitor Antonio Corrêa, additional, Pearson, Alice, additional, Peede, David, additional, Perez, Manolo F., additional, Rodrigues, Murillo F., additional, Smith, Chris C. R., additional, Spence, Jeffrey P., additional, Teterina, Anastasia, additional, Tittes, Silas, additional, Unneberg, Per, additional, Vazquez, Juan Manuel, additional, Waples, Ryan K., additional, Wohns, Anthony Wilder, additional, Wong, Yan, additional, Baumdicker, Franz, additional, Cartwright, Reed A., additional, Gorjanc, Gregor, additional, Gutenkunst, Ryan N., additional, Kelleher, Jerome, additional, Kern, Andrew D., additional, Ragsdale, Aaron P., additional, Ralph, Peter L., additional, Schrider, Daniel R., additional, and Gronau, Ilan, additional

Published
2023
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16. Expanding the stdpopsim species catalog, and lessons learned for realistic genome simulations

Author

Lauterbur, M. Elise, Cavassim, Maria Izabel A., Gladstein, Ariella L., Gower, Graham, Pope, Nathaniel S., Tsambos, Georgia, Adrion, Jeffrey, Belsare, Saurabh, Biddanda, Arjun, Caudill, Victoria, Cury, Jean, Echevarria, Ignacio, Haller, Benjamin C., Hasan, Ahmed R., Huang, Xin, Iasi, Leonardo Nicola Martin, Noskova, Ekaterina, Obsteter, Jana, Pavinato, Vitor Antonio Correa, Pearson, Alice, Peede, David, Perez, Manolo F., Rodrigues, Murillo F., Smith, Chris C. R., Spence, Jeffrey P., Teterina, Anastasia, Tittes, Silas, Unneberg, Per, Vazquez, Juan Manuel, Waples, Ryan K., Wohns, Anthony Wilder, Wong, Yan, Baumdicker, Franz, Cartwright, Reed A., Gorjanc, Gregor, Gutenkunst, Ryan N., Kelleher, Jerome, Kern, Andrew D., Ragsdale, Aaron P., Ralph, Peter L., Schrider, Daniel R., Gronau, Ilan, Lauterbur, M. Elise, Cavassim, Maria Izabel A., Gladstein, Ariella L., Gower, Graham, Pope, Nathaniel S., Tsambos, Georgia, Adrion, Jeffrey, Belsare, Saurabh, Biddanda, Arjun, Caudill, Victoria, Cury, Jean, Echevarria, Ignacio, Haller, Benjamin C., Hasan, Ahmed R., Huang, Xin, Iasi, Leonardo Nicola Martin, Noskova, Ekaterina, Obsteter, Jana, Pavinato, Vitor Antonio Correa, Pearson, Alice, Peede, David, Perez, Manolo F., Rodrigues, Murillo F., Smith, Chris C. R., Spence, Jeffrey P., Teterina, Anastasia, Tittes, Silas, Unneberg, Per, Vazquez, Juan Manuel, Waples, Ryan K., Wohns, Anthony Wilder, Wong, Yan, Baumdicker, Franz, Cartwright, Reed A., Gorjanc, Gregor, Gutenkunst, Ryan N., Kelleher, Jerome, Kern, Andrew D., Ragsdale, Aaron P., Ralph, Peter L., Schrider, Daniel R., and Gronau, Ilan

Abstract

Simulation is a key tool in population genetics for both methods development and empirical research, but producing simulations that recapitulate the main features of genomic datasets remains a major obstacle. Today, more realistic simulations are possible thanks to large increases in the quantity and quality of available genetic data, and the sophistication of inference and simulation software. However, implementing these simulations still requires substantial time and specialized knowledge. These challenges are especially pronounced for simulating genomes for species that are not well-studied, since it is not always clear what information is required to produce simulations with a level of realism sufficient to confidently answer a given question. The community-developed framework stdpopsim seeks to lower this barrier by facilitating the simulation of complex population genetic models using up-to-date information. The initial version of stdpopsim focused on establishing this framework using six well-characterized model species (Adrion et al., 2020). Here, we report on major improvements made in the new release of stdpopsim (version 0.2), which includes a significant expansion of the species catalog and substantial additions to simulation capabilities. Features added to improve the realism of the simulated genomes include non-crossover recombination and provision of species-specific genomic annotations. Through community-driven efforts, we expanded the number of species in the catalog more than threefold and broadened coverage across the tree of life. During the process of expanding the catalog, we have identified common sticking points and developed the best practices for setting up genome-scale simulations. We describe the input data required for generating a realistic simulation, suggest good practices for obtaining the relevant information from the literature, and discuss common pitfalls and major considerations. These improvements to stdpopsim aim to further pro

Published
2023
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20. Expanding the stdpopsim species catalog, and lessons learned for realistic genome simulations

Author

Lauterbur, M. Elise, primary, Cavassim, Maria Izabel A., additional, Gladstein, Ariella L., additional, Gower, Graham, additional, Pope, Nathaniel S., additional, Tsambos, Georgia, additional, Adrion, Jeff, additional, Belsare, Saurabh, additional, Biddanda, Arjun, additional, Caudill, Victoria, additional, Cury, Jean, additional, Echevarria, Ignacio, additional, Haller, Benjamin C., additional, Hasan, Ahmed R., additional, Huang, Xin, additional, Iasi, Leonardo Nicola Martin, additional, Noskova, Ekaterina, additional, Obšteter, Jana, additional, Pavinato, Vitor Antonio Corrêa, additional, Pearson, Alice, additional, Peede, David, additional, Perez, Manolo F., additional, Rodrigues, Murillo F., additional, Smith, Chris C. R., additional, Spence, Jeffrey P., additional, Teterina, Anastasia, additional, Tittes, Silas, additional, Unneberg, Per, additional, Vazquez, Juan Manuel, additional, Waples, Ryan K., additional, Wohns, Anthony Wilder, additional, Wong, Yan, additional, Baumdicker, Franz, additional, Cartwright, Reed A., additional, Gorjanc, Gregor, additional, Gutenkunst, Ryan N., additional, Kelleher, Jerome, additional, Kern, Andrew D., additional, Ragsdale, Aaron P., additional, Ralph, Peter L., additional, Schrider, Daniel R., additional, and Gronau, Ilan, additional

Published
2022
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21. A new route for integron cassette dissemination among bacterial genomes

Author

Loot, Céline, primary, Millot, Gael A., additional, Richard, Egill, additional, Littner, Eloi, additional, Vit, Claire, additional, Lemoine, Frédéric, additional, Cury, Jean, additional, Darracq, Baptiste, additional, Niault, Théophile, additional, Lapaillerie, Delphine, additional, Parissi, Vincent, additional, Rocha, Eduardo PC, additional, and Mazel, Didier, additional

Published
2022
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23. Intracellular Positioning Systems Limit the Entropic Eviction of Secondary Replicons Toward the Nucleoid Edges in Bacterial Cells

Author

Dauverd -Girault, Julie, Planchenault, Charlène, Pons, Marine, Schiavon, Caroline, Siguier, Patricia, Rech, Jérôme, Guynet, Catherine, Dauverd-Girault, Julie, Cury, Jean, Rocha, Eduardo, Junier, Ivan, Cornet, François, Espéli, Olivier, espeli, olivier, Appel à projets générique - Génèse et maintenance des chromosomes secondaire bactériens - - MAGISBAC2014 - ANR-14-CE10-0007 - Appel à projets générique - VALID, Centre interdisciplinaire de recherche en biologie (CIRB), Labex MemoLife, École normale supérieure - Paris (ENS-PSL), Université Paris sciences et lettres (PSL)-Université Paris sciences et lettres (PSL)-Collège de France (CdF (institution))-Ecole Superieure de Physique et de Chimie Industrielles de la Ville de Paris (ESPCI Paris), Université Paris sciences et lettres (PSL)-École normale supérieure - Paris (ENS-PSL), Université Paris sciences et lettres (PSL)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS), Laboratoire de microbiologie et génétique moléculaires - UMR5100 (LMGM), Centre de Biologie Intégrative (CBI), Université Toulouse III - Paul Sabatier (UT3), Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées-Centre National de la Recherche Scientifique (CNRS)-Université Toulouse III - Paul Sabatier (UT3), Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées-Centre National de la Recherche Scientifique (CNRS), Génomique évolutive des Microbes / Microbial Evolutionary Genomics, Institut Pasteur [Paris] (IP)-Centre National de la Recherche Scientifique (CNRS), Biologie Computationnelle et Mathématique (TIMC-IMAG-BCM), Techniques de l'Ingénierie Médicale et de la Complexité - Informatique, Mathématiques et Applications Grenoble - UMR 5525 (TIMC-IMAG), VetAgro Sup - Institut national d'enseignement supérieur et de recherche en alimentation, santé animale, sciences agronomiques et de l'environnement (VAS)-Centre National de la Recherche Scientifique (CNRS)-Université Grenoble Alpes (UGA)-Institut polytechnique de Grenoble - Grenoble Institute of Technology (Grenoble INP ), Université Grenoble Alpes (UGA)-VetAgro Sup - Institut national d'enseignement supérieur et de recherche en alimentation, santé animale, sciences agronomiques et de l'environnement (VAS)-Centre National de la Recherche Scientifique (CNRS)-Université Grenoble Alpes (UGA)-Institut polytechnique de Grenoble - Grenoble Institute of Technology (Grenoble INP ), Université Grenoble Alpes (UGA), Institut Jean Roger, This work as funded by ANR ANR-14-CE10-0007-01 to OE, FC and ER by the CNRS PICS initiative to OE and IJ and by the Foundation ARC (PJA 20171206119) to OE, ANR-14-CE10-0007,MAGISBAC,Génèse et maintenance des chromosomes secondaire bactériens(2014), Ecole Superieure de Physique et de Chimie Industrielles de la Ville de Paris (ESPCI Paris), Université Paris sciences et lettres (PSL)-Université Paris sciences et lettres (PSL)-École normale supérieure - Paris (ENS Paris), Université Paris sciences et lettres (PSL)-Collège de France (CdF (institution))-Ecole Superieure de Physique et de Chimie Industrielles de la Ville de Paris (ESPCI Paris), Université Paris sciences et lettres (PSL)-Collège de France (CdF (institution))-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS), Laboratoire de microbiologie et génétique moléculaires (LMGM), Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées-Centre National de la Recherche Scientifique (CNRS)-Centre de Biologie Intégrative (CBI), Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées-Centre National de la Recherche Scientifique (CNRS)-Centre National de la Recherche Scientifique (CNRS), Université Paris sciences et lettres (PSL), Génétique des Interactions macromoléculaires, Institut Pasteur [Paris]-Centre National de la Recherche Scientifique (CNRS), Génomique et Évolution des Microorganismes (TIMC-GEM ), Techniques de l'Ingénierie Médicale et de la Complexité - Informatique, Mathématiques et Applications, Grenoble - UMR 5525 (TIMC ), IMAG-VetAgro Sup - Institut national d'enseignement supérieur et de recherche en alimentation, santé animale, sciences agronomiques et de l'environnement (VAS)-Centre National de la Recherche Scientifique (CNRS)-Université Grenoble Alpes (UGA)-Institut polytechnique de Grenoble - Grenoble Institute of Technology (Grenoble INP ), Université Grenoble Alpes (UGA)-IMAG-VetAgro Sup - Institut national d'enseignement supérieur et de recherche en alimentation, santé animale, sciences agronomiques et de l'environnement (VAS)-Centre National de la Recherche Scientifique (CNRS)-Université Grenoble Alpes (UGA)-Institut polytechnique de Grenoble - Grenoble Institute of Technology (Grenoble INP ), École normale supérieure - Paris (ENS Paris), Université Paris sciences et lettres (PSL)-École normale supérieure - Paris (ENS Paris), Biologie Computationnelle et Modélisation (TIMC-BCM ), Translational Innovation in Medicine and Complexity / Recherche Translationnelle et Innovation en Médecine et Complexité - UMR 5525 (TIMC ), Université Paris sciences et lettres (PSL)-Centre National de la Recherche Scientifique (CNRS)-Institut National de la Santé et de la Recherche Médicale (INSERM), Université de Toulouse (UT)-Université de Toulouse (UT)-Centre National de la Recherche Scientifique (CNRS)-Université Toulouse III - Paul Sabatier (UT3), and Université de Toulouse (UT)-Université de Toulouse (UT)-Centre National de la Recherche Scientifique (CNRS)

Subjects
[SDV.BC.BC]Life Sciences [q-bio]/Cellular Biology/Subcellular Processes [q-bio.SC], [SDV.BBM.BM] Life Sciences [q-bio]/Biochemistry, Molecular Biology/Molecular biology, chemistry.chemical_compound, 0302 clinical medicine, Plasmid, Structural Biology, Chromosome Segregation, chromosome, Replicon, 0303 health sciences, Chromosomes, Bacterial, partition, segregation, Cell biology, [SDV.MP]Life Sciences [q-bio]/Microbiology and Parasitology, MESH: DNA, Circular, polymer unmixing, DNA, Circular, Intracellular, Plasmids, DNA, Bacterial, MESH: Chromosomes, Bacterial, signal transduction and intracellular signaling Keywords: plasmid, MESH: Biological Transport, MESH: Chromosome Segregation, MESH: Replicon, [SDV.BC]Life Sciences [q-bio]/Cellular Biology, Bacterial genome size, Biology, MESH: Enterobacteriaceae, 03 medical and health sciences, Enterobacteriaceae, trafficking, MESH: Plasmids, plasmid, [SDV.BBM] Life Sciences [q-bio]/Biochemistry, Molecular Biology, [SDV.BC.BC] Life Sciences [q-bio]/Cellular Biology/Subcellular Processes [q-bio.SC], Nucleoid, [SDV.BBM]Life Sciences [q-bio]/Biochemistry, Molecular Biology, [SDV.BC] Life Sciences [q-bio]/Cellular Biology, Molecular Biology, 030304 developmental biology, spatiotemporal organization, Chromosome, Biological Transport, [SDV.BBM.BM]Life Sciences [q-bio]/Biochemistry, Molecular Biology/Molecular biology, biochemical phenomena, metabolism, and nutrition, MESH: DNA, Bacterial, [SDV.MP.BAC]Life Sciences [q-bio]/Microbiology and Parasitology/Bacteriology, Section/Category: Sorting, chemistry, Cytoplasm, bacteria, [SDV.MP.BAC] Life Sciences [q-bio]/Microbiology and Parasitology/Bacteriology, 030217 neurology & neurosurgery, DNA
Abstract

International audience; Bacterial genomes, organized intracellularly as nucleoids, are composed of a main chromosome coexisting with different types of secondary replicons. Secondary replicons are major drivers of 16 bacterial adaptation by gene exchange. They are highly diverse in type and size, ranging from less than 2 to more than 1000 kb, and must integrate with bacterial physiology, including to the nucleoid dynamics, to limit detrimental costs leading to their counter-selection. We show that large DNA circles, whether from a natural plasmid or excised from the chromosome tend to localize in a dynamic manner in a zone separating the nucleoid from the cytoplasm at the edge of the nucleoid.This localization is in good agreement with in silico simulations of DNA circles in the nucleoid volume. Subcellular positioning systems counteract this tendency, allowing replicons to enter the nucleoid space. In enterobacteria, these systems are found in replicons above 25 kb, defining the limit with small randomly segregated plasmids. Larger replicons carry at least one of the three described family of systems, ParAB, ParRM and StbA. Replicons above 180 kb all carry a ParAB system, suggesting this system is specifically required in the cases of large replicons. Simulations demonstrated that replicon size profoundly affects localization, compaction and dynamics of DNA circles in the nucleoid volume. The present work suggests that presence of partition systems on the larger plasmids or chromids is not only due to selection for accurate segregation but also to counteract their unmixing with the chromosome and consequent exclusion from the nucleoid.

Published
2020
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24. Comprendre et inférer la transmission culturelle du succès reproducteur

Author

Guez, Jérémy, Achaz, Guillaume, Bienvenu, François, Cury, Jean, Toupance, Bruno, Heyer, Evelyne, Jay, Flora, Austerlitz, Frederic, Éco-Anthropologie (EA), Muséum national d'Histoire naturelle (MNHN)-Centre National de la Recherche Scientifique (CNRS), Laboratoire Interdisciplinaire des Sciences du Numérique (LISN), Institut National de Recherche en Informatique et en Automatique (Inria)-CentraleSupélec-Université Paris-Saclay-Centre National de la Recherche Scientifique (CNRS), Collège de France (CdF (institution)), Institute for Theoretical Studies of ETH Zürich (ETH-ITS), TAckling the Underspecified (TAU), Inria Saclay - Ile de France, Institut National de Recherche en Informatique et en Automatique (Inria)-Institut National de Recherche en Informatique et en Automatique (Inria)-Laboratoire de Recherche en Informatique (LRI), CentraleSupélec-Université Paris-Saclay-Centre National de la Recherche Scientifique (CNRS)-CentraleSupélec-Université Paris-Saclay-Centre National de la Recherche Scientifique (CNRS), Bioinformatique (LRI) (BioInfo - LRI), Laboratoire de Recherche en Informatique (LRI), and CNRS

Subjects
[SDV]Life Sciences [q-bio]
Abstract

International audience

Published
2022

27. dnadna: DEEP NEURAL ARCHITECTURES FOR DNA - A DEEP LEARNING FRAMEWORK FOR POPULATION GENETIC INFERENCE

Author

Sanchez, Théophile, Madison Bray, Erik, Jobic, Pierre, Guez, Jérémy, Letournel, Anne-Catherine, Charpiat, Guillaume, Cury, Jean, Jay, Flora, Laboratoire Interdisciplinaire des Sciences du Numérique (LISN), CentraleSupélec-Université Paris-Saclay-Centre National de la Recherche Scientifique (CNRS), Accompagnement et Soutien aux Activités de Recherche & Développement (ASARD), CentraleSupélec-Université Paris-Saclay-Centre National de la Recherche Scientifique (CNRS)-CentraleSupélec-Université Paris-Saclay-Centre National de la Recherche Scientifique (CNRS), Éco-Anthropologie (EAE), Muséum national d'Histoire naturelle (MNHN)-Centre National de la Recherche Scientifique (CNRS), TAckling the Underspecified (TAU), Inria Saclay - Ile de France, Institut National de Recherche en Informatique et en Automatique (Inria)-Institut National de Recherche en Informatique et en Automatique (Inria)-Laboratoire Interdisciplinaire des Sciences du Numérique (LISN), BioInformatique (BioInfo), and CentraleSupélec-Université Paris-Saclay-Centre National de la Recherche Scientifique (CNRS)-CentraleSupélec-Université Paris-Saclay-Centre National de la Recherche Scientifique (CNRS)-Science des Données (SDD)

Subjects
[SDV.GEN]Life Sciences [q-bio]/Genetics, [SDV.GEN.GPO]Life Sciences [q-bio]/Genetics/Populations and Evolution [q-bio.PE], deep neural networks, software, population genetics, genomic data, supervised learning, [INFO.INFO-AI]Computer Science [cs]/Artificial Intelligence [cs.AI]
Abstract

We present dnadna, a flexible python-based software for deep learning inference in population genetics. It is task-agnostic and aims at facilitating the development, reproducibility, dissemination, and reusability of neural networks designed for genetic polymorphism data. dnadna defines multiple user-friendly workflows. First, users can implement new architectures and tasks, while benefiting from dnadna input/output and other utility functions, training procedure and test environment, which not only saves time but also decreases the probability of bugs. Second, implemented networks can be re-optimized based on user-specified training sets and/or tasks. Finally, users can apply pretrained networks in order to predict evolutionary history from alternative real or simulated genetic datasets, without the need of extensive knowledge in deep learning. Thanks to dnadna, newly implemented architectures and pretrained networks are easily shareable with the community for further benchmarking or applications. dnadna comes with a peer-reviewed exchangeable neural network allowing demographic inference from SNP data, that can be used directly or retrained to solve other tasks. Toy networks are also available to ease the exploration of the software, and we expect that the range of available architectures will keep expanding thanks to contributions from the community.

Published
2021

32. Deep learning for population size history inference: Design, comparison and combination with approximate Bayesian computation.

Author

Sanchez, Théophile, Cury, Jean, Charpiat, Guillaume, and Jay, Flora

Subjects
*DEEP learning, *ARTIFICIAL neural networks, *HAPLOTYPES, *SINGLE nucleotide polymorphisms, *POPULATION genetics, *CATTLE breeds
Abstract

For the past decades, simulation‐based likelihood‐free inference methods have enabled researchers to address numerous population genetics problems. As the richness and amount of simulated and real genetic data keep increasing, the field has a strong opportunity to tackle tasks that current methods hardly solve. However, high data dimensionality forces most methods to summarize large genomic data sets into a relatively small number of handcrafted features (summary statistics). Here, we propose an alternative to summary statistics, based on the automatic extraction of relevant information using deep learning techniques. Specifically, we design artificial neural networks (ANNs) that take as input single nucleotide polymorphic sites (SNPs) found in individuals sampled from a single population and infer the past effective population size history. First, we provide guidelines to construct artificial neural networks that comply with the intrinsic properties of SNP data such as invariance to permutation of haplotypes, long scale interactions between SNPs and variable genomic length. Thanks to a Bayesian hyperparameter optimization procedure, we evaluate the performance of multiple networks and compare them to well‐established methods like Approximate Bayesian Computation (ABC). Even without the expert knowledge of summary statistics, our approach compares fairly well to an ABC approach based on handcrafted features. Furthermore, we show that combining deep learning and ABC can improve performance while taking advantage of both frameworks. Finally, we apply our approach to reconstruct the effective population size history of cattle breed populations. [ABSTRACT FROM AUTHOR]

Published
2021
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33. Intracellular positioning systems limit the entropic eviction of 1 secondary replicons toward the nucleoid edges in bacterial cells

Author

Planchenault, Charlène, Pons, Marine, Schiavon, Caroline, Siguier, Patricia, Rech, Jérôme, Guynet, Catherine, Dauverd -Girault, Julie, Cury, Jean, Rocha, Eduardo, Junier, Ivan, Cornet, François, Espéli, Olivier, Centre interdisciplinaire de recherche en biologie (CIRB), Collège de France (CdF)-Institut National de la Santé et de la Recherche Médicale (INSERM)-PSL Research University (PSL)-Centre National de la Recherche Scientifique (CNRS), Laboratoire de microbiologie et génétique moléculaires (LMGM), Université Toulouse III - Paul Sabatier (UT3), Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées-Centre National de la Recherche Scientifique (CNRS), Génomique évolutive des Microbes / Microbial Evolutionary Genomics, Centre National de la Recherche Scientifique (CNRS)-Institut Pasteur [Paris], Biologie Computationnelle et Mathématique (TIMC-IMAG-BCM), Techniques de l'Ingénierie Médicale et de la Complexité - Informatique, Mathématiques et Applications, Grenoble - UMR 5525 (TIMC-IMAG), Université Joseph Fourier - Grenoble 1 (UJF)-Institut polytechnique de Grenoble - Grenoble Institute of Technology (Grenoble INP)-IMAG-Centre National de la Recherche Scientifique (CNRS)-Université Grenoble Alpes (UGA)-Université Joseph Fourier - Grenoble 1 (UJF)-Institut polytechnique de Grenoble - Grenoble Institute of Technology (Grenoble INP)-IMAG-Centre National de la Recherche Scientifique (CNRS)-Université Grenoble Alpes (UGA), Institut Jean Roget, This work as funded by ANR ANR-14-CE10-0007-01 to OE, FC and ER by the CNRS PICS initiative to OE and IJ and by the Foundation ARC (PJA 20171206119) to OE, and ANR-14-CE10-0007,MAGISBAC,Génèse et maintenance des chromosomes secondaire bactériens(2014)

Subjects
bacteria, [SDV.BBM]Life Sciences [q-bio]/Biochemistry, Molecular Biology, [SDV.BBM.BM]Life Sciences [q-bio]/Biochemistry, Molecular Biology/Molecular biology, [SDV.BC]Life Sciences [q-bio]/Cellular Biology, [SDV.BC.BC]Life Sciences [q-bio]/Cellular Biology/Subcellular Processes [q-bio.SC], biochemical phenomena, metabolism, and nutrition, [SDV.MP.BAC]Life Sciences [q-bio]/Microbiology and Parasitology/Bacteriology
Abstract

International audience; Bacterial genomes, organized intracellularly as nucleoids, are composed of a main chromosome coexisting with different types of secondary replicons. Secondary replicons are major drivers of 16 bacterial adaptation by gene exchange. They are highly diverse in type and size, ranging from less than 2 to more than 1000 kb, and must integrate with bacterial physiology, including to the nucleoid dynamics, to limit detrimental costs leading to their counter-selection. We show that large DNA circles, whether from a natural plasmid or excised from the chromosome tend to localize in a dynamic manner in a zone separating the nucleoid from the cytoplasm at the edge of the nucleoid.This localization is in good agreement with in silico simulations of DNA circles in the nucleoid volume. Subcellular positioning systems counteract this tendency, allowing replicons to enter the nucleoid space. In enterobacteria, these systems are found in replicons above 25 kb, defining the limit with small randomly segregated plasmids. Larger replicons carry at least one of the three described family of systems, ParAB, ParRM and StbA. Replicons above 180 kb all carry a ParAB system, suggesting this system is specifically required in the cases of large replicons. Simulations demonstrated that replicon size profoundly affects localization, compaction and dynamics of DNA circles in the nucleoid volume. The present work suggests that presence of partition systems on the larger plasmids or chromids is not only due to selection for accurate segregation but also to counteract their unmixing with the chromosome and consequent exclusion from the nucleoid.

Published
2019
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34. Evolutionary genomics of conjugative elements and integrons

Author

Cury, Jean, Génomique évolutive des Microbes / Microbial Evolutionary Genomics, Institut Pasteur [Paris] (IP)-Centre National de la Recherche Scientifique (CNRS), Université Sorbonne Paris Cité, Eduardo Pimentel Cachapuz Rocha, and Institut Pasteur [Paris]-Centre National de la Recherche Scientifique (CNRS)

Subjects
Bioinformatique, Bioinformatics, structural biology and genomics, biologie structurale et génomique, [SDV.MHEP]Life Sciences [q-bio]/Human health and pathology
Abstract

No abstract; Pas de résumé

Published
2017

35. Génomique évolutive des éléments conjugués et des intégrons

Author

Cury, Jean, Génomique évolutive des Microbes / Microbial Evolutionary Genomics, Institut Pasteur [Paris]-Centre National de la Recherche Scientifique (CNRS), Université Sorbonne Paris Cité, and Eduardo Pimentel Cachapuz Rocha

Subjects
Bioinformatique, Bioinformatics, structural biology and genomics, biologie structurale et génomique, [SDV.MHEP]Life Sciences [q-bio]/Human health and pathology
Abstract

No abstract; Pas de résumé

Published
2017

36. Differences in Integron Cassette Excision Dynamics Shape a Trade-Off between Evolvability and Genetic Capacitance

Author

Loot, Céline, Nivina, Aleksandra, Cury, Jean, Escudero, José, Ducos-Galand, Magaly, Bikard, David, Rocha, Eduardo, Mazel, Didier, Plasticité du Génome Bactérien - Bacterial Genome Plasticity (PGB), Institut Pasteur [Paris]-Centre National de la Recherche Scientifique (CNRS), Université Paris Descartes - Paris 5 (UPD5), Génomique évolutive des Microbes / Microbial Evolutionary Genomics, This work was supported by the Institut Pasteur, the Centre National de la Recherche Scientifique, Fondation pour la Recherche Médicale (project DBF20160635736), the French Government Investissement d’Avenir program Laboratoire d’Excellence 'Integrative Biology of Emerging Infectious Diseases' (ANR-10-LABX-62-IBEID), the French National Research Agency (ANR-12-BLAN-DynamINT), the European Union Seventh Framework Program (FP7-HEALTH-2011-single-stage), the 'Evolution and Transfer Of Antibiotic Resistance' (EvoTAR), Paris Descartes University—Sorbonne Paris Cité, Fondation pour la Recherche Médicale (FDT20150532465) and École Doctorale Frontières du Vivant (FdV)—Programme Bettencourt (to A.N.), Marie Curie Intra-European Fellowship for Career Development (FP-7-PEOPLE-2011-IEF, ICADIGE) (to J.A.E.), and European Research Council grant (EVOMOBILOME grant 281605) (to E.P.C.R. and J.C.)., We thank Claire Vit for helpful discussions and Sebastian Aguilar Pierlé for reading the manuscript., ANR-10-LABX-0062,IBEID,Integrative Biology of Emerging Infectious Diseases(2010), ANR-12-BSV3-0015,DynamINT,Recombination des cassettes d'intégron: dynamique in vivo et in vitro(2012), European Project: 282004,EC:FP7:HEALTH,FP7-HEALTH-2011-single-stage,EVOTAR(2011), European Project: 303022,EC:FP7:PEOPLE,FP7-PEOPLE-2011-IEF,ICADIGE(2012), European Project: 281605,EC:FP7:ERC,ERC-2011-StG_20101109,EVOMOBILOME(2012), Institut Pasteur [Paris] (IP)-Centre National de la Recherche Scientifique (CNRS), Plasticité du Génome Bactérien, Centre National de la Recherche Scientifique (CNRS)-Institut Pasteur [Paris], and ANR-10-LABX-62-IBEID,IBEID,Laboratoire d'Excellence 'Integrative Biology of Emerging Infectious Diseases'(2010)

Subjects
Recombination, Genetic, replication, integron, Bacteria, MESH: Interspersed Repetitive Sequence, MESH: Adaptation, Biological, [SDV]Life Sciences [q-bio], Adaptation, Biological, site-specific recombination, Computational Biology, attC sites, Microbiology, QR1-502, Integrons, MESH: Integrons, Evolution, Molecular, Interspersed Repetitive Sequences, MESH: Bacteria, MESH: Recombination, Genetic, cassette dynamics, MESH: Evolution, Molecular, Research Article, MESH: Computational Biology
Abstract

Integrons ensure a rapid and “on demand” response to environmental stresses driving bacterial adaptation. They are able to capture, store, and reorder functional gene cassettes due to site-specific recombination catalyzed by their integrase. Integrons can be either sedentary and chromosomally located or mobile when they are associated with transposons and plasmids. They are respectively called sedentary chromosomal integrons (SCIs) and mobile integrons (MIs). MIs are key players in the dissemination of antibiotic resistance genes. Here, we used in silico and in vivo approaches to study cassette excision dynamics in MIs and SCIs. We show that the orientation of cassette arrays relative to replication influences attC site folding and cassette excision by placing the recombinogenic strands of attC sites on either the leading or lagging strand template. We also demonstrate that stability of attC sites and their propensity to form recombinogenic structures also regulate cassette excision. We observe that cassette excision dynamics driven by these factors differ between MIs and SCIs. Cassettes with high excision rates are more commonly found on MIs, which favors their dissemination relative to SCIs. This is especially true for SCIs carried in the Vibrio genus, where maintenance of large cassette arrays and vertical transmission are crucial to serve as a reservoir of adaptive functions. These results expand the repertoire of known processes regulating integron recombination that were previously established and demonstrate that, in terms of cassette dynamics, a subtle trade-off between evolvability and genetic capacitance has been established in bacteria., IMPORTANCE The integron system confers upon bacteria a rapid adaptation capability in changing environments. Specifically, integrons are involved in the continuous emergence of bacteria resistant to almost all antibiotic treatments. The international situation is critical, and in 2050, the annual number of deaths caused by multiresistant bacteria could reach 10 million, exceeding the incidence of deaths related to cancer. It is crucial to increase our understanding of antibiotic resistance dissemination and therefore integron recombination dynamics to find new approaches to cope with the worldwide problem of multiresistance. Here, we studied the dynamics of recombination and dissemination of gene encoding cassettes carried on integrons. By combining in silico and in vivo analyses, we show that cassette excision is highly regulated by replication and by the intrinsic properties of cassette recombination sites. We also demonstrated differences in the dynamics of cassette recombination between mobile and sedentary chromosomal integrons (MIs and SCIs). For MIs, a high cassette recombination rate is favored and timed to conditions when generating diversity (upon which selection can act) allows for a rapid response to environmental conditions and stresses. In contrast, for SCIs, cassette excisions are less frequent, limiting cassette loss and ensuring a large pool of cassettes. We therefore confirm a role of SCIs as reservoirs of adaptive functions and demonstrate that the remarkable adaptive success of integron recombination system is due to its intricate regulation.

Published
2017
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38. Host range and genetic plasticity explain the coexistence of integrative and extrachromosomal mobile genetic element

Author

Agence Nationale de la Recherche (France), European Research Council, European Commission, Ministerio de Economía y Competitividad (España), Cury, Jean, Oliveira, Pedro H., Cruz, Fernando de la, Rocha, Eduardo P. C., Agence Nationale de la Recherche (France), European Research Council, European Commission, Ministerio de Economía y Competitividad (España), Cury, Jean, Oliveira, Pedro H., Cruz, Fernando de la, and Rocha, Eduardo P. C.

Abstract

Self-transmissible mobile genetic elements drive horizontal gene transfer between prokaryotes. Some of these elements integrate in the chromosome, whereas others replicate autonomously as plasmids. Recent works showed the existence of few differences, and occasional interconversion, between the two types of elements. Here, we enquired on why evolutionary processes have maintained the two types of mobile genetic elements by comparing integrative and conjugative elements (ICE) with extrachromosomal ones (conjugative plasmids) of the highly abundant MPFT conjugative type. We observed that plasmids encode more replicases, partition systems, and antibiotic resistance genes, whereas ICEs encode more integrases and metabolism-associated genes. ICEs and plasmids have similar average sizes, but plasmids are much more variable, have more DNA repeats, and exchange genes more frequently. On the other hand, we found that ICEs are more frequently transferred between distant taxa. We propose a model where the different genetic plasticity and amplitude of host range between elements explain the co-occurrence of integrative and extrachromosomal elements in microbial populations. In particular, the conversion from ICE to plasmid allows ICE to be more plastic, while the conversion from plasmid to ICE allows the expansion of the element’s host range.

Published
2018

40. What does mining ICE in bacterial genomes reveal?

Author

Cury, Jean, Abby, Sophie S., Guglielmini, Julien, Garcillán-Barcia, M. Pilar, Cruz, Fernando de la, Touchon, Marie, and Rocha, Eduardo P. C.

Abstract

Resumen del trabajo presentado al Plasmid Biology Meeting, celebrado en Cambridge (UK) del 18 al 23 de septiembre de 2016., Conjugative elements play a major role in bacterial evolution. They have been widely studied when associated with plasmids, however, the role and importance of Integrative and Conjugative Elements (ICE) remain less clear. Yet, it has been shown that ICEs are more abundant than conjugative plasmids in bacterial genomes. Using comparative genomics, we analyzed about 200 ICEs, which we delimited precisely. This unique dataset allowed us to have a more general picture of ICEs. We could outline for the first time their general organization and their relation to their host’s genome. More importantly, we infer some evolutionary properties of ICEs. Indeed we look for a wide range of mobile genetic element associated functions like restriction modification systems, integrons, toxin-antitoxins, entry-exclusion systems, among other functions. This accurate annotation allowed us to better understand ICE’s relationship to its host. This provides quantitative new information on ICEs and allows us to better understand their broader role in the evolution of bacteria.

Published
2016

42. Evolutionary dynamics and genomic features of the Elizabethkingia anophelis 2015 to 2016 Wisconsin outbreak strain

Author

Perrin, Amandine, primary, Larsonneur, Elise, additional, Nicholson, Ainsley C., additional, Edwards, David J., additional, Gundlach, Kristin M., additional, Whitney, Anne M., additional, Gulvik, Christopher A., additional, Bell, Melissa E., additional, Rendueles, Olaya, additional, Cury, Jean, additional, Hugon, Perrine, additional, Clermont, Dominique, additional, Enouf, Vincent, additional, Loparev, Vladimir, additional, Juieng, Phalasy, additional, Monson, Timothy, additional, Warshauer, David, additional, Elbadawi, Lina I., additional, Walters, Maroya Spalding, additional, Crist, Matthew B., additional, Noble-Wang, Judith, additional, Borlaug, Gwen, additional, Rocha, Eduardo P. C., additional, Criscuolo, Alexis, additional, Touchon, Marie, additional, Davis, Jeffrey P., additional, Holt, Kathryn E., additional, McQuiston, John R., additional, and Brisse, Sylvain, additional

Published
2017
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47. The Genomic Diversification of the Whole Acinetobacter Genus: Origins, Mechanisms, and Consequences

Author

Touchon, Marie, primary, Cury, Jean, additional, Yoon, Eun-Jeong, additional, Krizova, Lenka, additional, Cerqueira, Gustavo C., additional, Murphy, Cheryl, additional, Feldgarden, Michael, additional, Wortman, Jennifer, additional, Clermont, Dominique, additional, Lambert, Thierry, additional, Grillot-Courvalin, Catherine, additional, Nemec, Alexandr, additional, Courvalin, Patrice, additional, and Rocha, Eduardo P.C., additional

Published
2014
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48. A simple, reproducible and cost-effective procedure to analyse gut phageome: from phage isolation to bioinformatic approach.

Author

d'Humières, Camille, Touchon, Marie, Dion, Sara, Cury, Jean, Ghozlane, Amine, Garcia-Garcera, Marc, Bouchier, Christiane, Ma, Laurence, Denamur, Erick, and P.C.Rocha, Eduardo

Subjects
ENTEROTYPES, BACTERIOPHAGES, GENOMES, POLYETHYLENE glycol, GENE amplification, TAXONOMY
Abstract

The microbiota of the human gut is a complex and rich community where bacteria and their viruses, the bacteriophages, are dominant. There are few studies on the phage community and no clear standard for isolating them, sequencing and analysing their genomes. Since this makes comparisons between studies difficult, we aimed at defining an easy, low-cost, and reproducible methodology. We analysed five different techniques to isolate phages from human adult faeces and developed an approach to analyse their genomes in order to quantify contamination and classify phage contigs in terms of taxonomy and lifestyle. We chose the polyethylene glycol concentration method to isolate phages because of its simplicity, low cost, reproducibility, and of the high number and diversity of phage sequences that we obtained. We also tested the reproducibility of this method with multiple displacement amplification (MDA) and showed that MDA severely decreases the phage genetic diversity of the samples and the reproducibility of the method. Lastly, we studied the influence of sequencing depth on the analysis of phage diversity and observed the beginning of a plateau for phage contigs at 20,000,000 reads. This work contributes to the development of methods for the isolation of phages in faeces and for their comparative analysis. [ABSTRACT FROM AUTHOR]

Published
2019
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49. Exploring the diversity of anti-defense systems across prokaryotes, phages and mobile genetic elements.

Author

Tesson F, Huiting E, Wei L, Ren J, Johnson M, Planel R, Cury J, Feng Y, Bondy-Denomy J, and Bernheim A

Abstract

The co-evolution of prokaryotes, phages and mobile genetic elements (MGEs) has driven the diversification of defense and anti-defense systems alike. Anti-defense proteins have diverse functional domains, sequences and are typically small, creating a challenge to detect anti-defense homologs across prokaryotic and phage genomes. To date, no tools comprehensively annotate anti-defense proteins within a desired sequence. Here, we developed 'AntiDefenseFinder'-a free open-source tool and web service that detects 156 anti-defense systems of one or more proteins in any genomic sequence. Using this dataset, we identified 47 981 anti-defense systems distributed across prokaryotes and their viruses. We found that some genes co-localize in 'anti-defense islands', including Escherichia coli T4 and Lambda phages, although many appear standalone. Eighty-nine per cent anti-defense systems localize only or preferentially in MGE. However, >80% of anti-Pycsar protein 1 (Apyc1) resides in nonmobile regions of bacterial genomes. Evolutionary analysis and biochemical experiments revealed that Apyc1 likely originated in bacteria to regulate cyclic nucleotide (cNMP) signaling, but phage co-opted Apyc1 to overcome cNMP-utilizing defenses. With the AntiDefenseFinder tool, we hope to facilitate the identification of the full repertoire of anti-defense systems in MGEs, the discovery of new protein functions and a deeper understanding of host-pathogen arms race., (© The Author(s) 2024. Published by Oxford University Press on behalf of Nucleic Acids Research.)

Published
2024
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50. Evolutionary origins of archaeal and eukaryotic RNA-guided RNA modification in bacterial IS110 transposons.

Author

Vaysset H, Meers C, Cury J, Bernheim A, and Sternberg SH

Abstract

Transposase genes are ubiquitous in all domains of life and provide a rich reservoir for the evolution of novel protein functions. Here we report deep evolutionary links between bacterial IS110 transposases, which catalyze RNA-guided DNA recombination using bridge RNAs, and archaeal/eukaryotic Nop5-family proteins, which promote RNA-guided RNA 2'-O-methylation using C/D-box snoRNAs. Based on conservation in the protein primary sequence, domain architecture, and three-dimensional structure, as well as common architectural features of the non-coding RNA components, we propose that programmable RNA modification emerged via exaptation of components derived from IS110-like transposons. Alongside recent studies highlighting the origins of CRISPR-Cas9 and Cas12 in IS605-family transposons, these findings underscore how recurrent domestication events of transposable elements gave rise to complex RNA-guided biological mechanisms., Competing Interests: COMPETING INTERESTS The authors declare no competing interests.

Published
2024
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