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2. A virally encoded tRNA neutralizes the PARIS antiviral defence system

Author

Burman, Nathaniel, Belukhina, Svetlana, Depardieu, Florence, Wilkinson, Royce A., Skutel, Mikhail, Santiago-Frangos, Andrew, Graham, Ava B., Livenskyi, Alexei, Chechenina, Anna, Morozova, Natalia, Zahl, Trevor, Henriques, William S., Buyukyoruk, Murat, Rouillon, Christophe, Saudemont, Baptiste, Shyrokova, Lena, Kurata, Tatsuaki, Hauryliuk, Vasili, Severinov, Konstantin, Groseille, Justine, Thierry, Agnès, Koszul, Romain, Tesson, Florian, Bernheim, Aude, Bikard, David, Wiedenheft, Blake, and Isaev, Artem

Published
2024
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10. 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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12. Viral proteins activate PARIS-mediated tRNA degradation and viral tRNAs rescue infection

Author

Burman, Nathaniel, primary, Belukhina, Svetlana, additional, Depardieu, Florence, additional, Wilkinson, Royce A., additional, Skutel, Mikhail, additional, Santiago-Frangos, Andrew, additional, Graham, Ava B., additional, Livenskyi, Alexei, additional, Chechenina, Anna, additional, Morozova, Natalia, additional, Zahl, Trevor, additional, Henriques, William S., additional, Buyukyoruk, Murat, additional, Rouillon, Christophe, additional, Shyrokova, Lena, additional, Kurata, Tatsuaki, additional, Hauryliuk, Vasili, additional, Severinov, Konstantin, additional, Groseille, Justine, additional, Thierry, Agnès, additional, Koszul, Romain, additional, Tesson, Florian, additional, Bernheim, Aude, additional, Bikard, David, additional, Wiedenheft, Blake, additional, and Isaev, Artem, additional

Published
2024
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16. Predicting phage-bacteria interactions at the strain level from genomes

Author

Gaborieau, Baptiste, primary, Vaysset, Hugo, additional, Tesson, Florian, additional, Charachon, Ines, additional, Dib, Nicolas, additional, Bernier, Juliette, additional, Dequidt, Tanguy, additional, Georjon, Heloise, additional, Clermont, Olivier, additional, Hersen, Pascal, additional, Debarbieux, Laurent, additional, Ricard, Jean-Damien, additional, Denamur, Erick, additional, and Bernheim, Aude, additional

Published
2023
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23. A widespread family of phage-inducible chromosomal islands only steals bacteriophage tails to spread in nature

Author

Rousset, François, Depardieu, Florence, Miele, Solange, Dowding, Julien, Laval, Anne-Laure, Lieberman, Erica, Garry, Daniel, Rocha, Eduardo P.C., Bernheim, Aude, Bikard, David, Génomique évolutive des Microbes / Microbial Evolutionary Genomics, Institut Pasteur [Paris] (IP)-Centre National de la Recherche Scientifique (CNRS)-Université Paris Cité (UPCité), This work was supported by grants MR/M003876/1, MR/V000772/1, and MR/S00940X/1 from the Medical Research Council (UK), BB/N002873/1, BB/V002376/1, BB/V009583/1, and BB/S003835/1 from the Biotechnology and Biological Sciences Research Council (BBSRC, UK), ERC-ADG-2014 Proposal no. 670932 Dut-signal (from EU), and Wellcome Trust 201531/Z/16/Z to J.R.P., and grants INCEPTION project (PIA/ANR-16-CONV-0005), Equipe FRM (Fondation pour la Recherche Médicale): EQU201903007835, Laboratoire d’Excellence IBEID Integrative Biology of Emerging Infectious Diseases (ANR-10-LABX-62-IBEID), and SALMOPROPHAGE ANR-16-CE16-0029 to E.P.C.R. L.M.-R. was the recipient of a Spanish postdoctoral fellowship from the Fundación Ramón Areces (2018–2020). A.F.-S. is the recipient of a fellowship from Imperial College., ANR-16-CONV-0005,INCEPTION,Institut Convergences pour l'étude de l'Emergence des Pathologies au Travers des Individus et des populatiONs(2016), ANR-10-LABX-0062,IBEID,Integrative Biology of Emerging Infectious Diseases(2010), ANR-16-CE12-0029,Salmo_prophages,Co-évolution des génomes bactériens et de leurs prophages: cooptation des prophages et conversion lysogenique chez Salmonella(2016), European Project: 670932,H2020,ERC-2014-ADG,DUT-signal(2015), University of Glasgow, King Saud Bin Abdulaziz University for Health Sciences [Riyadh] (KSAU-HS), Imperial College London, Institut Pasteur [Paris]-Centre National de la Recherche Scientifique (CNRS)-Université Paris Cité (UPCité), National University of Singapore (NUS), This work was supported by grants MR/M003876/1, MR/V000772/1 and MR/S00940X/1 from the Medical Research Council (UK), BB/N002873/1, BB/V002376/1 and BB/S003835/1 from the Biotechnology and Biological Sciences Research Council (BBSRC, UK), ERC-ADG-2014 Proposal n° 670932 Dut-signal (from EU), and Wellcome Trust 201531/Z/16/Z to JRP, and grants INCEPTION project (PIA/ANR-16-CONV-0005), Equipe FRM (Fondation pour la Recherche Médicale): EQU201903007835, Laboratoire d’Excellence IBEID Integrative Biology of Emerging Infectious Diseases [ANR-10-LABX-62-IBEID], and SALMOPROPHAGE ANR-16-CE16-0029 to EPCR., and ANR-05-GANI-0001,GenOvul,Exploitation de la variabilité génétique intra et inter-espèces pour l'étude du déterminisme génétique du taux d'ovulation(2005)

Subjects
small capsid formation, [SDV.BID.EVO]Life Sciences [q-bio]/Biodiversity/Populations and Evolution [q-bio.PE], [SDV]Life Sciences [q-bio], packaging, [SDV.BID.SPT]Life Sciences [q-bio]/Biodiversity/Systematics, Phylogenetics and taxonomy, [SDV.MP.BAC]Life Sciences [q-bio]/Microbiology and Parasitology/Bacteriology, Microbiology, tail, bacteriophage, Virology, Parasitology, convergent evolution, pathogenicity islands, gene transfer, PICI
Abstract

Phage satellites interfere with helper phage packaging through the production of small-capsids, where only satellites can be packaged. So far, in all the analysed systems, the satellite-sized capsids are composed of phage proteins. Here we report the first demonstration that a family of phage-inducible chromosomal island (PICIs), a type of satellites, encodes all the proteins required for both the production of the small-sized capsids and the exclusive packaging of the PICIs into these capsids. Therefore, this new family, that we have named cf-PICIs (capsid forming PICIs), only requires phage tails to generate infective PICI particles. Remarkably, the representative cf-PICI reproduces without cost for their helper phages, suggesting that the relationship between these elements is not parasitic but commensalistic. Finally, our phylogenomic studies indicate that cf-PICIs are present both in Gram-positive and Gram-negative bacteria and have evolved at least three times independently to spread widely into the satellite universe.

Published
2022
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24. An expanded arsenal of immune systems that protect bacteria from phages

Author

Millman, Adi, primary, Melamed, Sarah, additional, Leavitt, Azita, additional, Doron, Shany, additional, Bernheim, Aude, additional, Hör, Jens, additional, Garb, Jeremy, additional, Bechon, Nathalie, additional, Brandis, Alexander, additional, Lopatina, Anna, additional, Ofir, Gal, additional, Hochhauser, Dina, additional, Stokar-Avihail, Avigail, additional, Tal, Nitzan, additional, Sharir, Saar, additional, Voichek, Maya, additional, Erez, Zohar, additional, Ferrer, Jose Lorenzo M., additional, Dar, Daniel, additional, Kacen, Assaf, additional, Amitai, Gil, additional, and Sorek, Rotem, additional

Published
2022
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25. Phages and their satellites encode hotspots of antiviral systems

Author

Rousset, François, primary, Depardieu, Florence, additional, Miele, Solange, additional, Dowding, Julien, additional, Laval, Anne-Laure, additional, Lieberman, Erica, additional, Garry, Daniel, additional, Rocha, Eduardo P.C., additional, Bernheim, Aude, additional, and Bikard, David, additional

Published
2022
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31. Bacterial Retrons Function In Anti-Phage Defense

Author

Millman, Adi, primary, Bernheim, Aude, additional, Stokar-Avihail, Avigail, additional, Fedorenko, Taya, additional, Voichek, Maya, additional, Leavitt, Azita, additional, Oppenheimer-Shaanan, Yaara, additional, and Sorek, Rotem, additional

Published
2020
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32. Prokaryotic viperins produce diverse antiviral molecules

Author

Bernheim, Aude, primary, Millman, Adi, additional, Ofir, Gal, additional, Meitav, Gilad, additional, Avraham, Carmel, additional, Shomar, Helena, additional, Rosenberg, Masha M., additional, Tal, Nir, additional, Melamed, Sarah, additional, Amitai, Gil, additional, and Sorek, Rotem, additional

Published
2020
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34. CRISPRCasFinder, an update of CRISRFinder, includes a portable version, enhanced performance and integrates search for Cas proteins

Author

Couvin, David, Bernheim, Aude, Toffano-Nioche, Claire, Touchon, Marie, Michalik, Juraj, Néron, Bertrand, Rocha, Eduardo P C, Vergnaud, Gilles, Gautheret, Daniel, Pourcel, Christine, Institut de Biologie Intégrative de la Cellule (I2BC), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Université Paris-Saclay-Centre National de la Recherche Scientifique (CNRS), Génomique évolutive des Microbes / Microbial Evolutionary Genomics, Institut Pasteur [Paris]-Centre National de la Recherche Scientifique (CNRS), Centre de Recherche en Informatique, Signal et Automatique de Lille - UMR 9189 (CRIStAL), Centrale Lille-Université de Lille-Centre National de la Recherche Scientifique (CNRS), Centre de Bioinformatique, Biostatistique et Biologie Intégrative (C3BI), Institut Français de Bioinformatique (IFB) [ANR–11–INSB–0013, in part], European Defense Agency Research and Technology project JIP-ICET2 A-1341-RT-GP, called Bioforensics for Biodefence (B2-forensics). Funding for open access charge: ANR Grant., We thank Stefan Kurtz for making Vmatch an open source project without licensing requirements. We thank Christine Drevet, Maud Pupin, Luis M. Rodriguez and Lee S. Katz for their help in the previous developments of CRISPRFinder. We are particularly grateful to the SICS team (I2BC), and especially to Cyrille Petat and Pierre-Albert Charbit for the development of the web application. We also acknowledge the constant help and support by Arnaud Martel and Anne-Pascale Jaudier. We thank Mélina Gallopin, David Christiany, Nicolas Villeriot, Nicolas Maillet, Fabrice Leclerc and Emilie Drouineau for helpful comments and for testing the standalone software, ANR-11-INBS-0013,IFB (ex Renabi-IFB),Institut français de bioinformatique(2011), and Institut Pasteur [Paris] (IP)-Centre National de la Recherche Scientifique (CNRS)

Subjects
Internet, [SDV.GEN.GPO]Life Sciences [q-bio]/Genetics/Populations and Evolution [q-bio.PE], [SDV.BBM.GTP]Life Sciences [q-bio]/Biochemistry, Molecular Biology/Genomics [q-bio.GN], [SDV.BID.EVO]Life Sciences [q-bio]/Biodiversity/Populations and Evolution [q-bio.PE], Web Server Issue, CRISPR-Associated Proteins, Clustered Regularly Interspaced Short Palindromic Repeats, CRISPR-Cas Systems, [INFO.INFO-BI]Computer Science [cs]/Bioinformatics [q-bio.QM], [SDV.BIBS]Life Sciences [q-bio]/Quantitative Methods [q-bio.QM], [SDV.MP.BAC]Life Sciences [q-bio]/Microbiology and Parasitology/Bacteriology, Software
Abstract

International audience; CRISPR (clustered regularly interspaced short palin-dromic repeats) arrays and their associated (Cas) proteins confer bacteria and archaea adaptive immunity against exogenous mobile genetic elements, such as phages or plasmids. CRISPRCasFinder allows the identification of both CRISPR arrays and Cas proteins. The program includes: (i) an improved CRISPR array detection tool facilitating expert validation based on a rating system, (ii) prediction of CRISPR orientation and (iii) a Cas protein detection and typing tool updated to match the latest classification scheme of these systems. CRISPRCasFinder can either be used online or as a standalone tool compatible with Linux operating system. All third-party software packages employed by the program are freely available. CRISPRCasFinder is available at https://crisprcas.i2bc.paris-saclay.fr.

Published
2018
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41. La distribution des systèmes CRISPR-Cas est affectée par les interactions avec les voies de réparation de l'ADN

Author

Bernheim, Aude, Biologie de Synthèse - Synthetic biology, Institut Pasteur [Paris], Université Sorbonne Paris Cité, Eduardo Pimentel Cachapuz Rocha, David Bikard, Génomique évolutive des Microbes / Microbial Evolutionary Genomics, Institut Pasteur [Paris] (IP)-Centre National de la Recherche Scientifique (CNRS)-Université Paris Cité (UPCité), Université Paris Cité (UPCité)-Microbiologie Intégrative et Moléculaire (UMR6047), Institut Pasteur [Paris] (IP)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS)-Institut Pasteur [Paris] (IP)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS), Université Paris Descartes, Eduardo ROCHA, and Marie Touchon

Subjects
[SDV.GEN]Life Sciences [q-bio]/Genetics, Evolution, [SDV]Life Sciences [q-bio], Systèmes de défense, Defense systems, Immunity, CRISPR Cas, DNA repair, Évolution, Réparation de l’ADN, [SDV.MP]Life Sciences [q-bio]/Microbiology and Parasitology, CRISPR, Phages, Immunité, CRISPR-Cas
Abstract

CRISPR-Cas systems confer bacteria and archea an adaptative immunity against phages and other invading genetic elements playing an important role in bacterial evolution. Only 47% of bacterial genomes harbor a CRISPR-Cas system despite their high rate of horizontal transfer. Hypothesis such as the cost of autoimmu- nity or the trade off between a constitutive or an inducible defense system have been put forward to explain this paradox. I propose that the genetic background plays an important role in the process of maintaining a CRISPR-Cas system af- ter its transfer. More precisely I hypothesized that CRISPR-Cas systems interact with DNA repair pathways. To test this idea, we detected DNA repair pathways and CRISPR-Cas systems in bacterial genomes and studied their co-occurences. We report both positive and negative associations that we interpret as poten- tial antagonistic or synergistic interactions. We then focused on one interaction to validate our result experimentally and explored molecular mechanisms behind those interactions. My findings give insights on the complex interactions between CRISPR-Cas systems and DNA repair mechanisms in bacteria and provide a first example on the necessity of accommodation of CRISPR-Cas systems to a specific genetic context to be selected and maintained in bacterial genomes.; Les systèmes CRISPR-Cas confèrent aux bactéries une immunité adaptative contre les éléments génétiques mobiles jouant ainsi un rôle important dans l’évolution bactérienne. Cependant, moins de la moitié des génomes bactériens encodent des systèmes CRISPR-Cas ; cela, malgré la protection qu’ils confèrent et leur haut taux de transfert horizontal. Des hypothèses telles que le coût des phénomènes d’auto-immunité ou de posséder des défenses adaptatives plutôt qu’innées ont été mises en avant pour expliquer ce paradoxe. Je propose une nouvelle hypothèse complémentaire : le contexte génétique jouerait un rôle important dans la fixation d’un système CRISPR-Cas après son transfert. Plus précisément, j’ai étudié comment les interactions entre les systèmes de réparation de l’ADN et les CRISPR-Cas influencent la distribution de ces derniers. Pour cela, j’ai d’abord examiné finement la distribution des systèmes CRISPR-Cas dans les génomes bactériens. J’ai ensuite analysé les co-occurences des systèmes de réparation de l’ADN et des CRISPR-Cas et démontré l’existence d’associations positives et négatives entre eux. Enfin, je me suis concentrée sur une des associations négatives découvertes pour valider mes prédictions expérimentalement et comprendre les mécanismes moléculaires sous-jacents. Mes travaux permettent de mieux comprendre les interactions complexes entre systèmes de réparation de l’ADN et CRISPR-Cas et démontrent la nécessite d’accommodation des CRISPR-Cas à un contexte génétique pour être sélectionnés et maintenus dans les génomes bactériens.

Published
2017

42. The distribution of CRISPR-Cas systems is affected by interactions with DNA repair pathways

Author

Bernheim, Aude, Biologie de Synthèse - Synthetic biology, Institut Pasteur [Paris], Université Sorbonne Paris Cité, Eduardo Pimentel Cachapuz Rocha, David Bikard, and Institut Pasteur [Paris] (IP)

Subjects
[SDV.GEN]Life Sciences [q-bio]/Genetics, Evolution, CRISPR, Systèmes de défense, Defense systems, Phages, Immunity, Immunité, DNA repair, Évolution, CRISPR-Cas, Réparation de l’ADN
Abstract

CRISPR-Cas systems confer bacteria and archea an adaptative immunity against phages and other invading genetic elements playing an important role in bacterial evolution. Only 47% of bacterial genomes harbor a CRISPR-Cas system despite their high rate of horizontal transfer. Hypothesis such as the cost of autoimmu- nity or the trade off between a constitutive or an inducible defense system have been put forward to explain this paradox. I propose that the genetic background plays an important role in the process of maintaining a CRISPR-Cas system af- ter its transfer. More precisely I hypothesized that CRISPR-Cas systems interact with DNA repair pathways. To test this idea, we detected DNA repair pathways and CRISPR-Cas systems in bacterial genomes and studied their co-occurences. We report both positive and negative associations that we interpret as poten- tial antagonistic or synergistic interactions. We then focused on one interaction to validate our result experimentally and explored molecular mechanisms behind those interactions. My findings give insights on the complex interactions between CRISPR-Cas systems and DNA repair mechanisms in bacteria and provide a first example on the necessity of accommodation of CRISPR-Cas systems to a specific genetic context to be selected and maintained in bacterial genomes.; Les systèmes CRISPR-Cas confèrent aux bactéries une immunité adaptative contre les éléments génétiques mobiles jouant ainsi un rôle important dans l’évolution bactérienne. Cependant, moins de la moitié des génomes bactériens encodent des systèmes CRISPR-Cas ; cela, malgré la protection qu’ils confèrent et leur haut taux de transfert horizontal. Des hypothèses telles que le coût des phénomènes d’auto-immunité ou de posséder des défenses adaptatives plutôt qu’innées ont été mises en avant pour expliquer ce paradoxe. Je propose une nouvelle hypothèse complémentaire : le contexte génétique jouerait un rôle important dans la fixation d’un système CRISPR-Cas après son transfert. Plus précisément, j’ai étudié comment les interactions entre les systèmes de réparation de l’ADN et les CRISPR-Cas influencent la distribution de ces derniers. Pour cela, j’ai d’abord examiné finement la distribution des systèmes CRISPR-Cas dans les génomes bactériens. J’ai ensuite analysé les co-occurences des systèmes de réparation de l’ADN et des CRISPR-Cas et démontré l’existence d’associations positives et négatives entre eux. Enfin, je me suis concentrée sur une des associations négatives découvertes pour valider mes prédictions expérimentalement et comprendre les mécanismes moléculaires sous-jacents. Mes travaux permettent de mieux comprendre les interactions complexes entre systèmes de réparation de l’ADN et CRISPR-Cas et démontrent la nécessite d’accommodation des CRISPR-Cas à un contexte génétique pour être sélectionnés et maintenus dans les génomes bactériens.

Published
2017

47. A matter of background: DNA repair pathways as a possible cause for the sparse distribution of CRISPR-Cas systems in bacteria.

Author

Touchon, Marie, Rocha, Eduardo P. C., Bernheim, Aude, and Bikard, David

Subjects
DNA repair, CRISPRS, BACTERIAL genetics, PROTEOBACTERIA, DOUBLE-strand DNA breaks, DOUBLE-stranded RNA
Abstract

The absence of CRISPR-Cas systems in more than half of the sequenced bacterial genomes is intriguing, because their role in adaptive immunity and their frequent transfer between species should have made them almost ubiquitous, as is the case in Archaea. Here, we investigate the possibility that the success of CRISPR-Cas acquisition by horizontal gene transfer is affected by the interactions of these systems with the host genetic background and especially with components of double-strand break repair systems (DSBRS). We first described the distribution of systems specialized in the repair of double-strand breaks in Bacteria: homologous recombination and nonhomologous end joining. This allowed us to show that such systems are more often positively or negatively correlated with the frequency of CRISPR-Cas systems than random genes of similar frequency. The detailed analysis of these co-occurrence patterns shows that our method identifies previously known cases of mechanistic interactions between these systems. It also reveals other positive and negative patterns of co-occurrence between DSB-RS and CRISPR-Cas systems. Notably, it shows that the patterns of distribution of CRISPR-Cas systems in Proteobacteria are strongly dependent on the epistatic groups including RecBCD and AddAB. Our results suggest that the genetic background plays an important role in the success of adaptive immunity in different bacterial clades and provide insights to guide further experimental research on the interactions between CRISPR-Cas and DSB-RS. [ABSTRACT FROM AUTHOR]

Published
2019
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