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The ecology and evolution of microbial immune systems [1]

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Date: 2024-09

09:00-09:30 Real-time arms race: coevolution of phages and vibrio in natural populations Facing the therapeutic impasse of antibiotics, farming systems, including aquaculture, should consider the extraordinary resource of phages, natural bacterial predators, for environmentally friendly practices. Sustainable and safe use of phages requires an understanding of their specificity and evolution. However, our knowledge of phage infection mechanisms is mainly based on model systems in laboratory conditions, which do not reflect the enormous diversity that exists in nature. Using natural populations of marine bacteria (vibrios) infecting oysters, we have shown that most phages have a narrow host range. Their specificity depends first on their ability to bind to the host surface and second on their capacity to resist intracellular defence mechanisms. In the case of the oyster pathogen Vibrio crassostreae, we can track coevolutionary lineages in the marine environment. These are phage species capable of adsorbing specifically to clades nested within V crassostreae. I will present preliminary results from a follow-up of these lineages in a new time-series sampling and genomic analyses that allow us to propose evolutionary scenarios. Emerging resistance to phages in nature primarily results from horizontal gene transfer. We have discovered a family of phage satellites, named Phage-Inducible Chromosomal Minimalist Islands (PICMIs), which are widely distributed in the Vibrionaceae family. PICMIs are characterized by their reduced gene content, lack of genes for capsid remodelling, and the packaging of their DNA as a concatemer. These islands integrate into the bacterial host genome adjacent to the fis regulator and encode three core proteins essential for excision and replication. PICMIs rely on virulent phage particles to spread to other bacteria and protect their hosts from competitive phages without interfering with their helper phage. The discovery of PICMIs highlights the necessity of fully characterizing virulent phages and their host producers to prevent the spread of satellite-mediated resistance in phage therapy. In conclusion, exploring natural populations of phages and bacteria is essential for developing fundamental knowledge, providing a solid basis for informed consideration of new therapeutic avenues in the fight against pathogens, while preserving the delicate balance of the microbial ecosystem. Professor Frederique Le Roux, University de Montreal, Canada Professor Frederique Le Roux, University de Montreal, Canada Dr Le Roux explores the paradoxical sustainability of parasitism through her research on various microbes. She completed her doctoral thesis on the human Epstein-Barr virus at the Ecole Normale Superieure of Lyon and conducted postdoctoral research at the Institut Gustave Roussy. Her subsequent work includes studying protozoan parasites of bivalve molluscs at Ifremer, and Vibrio bacteria pathogenic to oysters and shrimp corals at the Institut Pasteur in Paris, Harvard Medical School in Boston, and the Roscoff Marine Station. More recently, she has focused on vibriophages. Since September 2023, she has held the Canada Research Chair of Excellence in the Eco-Evo-Patho of Microbes in Nature and serves as a Professor at the University of Montreal. As an IVADO member, she and her team investigate the mechanisms and evolution of interactions between bacteria and their phages in natural populations.

09:30-09:45 Discussion

09:45-10:15 Fighting with phages: how vibrio cholerae defends against viral attack The evolution of all forms of life is a history of the relentless conflict between hosts and parasites. Viral parasites of bacteria, known as phages, are key components of all ecosystems and profoundly influence the biology of their bacterial hosts. Phages select for bacteria that evade phage predation by deploying elaborate and mechanistically diverse defence systems, the full breadth of which is only beginning to be realised. Phages also drive the mobilisation and dissemination of genetic material. Yet, despite the central role of phages in microbial evolution and ecology, molecular insight into the reciprocal dynamics of phage-bacterial adaptations in nature is lacking, particularly in clinical contexts. As a direct consequence, the discovery of phage-encoded defence inhibitors dramatically lags behind the known arsenal of bacterial defences. In partnership with international collaborators, my lab has established a longitudinal collection focused on the diarrheal pathogen, Vibrio cholerae, and the lytic phages that prey on this pathogen as it causes disease in humans. Leveraging genomic and mechanistic approaches, we use this tractable platform to gain an in-depth understanding of how these interacting microbes coevolve within the context of human infection. I will discuss mechanisms of defence in epidemic V cholerae mediated by parasitic mobile genetic elements and how phage-encoded mechanisms countering these elements have driven their diversification in epidemic V cholerae. Dr Kim Seed, University of California, USA Dr Kim Seed, University of California, USA Dr Kim Seed is an Associate Professor in the Department of Plant and Microbial Biology at the University of California, Berkeley. Professor Seed’s laboratory investigates how phages impact the evolution and selection of epidemic Vibrio cholerae, the causative agent of cholera.

10:15-10:30 Discussion

10:30-11:00 Break

11:00-11:30 Viral tRNAs rescue host tRNA degradation by the PARIS bacterial immune system The Phage Anti-Restriction Induced System (PARIS) was first identified within hotspots of anti-phage defence systems carried by satellites of the P4 family. There it acts as an anti-anti-restriction system by blocking the infection of phages carrying anti-restriction proteins such as the T7 Ocr. PARIS is composed of a 53 kDa ABC ATPase (AriA) and a 35 kDa TOPRIM nuclease (AriB) that assemble into a 425 kDa supramolecular immune complex. We use cryo-EM to determine the structure of this complex which explains how six molecules of AriA assemble into a propeller-shaped scaffold that coordinates three subunits of AriB. ATP-dependent detection of foreign proteins triggers the release of AriB, which assembles into a homodimeric nuclease that blocks infection by cleaving the host tRNALys. Phage T5 subverts PARIS immunity through expression of a tRNALys variant that prevent PARIS-mediated cleavage, and thereby restores viral infection. PARIS is one of an emerging set of immune systems that target tRNA to trigger translational arrest. It also belongs to a broader family of systems that employ ABC ATPases to sense viral infections. Professor David Bikard, Institut Pasteur, France Professor David Bikard, Institut Pasteur, France David Bikard is the head of the Synthetic Biology lab at the Institut Pasteur in Paris. He obtained an engineering degree from AgroParisTech and a PhD from Paris Diderot University for his work performed at the Institut Pasteur on the integron bacterial recombination system. He then joined the laboratory of Luciano Marraffini at the Rockefeller University as a postdoctoral fellow where he started to work on CRISPR systems. David is interested in the genetic innovation that occurs as a result of the competition between bacteria and phages and how it can be harnessed for biotechnological applications.

11:30-11:45 Discussion

11:45-12:15 How do microbial immune systems spread in nature? Microbial immune systems play a crucial role in protecting microbes from foreign mobile genetic elements (MGEs) such as bacteriophages, satellites, and plasmids. These defence mechanisms can be readily acquired or lost by bacteria, facilitating their adaptation to various threats. Interestingly, many microbial immune systems are themselves encoded by MGEs, linking their distribution directly to the movement of these MGEs. However, not all immune systems are associated with MGEs; some are integrated into different regions of bacterial chromosomes. This raises intriguing questions about the transfer mechanisms of these chromosomally encoded immune systems between bacterial strains. In this talk, we will explore the roles of lateral transduction and lateral cotransduction in the mobility of chromosomal defence islands that harbour multiple immune systems. Lateral transduction, a robust gene transfer process mediated by bacteriophages, enables the transfer of large segments of bacterial DNA from one bacterium to another. Lateral cotransduction, a more recently described mechanism, further expands our understanding of gene mobilisation facilitated by phage-inducible chromosomal islands (PICIs). We will examine how these processes contribute to the horizontal gene transfer of immune systems across bacterial populations, and their impact on bacterial adaptation and evolutionary dynamics. Our findings will illuminate the complex interactions between phages and bacteria, revealing how these interactions govern the genetic flow and diversity of immune systems within microbial communities. Understanding these mechanisms is vital for gaining insights into the spread of resistance traits and the ongoing evolutionary arms race between microbes and their viral predators. Professor José Penades, Imperial College London, UK Professor José Penades, Imperial College London, UK Professor Penadés studies the emergence and evolution of clinically significant bacteria. His research team is renowned for their insights into how bacteriophages (viruses that target bacteria) and other mobile genetic elements facilitate bacterial chromosomal gene transfer, driving bacterial evolution. He discovered the most potent mechanism of bacteriophage-mediated gene transfer to date: lateral transduction, which makes bacterial chromosomes more mobile than traditional mobile DNA elements. Professor Penadés also uncovered and studied the transfer mechanism of a widespread and clinically critical family of genetic elements in various bacterial pathogens: Phage-Inducible Chromosomal Islands (PICIs). His lab found that PICIs use a new, highly adaptable form of gene transfer, distinct from lateral transduction, termed lateral cotransduction. These findings enhance our understanding of genetic mobility and its impact on bacterial adaptation and virulence.

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[1] Url: https://royalsociety.org/science-events-and-lectures/2024/09/microbial-immune-systems/

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