Unravelling tripartite species co-evolution under environmental change: can prophages accelerate bacterial virulence evolution?

• Applicant: Professorin Dr. Olivia Roth, since 12/2018
• Subject Area: Evolution and Systematics of Plants and Fungi ; Evolution, Anthropology
• Term: from 2015 to 2024
• Project identifier: Deutsche Forschungsgemeinschaft (DFG) - Project number 274695381

Adaptation and counter-adaptation between two interacting species can be very fast, making species interactions ideal to study rapid coadaptation on contemporary time scales. While both theoretical models and empirical studies deal with dual interactions, data including interactions of more than two species are scarce. However, in a natural scenario, most if not all species interact with more than one species. In addition, anthropogenic influences are changing selection regimes with broad implications on species interactions. Therefore, studies that address species interactions in an appropriate context with all relevant species and abiotic factors involved are urgently needed.During phase I we suggested studying rapid evolutionary adaptation in a three-way host-parasite interaction using an established model system consisting of pipefish Syngnathus typhle (i.e the final animal host), bacteria of the genus Vibrio, and it’s associated temperate phages (i.e. small viruses that infect Vibrio bacteria). With the ability to integrate into the bacterial genome, a temperate phage becomes a prophage that can provide its bacterial host (which is then called a lysogen) with beneficial genes, for instance virulence genes that may increase bacterial genome plasticity and ultimately bacterial fitness.During phase I we could demonstrate that environmental changes, such as reduced and thus stressful salinity conditions alter infection dynamics as well as co-evolutionary trajectories between bacteria and temperate phages. Using a co-evolution experiment between Vibrio sp. and a temperate phage we observed rapid adaptation in terms of bacterial resistance evolution against the phage. At stressful salinities lysogens were favoured over phage resistant mutants, whereas at ambient salinities lysogens were too costly and rapidly went extinct.We now propose (1) to perform whole genome sequencing on selected lysogens and mutants from those populations to identify the underlying genomic changes and mechanisms by which prophages integrate into the bacterial chromosome (random vs. site specific) and by which bacteria evolve resistance against temperate phages in dependence of environmental change. And (2) to investigate how an additional biotic interaction partner, the eukaryotic host and its immune system might constrain or promote Vibrio-phage co-evolution, and how it may ultimately accelerate Vibrio virulence evolution. To do so, we will use two different serial passage experiments, in which we follow phage-bacteria co-evolution inside the eukaryotic host. The obtained results will unravel basic mechanisms underlying co-evolutionary processes between bacteria and temperate phages and will provide novel insights into rapid virulence evolution and how it is accelerated by prophages and environmental change.

• DFG Programme: Priority Programmes
• Subproject of: SPP 1819: Rapid evolutionary adaptation: Potential and constraints
• International Connection: Norway
• Cooperation Partners: Sissel Jentoft, Ph.D.; Professorin Anne Kupczok, Ph.D.
• Ehemalige Antragstellerin: Professorin Carolin Wendling, Ph.D., until 11/2018