Bacteria in the wild carry a chaotic mix of genetic parasites and immune systems, but the classic long-term evolution experiment that tracks how bacteria change over decades deliberately stripped those elements away. This project will reboot that experiment by adding back the natural diversity of mobile genetic elements and defence systems, then watching how they shape bacterial evolution over thousands of generations. The gap is stark: we know that defence systems and mobile elements dominate real bacterial genomes, and we know that evolution in a stripped-down lab strain follows predictable patterns, but no one has connected the two. Without that connection, predictions about how bacteria evolve in the wild—in soil, in hospitals, in the human gut—remain guesswork. This is fundamental science. If it succeeds, it will transform our causal understanding of how bacteria evolve over long timescales, revealing whether genetic parasites accelerate or slow adaptation, and whether defence systems drive the very genome rearrangements that create new functions. That deeper understanding could eventually improve predictions about antibiotic resistance emergence or pathogen evolution, but the immediate payoff is a mechanistic theory of bacterial genome evolution that currently does not exist.
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Two major conceptual breakthroughs have revolutionised our understanding of bacterial genome evolution during the past decade. First, genome re-sequencing of Lenski's long-term evolution experiment (LTEE) has revealed the complexity of mutational dynamics driving genome evolution, and that rates of molecular evolution are decoupled from rates of adaption through time, even for a model bacterium inhabiting the simplest of environments. Second, microbial genomics has revealed bacterial genomes to be dynamic battlefields replete with myriad defence systems (DSs) and menageries of mobile genetic elements (MGEs) that collaborate and compete with each other, whilst also spurring evolutionary innovation by driving the exchange of genetic material between lineages (horizontal gene transfer; HGT). These views of bacterial genome evolution are, however, disconnected because, by design, the LTEE used a model bacterium with a relatively simple genome depleted in MGEs and DSs compared to its counterparts in nature. Moreover, MGEs and DSs have only ever been included in short-term evolution experiments and never at levels of diversity seen in nature, meaning that their long-term impacts on bacterial genome evolution are unknown. To deliver a causal understanding of how MGEs and DSs shape long-term bacterial evolution requires that these conceptual breakthroughs be reconciled: augmenting the reductive complexity of LTEEs by integrating into this powerful approach the rich diversity of MGEs and DSs that we now know exists in nature. To achieve this, I will reboot the LTEE framework, using innovative experimental designs to directly test how MGEs and DSs shape the trajectory, tempo, and mode of long-term genome evolution and adaptation in bacteria. Discoveries from this project will transform our causal understanding of long-term bacterial evolution, enhancing our ability to predict the behaviour of natural systems, and forging an eco-evolutionary view of bacterial genomes.
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