The architecture and evolution of host control in a microbial symbiosis

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Beneficial symbioses are widespread in nature and underpin the function of both natural and manmade ecosystems. Moreover, by providing the interacting species with new ecological functions, symbiosis represents an important source of innovation and has thus played a crucial role in the evolution of life on Earth. In endosymbiosis, endosymbiont cells live within host cells and, as such, hosts have evolved mechanisms to control these endosymbionts, collectively termed "host control". However, despite decades of study, the molecular mechanisms that hosts use to control their endosymbionts remain poorly understood. In particular, how the architecture of host control systems has evolved to provide hosts with sufficient flexibility to respond to changing conditions whilst also being evolutionarily robust is unknown for any symbiosis. Experimental studies of these questions in many symbioses are challenging because symbiotic organisms are not easily cultured independently nor typically amenable to genetic manipulation. In this project we overcome these challenges by using an experimentally tractable microbial symbiosis between the single-celled ciliate host Paramecium and the green alga Chlorella for which we have developed tools to "knockdown" the expression of target genes. In this symbiosis, hosts exchange nitrogen compounds derived from heterotrophy for carbohydrates from algal photosynthesis. In previous work we discovered that hosts modulate the number of algal symbionts in response to light intensity to maximise their fitness gains, but how hosts exert this control is not clear. In preliminary experiments for this proposal, we have discovered two putative mechanisms of host control, combining both positive and negative control levers, that hosts appear to use to regulate the number of algal symbionts per host cell. We predict that such multi-layered host control enables more precise regulation of endosymbiont number across environmental gradients whilst also providing a degree of redundancy so that the system has greater evolutionary robustness. To test these ideas, we will perform "gene knockdown" experiments to disrupt either each individual or both host control mechanisms and measure how this affects host growth, plasticity and fitness. Using cutting edge molecular methods, we will discover how each of the host control mechanisms works through understanding their effect on gene regulation and metabolism in both the host and symbiont. Finally, we will use experimental evolution to discover how the symbiosis recovers from disruption of host control systems, and test whether multiple layers of control enhance evolutionary robustness. Together these experiments will advance our understanding of the biology of symbioses, helping to solve the long-standing evolutionary puzzle of how and why symbioses evolve. In so doing the research will also provide insight into how symbioses and the important functions they perform can be maintained in natural and man-made ecosystems.