Deciphering the processes of adaptation and exaptation driving the evolution of opportunism in bacteria

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Project Summary/Abstract In the last few decades, the importance of bacteria, not only as pathogens but also as beneficial organisms, has been elucidated. However, it has become clear that bacterial diversity and evolution is much more complex than initially thought. Because most systems do not allow for the integration of multiple approaches, there are still many fundamental questions that remain to be answered about bacterial evolution. Specifically, how bacteria evolve in the natural environment and what drives the evolution of different lifestyles in bacteria. From an evolutionary perspective, opportunistic bacteria are complex entities because of their wide-range of lifestyles. Their ability to be free-living, commensal, and pathogenic means that these organisms are highly adaptable, but the factors that influence their evolution remain a mystery. Understanding opportunistic bacterial evolution is important because they are responsible for causing dangerous hospital-acquired infections worldwide and are often multidrug resistant superbugs. Studies of bacterial evolution are primarily conducted using comparative genomic approaches or in vitro experimental evolution. However, the versatility and complexity of opportunistic bacteria, as well as their relationships with animal hosts, requires more realistic experimental settings. Here, we have developed a unique research program that will integrate multiple approaches, including in silico, in vitro, and in vivo analyses. Key to our research is our specific experimental evolution framework to study the interactions between four key players: i) an opportunistic bacterium, ii) their environmental predators, iii) an animal host and iv) the animal host microbiota. Our ability to pursue a multi-approach strategy is due to our tractable model systems. Our bacterial model systems, Serratia marcescens and Pseudomonas aeruginosa, are ubiquitous environmental and multi-drug resistant opportunistic pathogens of humans as well as many other organisms. We will use honeybees as our host model system (Apis mellifera), which are optimal for this research because they offer a natural environment in which to study opportunistic bacterial evolution and host-microbe interactions that is tractable, cost-effective, highly replicable, and can be easily manipulated. Importantly, the honeybee microbiota is a stable community that can also be easily manipulated. Our novel approach and systems will allow us to address many fundamental gaps in our understanding of bacterial evolution, including the forces that drive the evolution of opportunistic bacteria that exhibit changing lifestyles. In particular, we will identify what genes are involved in versatile lifestyles, what adaptive forces and associated tradeoffs are driving the evolution of opportunistic bacteria, and what functions are exapted during exposure to fluctuating environments and changing selective pressures. Results will have important fundamental implications but also health implications as they will reveal traits important for host colonization and virulence, which can be used for the development of new strategies for combating multidrug resistant opportunistic bacterial infections.