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

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.