Host-selected mutations converging on a global regulator drive an adaptive leap towards symbiosis in bacteria

Most bacteria that associate with animals do not cause harm, and many are essential to health or provide other benefits. An animal’s immune system must permit these beneficial associations and at the same time block harmful microbes. This ultimately means that even beneficial bacteria must adapt to the immune barriers that they encounter. Different species that live in a close relationship with each other are known as symbionts. A species of bacteria called Vibrio fischeri can form a mutually beneficial symbiotic relationship with squid. The squid provide food for the bacteria, but only the bacteria that successfully navigate immune barriers and reach the squid’s “light organ” are fed. In return, the bacteria produce bioluminescence, making the nocturnal squid appear like moonlight in the water. As the bacteria reproduce, some individuals randomly acquire genetic mutations, some of which might improve the bacteria’s chances of survival. Which mutations and associated traits allow bacteria to beat out the competition and evolve to become animal symbionts? To investigate, Pankey, Foxall et al. grew V. fischeri bacteria from several ancestors that were poor at colonizing squid. Groups of newly hatched squid selected potential symbionts from the resulting mix of bacteria. The selected symbionts were allowed to reproduce within the squid to form a new population of bacteria and were later vented out for a new batch of squid to sort through. This was repeated to ultimately form a final group of bacteria that had passed through 15 squid in turn. Unexpectedly, the bacteria in the final group all found the same solution to help them adapt to symbiotic life with the squid: mutations to the gene that encodes a signaling protein called BinK. Eight distinct mutations arose that dramatically changed how the bacteria interacted with squid. The evolved bacteria created a coating that hid them from squid immune cells and protected them from chemicals that squid use to kill invaders. The mutations also altered how the bacteria communicated with each other. This adjusted the intensity of light that they produced for their host to a more natural level, and improved their ability to grow on squid-provided food. Overall, the results presented by Pankey, Foxall et al. demonstrate that small genetic mutations can transform non-symbionts into symbionts, enabling them to evolve rapidly to form a symbiosis with a new host. This demonstrates that these bacteria already had the ability to coordinate the complex behaviors necessary to overcome the multiple barriers provided to them by the squid immune system. Other beneficial animal–bacteria associations are likely to work on similar principles; the study exemplifies the utility of experimental evolution systems and lays a foundation for further work to investigate these principles in more detail.