Bacterial adaptation to host association

Microorganisms are commonly found living in multicellular organisms. Taxonomically, individual symbionts and communities of microbes, microbiotas, of a variety of animals and plants have been well-described and it has become clear that they can have profound effects on their hosts' biology. The bacterial side of the association, however, has received comparatively little attention. In particular how microbes adjust to life with a host, and what drives the emergence and maintenance of microbe-host associations remains understudied. In this thesis, my main objective is therefore to improve our understanding of the traits and life history strategies that facilitate microbe-host associations. To that end I combine experimental study of bacterial isolates from the natural microbiota of the nematode Caenorhabditis elegans as a model system with predictions from mathematical models. In the first part of the thesis I focus on the functional ecology of the natural C. elegans microbiota. Integrating whole genome sequencing of bacterial isolates, metabolic modeling, and experiments, we found that the microbiota can synthesize all amino acids and vitamins essential to the worm. Further, we demonstrate that their predicted traits and metabolic repertoires lead to distinct life history strategies, shape interactions within the microbiota as well as worm colonization and worm population growth. The second part of the thesis addresses the evolution of bacteria in host-association. The first step is the development of the concept of a biphasic life cycle as an evolutionary intermediate between a free-living and a host-associated lifestyle. At this transition, matrix population models predict that bacteria can optimize fitness either by increasing replication rates or by modulating migration rates between host and environment. Experimentally evolving the microbiota isolate Pseudomonas lurida MYb11 in a biphasic life cycle with C. elegans, we find that a key step to associating is to simply stick to the host. Specifically, we observe the evolution of wrinkly colony types that show improved persistence in worms and a greater ability to form biofilms than the ancestral MYb11. This goes hand in hand with genetic mutations in regulators of the universal second messenger cyclic di-GMP, previously linked to the life history transition from motile to sessile and stress-tolerant. These findings highlight that bacteria can adapt to a host that they encounter periodically during a biphasic life cycle. Finally, I extend the focus to a two-member microbiota of MYb11 and Ochrobactrum vermis MYb71 and study interactions between these species and differences in their life history strategies when co-associating in C. elegans. This confirms that interactions within the microbiota are context-dependent and shift along the stages of the biphasic life cycle. Further, it demonstrates that different life history strategies co-exist in the microbiota, with the one centered on stress-tolerance being the most advantageous. Overall, this thesis emphasizes the importance of bacterial traits and life history to shaping life in association with a host. It thereby provides fundamental insights into the driving forces and possibly origin of microbe-host associations.


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