Temperate bacteriophages in Hydra and their role in metaorganism maintenance

All eukaryotic organisms are associated with a complex set of microbes, including bacteria, fungi and viruses. This association is termed metaorganism or holobiont. Bacteria are well-known key players within metaorganisms and play an important role in health and disease of their eukaryotic host. Shifts in the bacterial community composition are associated with diseases like inflammatory bowel disease, diabetes, obesity and even depression. Therefore, it is important to maintain a stable microbiome. Considering that bacteriophages (bacterial viruses, short: phages) are often obligate killers to their bacterial hosts, they can shape whole bacterial communities. Consequently, researching and understanding phage-bacteria interactions is of enormous importance. While several correlative virome studies have been conducted, little is known about the functional role of bacteriophages within metaorganisms. Hidden in the genome of their bacterial host, especially temperate phages are often neglected and overlooked. A perfect organism for studying bacteria-phage-host interactions is the freshwater polyp Hydra, because it features a host specific bacterial and viral community. To shed light on the role of temperate phages within metaorganisms, I first identified prophages that are integrated in Hydra-associated bacteria. Therefore, I screened the genomes of the bacterial culture collection of Hydra for prophage signatures, of which six phages are inducible by antibiotics and environmental stressors. With cross infection experiments I analyzed the host range of these phages, of which three featured a broad host range. One of them was the phage of Hydras main colonizer Curvibacter sp. (phage TJ1). To evaluate the role of this dominant phage TJ1 in homeostasis of Hydra, I analyzed the activity and the infectivity of this phage in vitro. I could demonstrate that phage TJ1 is active on the eukaryotic host and negatively affects the growth of the next most abundant bacterial colonizers: Duganella sp., Undibacterium sp. and Pelomonas sp.. Furthermore, I could show that the phage is not only inducible by environmental stressors but also by competing bacteria in vivo. This indicates that TJ1 is active on Hydra without additional, artificial stimulation. Although exposed to TJ1, susceptible bacterial isolates seem to be unable to evolve resistance on Hydra. To evaluate the mechanisms behind this observation, I conducted an in vitro coevolution experiment with phage TJ1 and the susceptible bacterial colonizers Duganella sp., Undibacterium sp. and Pelomonas sp.. I could show that after gaining resistance to the phage, the bacteria lose their ability to colonize their host, probably caused by mutations that resulted in reduced biofilm formation and motility. In conclusion, my results are an indication for the importance of temperate phages within metaorganisms and give insights into the functional role of the dominant Curvibacter phage TJ1. This phage contributes to the maintenance of Hydras species-specific bacterial community by down-regulating other highly abundant bacterial colonizers. Moreover, my data gives a hint to how temperate bacteriophages and bacteria can coexist on a eukaryotic host: High fitness costs in resistant strains may result in favouring phage susceptibility over resistance on Hydra.


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