Increased levels of one amino acid transforms a symbiont into a lethal pathobiont

Eukaryotic organisms are associated with complex microbial communities, whose alterations have been implicated in disease development. Nonetheless, it remains unclear whether these changes are a cause or a consequence of disease. Here, we report a causal link between environmentally induced shifts in the microbiota and disease development. Using the model organism Hydra, we observed changes in microbial community composition when transferring laboratory-grown Hydra to natural lake environments. These shifts were not only caused by new colonisers, but were also influenced by lake water nutrients. Moreover, selective manipulation of the nutrient environment induced compound-specific shifts in the microbiota followed by disease development. Finally, L-arginine supplementation alone caused a transition from symbiotic to pathogenic Pseudomonas, leading to upregulation of immune response genes, tissue degradation, and host death. These findings challenge the notion that host-associated microbiota is exclusively controlled by the host, highlighting the dynamic interplay between host epithelial environment, bacterial coloniser pool, and nutrient conditions of the surrounding water. Furthermore, our results show that overfeeding of the microbiota, allows uncontrolled bacterial growth. Depending on nutrient composition symbiotic bacteria can turn into pathogens. Environmental conditions may thus render symbionts a potential hazard to their hosts, blurring the divide between pathogenic and non-pathogenic symbionts.