Towards understanding the benefits, establishment and maintenance of host-microbe homeostasis in Hydra

Franzenburg, Sören

Animals evolved in a biotic environment dominated by microbes. Thus, all animals, ranging from simple invertebrates to primates, are host to complex microbial communities, which are essential for the host’s health. However, the mechanisms determining the community composition and homeostasis within this microbiota are not fully understood. The present thesis includes a detailed analysis of the microbiota in the cnidarian host Hydra, including its beneficial function, establishment, regulation and maintenance. First, the bacterial community composition was profiled in polyps of seven distinct species of hydras. Although laboratory reared under identical conditions for three decades, this survey revealed host-species specific bacterial communities, partially resembling host phylogeny. This finding indicated distinct selective pressures in different host species. Germfree Hydra polyps turned out to be prone to fungal infection. Controlled in vivo infections experiments identified several members of the microbiota to significantly inhibited fungal growth. Thus, bacterial symbionts seem to be an integral part of Hydra’s antifungal immunity. To identify regulatory principles of the microbiota assembly, the ontogenetic establishment of the bacterial community was investigated in Hydra. The community assembly turned out to follow a robust, temporal progression comprising conserved key features as the animal approaches adulthood. Mathematical modeling identified interbacterial interactions as well as host modulation to mediate this colonization process. How does the host sense its bacterial colonizers? To answer this question, transgenic Hydra polyps with an interfered Toll-like-receptor (TLR) signaling pathway were generated. TLR-signaling serves different functions in a variety of model organisms. The data of the present thesis clearly indicated a role of TLR-signaling in Hydra’s bacterial perception, being involved in the mediation of bacterial colonization and pathogen defense. Antimicrobial peptides (AMPs) of the arminin peptide family show highly species-specific expression profiles in four species of Hydra. Their potential roles in shaping the observed host-species specific bacterial communities were analyzed using arminin loss-of-function polyps. The specific, differential recolonization of arminin deficient polyps strongly indicated a role of these peptides in the selection of co-evolved bacterial associates. Taken together, the present study elucidates the active mediation of bacterial colonization by innate immune mechanisms of the host.

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Franzenburg, Sören: Towards understanding the benefits, establishment and maintenance of host-microbe homeostasis in Hydra. 2013.

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