Animal developmental programs occur within the context of coevolved associations with microbes. Hydra is one of the prime model systems for evolutionary developmental biologists. The fact that symbiotic interactions were discovered to be essential to development in numerous animals, lead us to propose using Hydra to uncover the common principles of symbiogenesis and their links to evolution with particular emphasis on developmental programs. Our prior work has shown that the epithelial surface is densely colonized by a stable multi-species bacterial community. Each Hydra species supports long-term associations with a different set of bacteria. Hydra host shapes the specific microbiome by means of the innate immune system and a rich repertoire of antimicrobial peptides.
In the first funding period (C1.1, PI Bosch) we established a long-term germ-free Hydra culture and discovered that (i) the presence and structure of this microbiota is critical not only for the health of the polyps but also for patterning processes and tissue homeostasis; (ii) the transcription factor FoxO provides a direct link between stem cell proliferation, tissue homeostasis, and the microbiota; and (iii) there is a direct interaction between neurons and microbes.
In the second funding period we will expand on the past findings to address two specific questions:
(i) How do resident microbiota affect developmental and patterning processes in adult Hydra polyps? Answering this question relies on large-scale unbiased and systematic identification of bacteria-responsive patterning-associated Hydra genes using comparative transcriptomic analysis (RNAseq) followed by their functional analysis.
(ii) Do microbes play a role in Hydra´s early embryonic development? And more specifically, do resident microbiota influence neurogenesis in embryos and/or in adults? Is the resident microbiota involved in educating neuronal precursor cells/stem cells which, in turn, influence the composition of the microbiota? This question is based on preliminary observations of polyps with abnormal morphology hatching from eggs produced by germ-free females.
Our newly established mass-culture of long-term germ-free animals in combination with the well-equipped tool box for studying Hydra development and the expertise of the CRC consortium in analysing and modelling interactions between microbes and evolving metaorganisms will allow to find answers to these questions. Elucidating these issues will not only contribute to the understanding of host interactions with microbial communities in one of the simplest possible animal systems but may also provide conceptual insights into the complexity of host-microbe interactions in general. The project will assist our understanding of how all of the parts of a living organism operate together within a meta-organismic framework.