eprintid: 28915 rev_number: 19 eprint_status: archive userid: 5434 dir: disk0/00/02/89/15 datestamp: 2020-10-08 10:31:36 lastmod: 2020-10-12 12:01:16 status_changed: 2020-10-08 10:31:36 type: doctoralThesis metadata_visibility: show creators_name: Voss, Philipp Alexander title: Cellular processes underlying symbiosis establishment in Aiptasia, a model for cnidarian-dinoflagellate endosymbiosis subjects: ddc-500 subjects: ddc-570 divisions: i-140001 divisions: i-721000 adv_faculty: af-14 abstract: Coral reefs are the most biodiverse ecosystems on Earth. Their productivity is powered by the symbiotic association between corals and unicellular photosynthetic dinoflagellates of the family Symbiodiniaceae. These symbionts reside inside the corals’ cells in specialized organelles, the symbiosomes, from where they transfer energy-rich compounds to the corals to support their nutrition. Interestingly, symbiosis is re-established every generation, as most corals produce symbiont-free offspring, which acquire symbionts from the surrounding sea water by phagocytosis. Despite the importance of symbiosis establishment for the coral life cycle, it is unclear how corals identify compatible symbionts and which mechanisms allow the symbionts to persist in their intracellular niche. For example, it is unknown how symbionts escape the host immune response and how symbiont-derived nutrients are integrated into the host cell metabolism. Using the sea anemone Aiptasia as a model, I characterized the underlying processes of symbiosis establishment. Aiptasia engages in symbiosis with similar species of Symbiodiniaceae as corals, and can be induced to produce larvae under laboratory conditions, providing access to symbiont-free larvae to study symbiosis establishment year-round. In a first step, I compared the uptake of compatible symbionts to that of free-living Symbiodiniaceae and inert beads in Aiptasia larvae. I uncovered that selection of symbionts occurs already prior to their phagocytosis and that while phagocytosis was size-selective, all tested particles were phagocytosed. This implies that additional mechanisms for the selection of compatible symbionts occur once potential symbionts have been phagocytosed. To assess the molecular mechanisms underlying symbiosis establishment in more detail, I developed a cell-specific method to compare gene expression in symbiotic and non-symbiotic cells. This revealed a major down regulation of various catabolic processes, including autophagy, as a response to symbiont uptake. Specifically, I found evidence that the shutdown of autophagy is regulated by a conserved gene-regulatory network under the control of the master regulator of cell growth and proliferation, mTOR (mechanistic target of rapamycin). mTOR is activated by symbiont-derived nutrients and symbiosis resulted in increased lipid storage and cell proliferation. Thus, I propose a model where symbiont-derived nutrients activate mTOR signaling, which acts as a mechanism of symbiont selection. Beneficial symbionts activate mTOR, resulting in their maintenance and allowing them to proliferate in the host tissue, while failure to activate mTOR would result in their autophagy. Currently, coral reefs are declining world-wide at unprecedented rates, mostly caused by global warming disrupting the symbiotic interaction leading to loss of symbionts from the host, a process known as ‘coral bleaching’. This thesis lays the foundation for future work studying the molecular mechanisms underlying symbiont selection and symbiosis establishment in cnidarian-dinoflagellate symbiosis. Understanding how corals select and stably integrate symbionts may help to predict how corals adapt to changing environments, a prerequisite to combat the loss of these important ecosystems. date: 2020 id_scheme: DOI id_number: 10.11588/heidok.00028915 ppn_swb: 1735355879 own_urn: urn:nbn:de:bsz:16-heidok-289153 date_accepted: 2020-07-22 advisor: HASH(0x55fc36c3d538) language: eng bibsort: VOSSPHILIPCELLULARPR2020 full_text_status: public place_of_pub: Heidelberg citation: Voss, Philipp Alexander (2020) Cellular processes underlying symbiosis establishment in Aiptasia, a model for cnidarian-dinoflagellate endosymbiosis. [Dissertation] document_url: https://archiv.ub.uni-heidelberg.de/volltextserver/28915/1/Thesis_Philipp_Voss_print_with-bookmarks.pdf