Mechanism of Symbiont Acquisition
Most corals produce non-symbiotic progeny that acquire symbionts anew each generation from the environment. Symbionts are phagocytosed by endodermal cells of non-symbiotic coral larvae and are then maintained inside their host cells in “symbiosomes”, distinct organelles resembling phagolysosomes.
Phagocytosis has originally evolved for nutrition and was only later adapted for pathogen clearance. Interestingly, corals and their symbiotic relatives are genomically highly complex and share gene repertoires for phagocytosis-related pathways, including innate immunity, with vertebrates. To date, it is unclear whether symbionts use similar mechanisms as pathogens to avoid digestion and allow intracellular persistence. We are interested in analyzing whether cnidarians such as symbiotic corals and Aiptasia have evolved distinct cell types for food uptake, symbiont acquisition and removal of pathogens. We aim to understand the molecular mechanisms underlying symbiont recognition and phagocytosis and analyze the molecular composition of “symbiosomes” in comparison to pathogen-containing organelles destined for destruction.
Finally, we attempt to dissect molecularly how cnidarians select suitable symbionts, a phenomenon known as ‘symbiosis specificity’ that has been implicated in the physiology and ecology of the host organism, such as adaptation to environmental change.
Coordination of Cell Function
Symbionts and host cells are metabolically dependent on each other and once symbionts are integrated into the host cells, cell functions such as nutrient exchange must be coordinated. Corals cannot synthesize cholesterol, a key molecule for membrane homeostasis of every cell and for cellular signaling. Dinoflagellates synthesize, in addition to cholesterol, many sterol derivatives and it is conceivable that corals rely on symbiont-derived sterols for maintaining cell function. We aim to identify the molecular key players involved in sterol transfer from symbionts and cellular use in the host and to analyze their function at the cellular and biochemical level. We are currently focusing on the Niemann-Pick Type C (NPC2) genes, coding for lysosomal proteins which are essential for cholesterol metabolism in humans. The NPC2 gene family is expanded in symbiotic corals and we also aim to understand the evolutionary origin of this gene family.
Cell proliferation is a prerequisite for development and growth. It is unclear whether and how symbionts and host cells coordinate cell division and symbiont distribution to daughter cells.
We aim to develop methods for live-imaging of dividing symbiotic cells as the basis for understanding whether the presence of symbionts influences host cell organization and function. Live-imaging approaches will uncover whether symbiotic host cells differ in rates of division, spatial organization of DNA replication or chromosome segregation when compared to non-symbiotic cells.
Evolution of Genome Organization
Each cell must dynamically organise its genetic information to allow faithful transcription, replication and partitioning during cell division. Histone-based chromatin organisation is a hallmark of eukaryotic genomes with one exception: the dinoflagellates which play key roles as primary producers, heterotrophs and symbionts in marine food webs. Dinoflagellates organise their extraordinary large genomes into liquid crystal-like arrays and genome packaging is driven by a unique group of proteins, the Dinoflagellate Viral Nucleo Proteins (DVNP). The DVNP proteins are thought to maintain the bulk of the highly-condensed dinoflagellate chromatin which exist alongside with some histone-based chromatin. To date it is unclear how dinoflagellates dynamically regulate the accessibility of their genomic content. In a novel line of research, we aim to use dinoflagellates of the genus Symbiodinium as model to unravel novel principles of eukaryotic genome organisation. To better understand how DVNPs drive dinoflagellate genome compaction and how the interplay between DVNP- and histone-based chromatin allows cellular functions and adaptation, we will combine genomics, cell biology and biochemistry.