Dinoflagellate symbionts escape vomocytosis by host cell immune suppression

Abstract

Emergence of the symbiotic lifestyle fostered the immense diversity of all ecosystems on Earth, but symbiosis plays a particularly remarkable role in marine ecosystems. Photosynthetic dinoflagellate endosymbionts power reef ecosystems by transferring vital nutrients to their coral hosts. The mechanisms driving this symbiosis, specifically those which allow hosts to discriminate between beneficial symbionts and pathogens, are not well understood. Here, we uncover that host immune suppression is key for dinoflagellate endosymbionts to avoid elimination by the host using a comparative, model systems approach. Unexpectedly, we find that the clearance of nonsymbiotic microalgae occurs by non-lytic expulsion (vomocytosis) and not intracellular digestion, the canonical mechanism used by professional immune cells to destroy foreign invaders. We provide evidence that suppression of TLR signalling by targeting the conserved MyD88 adapter protein has been co-opted for this endosymbiotic lifestyle, suggesting that this is an evolutionarily ancient mechanism exploited to facilitate symbiotic associations ranging from coral endosymbiosis to the microbiome of vertebrate guts. Main Text SummarySymbiotic interactions appear in all domains of life and are key drivers of adaption and evolutionary diversification. A prime example is the endosymbiosis between corals and eukaryotic, photosynthetic dinoflagellates, which the hosts take up from the environment by phagocytosis.Once intracellular, endosymbionts transfer vital nutrients to the corals, a process fundamental for survival in nutrient-poor environments (Muscatine, 1990;Yellowlees et al., 2008). A central question is how endosymbionts circumvent the hosts' defensive strategies to persist intracellularly and conversely, how hosts prevent invasion by non-symbiotic microorganisms. Here, we use a comparative approach in the anemone model Exaiptasia pallida (commonly Aiptasia) (Hambleton et al., 2019;Tolleter et al., 2013;Weis et al., 2008) to address this. Using RNA-seq, we show that symbiont phagocytosis leads to a broad scale, cell-specific transcriptional suppression of host innate immunity, but phagocytosis of non-symbiotic microalgae does not. We show that targeting MyD88 to inhibit canonical TLR signalling promotes symbiosis establishment. Using live imaging and chemical perturbations, we demonstrate that non-symbiotic microalgae are cleared from the host by ERK5-dependent vomocytosis (non-lytic expulsion) (Alvarez and Casadevall, 2006;Gilbert et al., 2017;Ma et al., 2006), and that immune suppression is key for symbiont persistence and for establishment of an intracellular LAMP1 niche. We propose that expulsion is a fundamental mechanism of ancient innate immunity used to eliminate foreign cells; a process that is subverted by symbionts in the endosymbiotic association that forms the foundation of coral reef ecosystems. University) Postdoctoral Program, and a PhD scholarship within the Graduate School "Evolutionary Novelty & Adaptation by the Baden-Württemberg Landesgraduier...

A stony coral cell atlas illuminates the molecular and cellular basis of coral symbiosis, calcification, and immunity

“…This photo-symbiosis sustains the high-energy demands of coral growth and reproduction, including skeleton production by massive calcium carbonate deposition. In addition to diverse metabolic adaptations ( Morris et al, 2019 ), coral immunity is considered to be a major factor for coral endosymbiosis, as well as for modulating interactions with other microbial eukaryotes and prokaryotes ( Jacobovitz et al, 2019 ; Kwong et al, 2019 ).…”