The coral microbiome in sickness, in health and in a changing world.

Stony corals, the engines and engineers of reef ecosystems, face unprecedented threats from anthropogenic environmental change. Corals are holobionts that comprise the cnidarian animal host and a diverse community of bacteria, archaea, viruses and eukaryotic microorganisms. Recent research shows that the bacterial microbiome has a pivotal role in coral biology. A healthy bacterial assemblage contributes to nutrient cycling and stress resilience, but pollution, overfishing and climate change can break down these symbiotic relationships, which results in disease, bleaching and, ultimately, coral death. Although progress has been made in characterizing the spatial-temporal diversity of bacteria, we are only beginning to appreciate their functional contribution. In this Review, we summarize the ecological and metabolic interactions between bacteria and other holobiont members, highlight the biotic and abiotic factors influencing the structure of bacterial communities and discuss the impact of climate change on these communities and their coral hosts. We emphasize how microbiome-based interventions can help to decipher key mechanisms underpinning coral health and promote reef resilience. Finally, we explore how recent technological developments may be harnessed to address some of the most pressing challenges in coral microbiology, providing a road map for future research in this field.

Host nutrient sensing is mediated by mTOR signaling in cnidarian-dinoflagellate symbiosis.

To survive in the nutrient-poor waters of the tropics, reef-building corals rely on intracellular, photosynthetic dinoflagellate symbionts. Photosynthates produced by the symbiont are translocated to the host, and this enables corals to form the structural foundation of the most biodiverse of all marine ecosystems. Although the regulation of nutrient exchange between partners is critical for ecosystem stability and health, the mechanisms governing how nutrients are sensed, transferred, and integrated into host cell processes are largely unknown. Ubiquitous among eukaryotes, the mechanistic target of the rapamycin (mTOR) signaling pathway integrates intracellular and extracellular stimuli to influence cell growth and cell-cycle progression and to balance metabolic processes. A functional role of mTOR in the integration of host and symbiont was demonstrated in various nutritional symbioses, and a similar role of mTOR was proposed for coral-algal symbioses. Using the endosymbiosis model Aiptasia, we examined the role of mTOR signaling in both larvae and adult polyps across various stages of symbiosis. We found that symbiosis enhances cell proliferation, and using an Aiptasia-specific antibody, we localized mTOR to symbiosome membranes. We found that mTOR signaling is activated by symbiosis, while inhibition of mTOR signaling disrupts intracellular niche establishment and symbiosis altogether. Additionally, we observed that dysbiosis was a conserved response to mTOR inhibition in the larvae of a reef-building coral species. Our data confim that mTOR signaling plays a pivotal role in integrating symbiont-derived nutrients into host metabolism and symbiosis stability, ultimately allowing symbiotic cnidarians to thrive in challenging environments.

Temporal and clonal characterization of neural stem cell niche recruitment in the medaka neuromast.

Stem cell populations are defined by their capacity to self-renew and to generate differentiated progeny. These unique characteristics largely depend on the stem cell micro-environment, the so-called stem cell niche. Niches were identified for most adult stem cells studied so far, but we know surprisingly little about how somatic stem cells and their niche come together during organ formation. Using the neuromasts of teleost fish, we have previously reported that neural stem cells recruit their niche from neighboring epithelial cells, which go through a morphological and molecular transformation. Here, we tackle quantitative, temporal, and clonal aspects of niche formation in neuromasts by using 4D imaging in transgenic lines, and lineage analysis in mosaic fish. We show that niche recruitment happens in a defined temporal window during the formation of neuromasts in medaka, and after that, the niche is enlarged mainly by the proliferation of niche cells. Niche recruitment is a non-clonal process that feeds from diverse epithelial cells that do not display a preferential position along the circumference of the forming neuromast. Additionally, we cover niche formation and expansion in zebrafish to show that distant species show common features during organogenesis in the lateral line system. Overall, our findings shed light on the process of niche formation, fundamental for the maintenance of stem cells not only in medaka but also in many other multicellular organisms.