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A role for primary cilia in coral calcification?

ABSTRACT: Cilia are evolutionarily conserved organelles that extend from the surface of cells and are found in diverse organisms from protozoans to multicellular organisms. Motile cilia play various biological functions by their beating motion, including mixing fluids and transporting food particles. Non-motile cilia act as sensors that signal cells about their microenvironment. In corals, cilia have been described in some of the cell layers but never in the calcifying epithelium, which is responsible for skeleton formation. In the present study, we used scanning electron microscopy and immunolabelling to investigate the cellular ciliature of the different tissue layers of the coral Stylophora pistillata, with a focus on the calcifying calicoblastic ectoderm. We show that the cilium of the calcifying cells is different from the cilium of the other cell layers. It is much shorter, and more importantly, its base is structurally distinct from the base observed in cilia of the other tissue layers. Based on these structural observations, we conclude that the cilium of the calcifying cells is a primary cilium. From what is known in other organisms, primary cilia are sensors that signal cells about their microenvironment. We discuss the implications of the presence of a primary cilium in the calcifying epithelium for our understanding of the cellular physiology driving coral calcification and its environmental sensitivity.

SUBMITTER: Tambutte E

PROVIDER: S-EPMC7960582 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:The North Atlantic Oscillation (NAO) has been hypothesized to drive interannual variability in Bermudan coral extension rates and reef-scale calcification through the provisioning of nutritional pulses associated with negative NAO winters. However, the direct influence of the NAO on Bermudan coral calcification rates remains to be determined and may vary between species and reef sites owing to implicit differences in coral life history strategies and environmental gradients across the Bermuda reef platform. In this study, we investigated the connection between negative NAO winters and Bermudan Diploria labyrinthiformis, Pseudodiploria strigosa, and Orbicella franksi coral calcification rates across rim reef, lagoon, and nearshore reef sites. Linear mixed effects modeling detected an inverse correlation between D. labyrinthiformis calcification rates and the winter NAO index, with higher rates associated with increasingly negative NAO winters. Conversely, there were no detectable correlations between P. strigosa or O. franksi calcification rates and the winter NAO index suggesting that coral calcification responses associated with negative NAO winters could be species-specific. The correlation between coral calcification rates and winter NAO index was significantly more negative at the outer rim of the reef (Hog Reef) compared to a nearshore reef site (Whalebone Bay), possibly indicating differential influence of the NAO as a function of the distance from the reef edge. Furthermore, a negative calcification anomaly was observed in 100% of D. labyrinthiformis cores in association with the 1988 coral bleaching event with a subsequent positive calcification anomaly in 1989 indicating a post-bleaching recovery in calcification rates. These results highlight the importance of assessing variable interannual coral calcification responses between species and across inshore-offshore gradients to interannual atmospheric modes such as the NAO, thermal stress events, and potential interactions between ocean warming and availability of coral nutrition to improve projections for future coral calcification rates under climate change.

Project description:UnlabelledBackgroundThe central tenet of cilia function is sensing and transmitting information. The capacity to directly contact extracellular surfaces would empower primary cilia to probe the environment for information about the nature and location of nearby surfaces. It has been well established that flagella and other motile cilia perform diverse cellular functions through adhesion. We hypothesized that mammalian primary cilia also interact with the extracellular environment through direct physical contact.MethodsWe identified cilia in rod photoreceptors and cholangiocytes in fixed mouse tissues and examined the structures that these cilia contact in vivo. We then utilized an MDCK cell culture model to characterize the nature of the contacts we observed.ResultsIn retina and liver tissue, we observed that cilia from nearby cells touch one another. Using MDCK cells, we found compelling evidence that these contacts are stable adhesions that form bridges between two cells, or networks between many cells. We examined the nature and duration of the cilia-cilia contacts and discovered primary cilia movements that facilitate cilia-cilia encounters. Stable adhesions form as the area of contact expands from a single point to a stretch of tightly bound, adjacent cilia membranes. The cilia-cilia contacts persisted for hours and were resistant to several harsh treatments such as proteases and DTT. Unlike many other cell adhesion mechanisms, calcium was not required for the formation or maintenance of cilia adhesion. However, swainsonine, which blocks maturation of N-linked glycoproteins, reduced contact formation. We propose that cellular control of adhesion maintenance is active because cilia adhesion did not prevent cell division; rather, contacts dissolved during mitosis as cilia were resorbed.ConclusionsThe demonstration that mammalian primary cilia formed prolonged, direct, physical contacts supports a novel paradigm: that mammalian primary cilia detect features of the extracellular space, not just as passive antennae, but also through direct physical contact. We present a model for the cycle of glycoprotein-dependent contact formation, maintenance, and termination, and discuss the implications for potential physiological functions of cilia-cilia contacts.

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A role for primary cilia in coral calcification?

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