Cell proliferation and migration during early development of a symbiotic scleractinian coral

Abstract

In scleractinian reef-building corals, patterns of cell self-renewal, migration and death remain virtually unknown, limiting our understanding of cellular mechanisms underlying initiation of calcification, and ontogenesis of the endosymbiotic dinoflagellate relationship. In this study, we pulse-labelled the coral Stylophora pistillata for 24 h with BrdU at four life stages (planula, early metamorphosis, primary polyp and adult colony) to investigate coral and endosymbiont cell proliferation during development, while simultaneously recording TUNEL-positive (i.e. apoptotic) nuclei. In the primary polyp, the fate of BrdU-labelled cells was tracked during a 3-day chase. The pharynx and gastrodermis were identified as the most proliferative tissues in the developing polyp, and BrdU-labelled cells accumulated in the surface pseudostratified epithelium and the skeletogenic calicodermis during the chase, revealing cell migration to these epithelia. Surprisingly, the lowest cell turnover was recorded in the calicodermis at all stages, despite active, ongoing skeletal deposition. In dinoflagellate symbionts, DNA synthesis was systematically higher than coral host gastrodermis, especially in planula and early metamorphosis. The symbiont to host cell ratio remained constant, however, indicating successive post-mitotic control mechanisms by the host of its dinoflagellate density in early life stages, increasingly shifting to apoptosis in the growing primary polyp.

Do reef corals age?

“…Maximal tissue growth occurs at sites of increasing surface area and not, necessarily, at sites of high skeletal extension. Indeed Lecointe et al (2016) specifically showed very little cellular proliferation in actively calcifying epithelium of Stylophora pistillata. Darke & Barnes (1993) traced the history of individual coral polyps via the growth patterns of their associated corallites (skeletal tubes secreted by the polyp).…”

Host and Symbiont Cell Cycle Coordination Is Mediated by Symbiotic State, Nutrition, and Partner Identity in a Model Cnidarian-Dinoflagellate Symbiosis

“…Several studies have characterized the cell cycles of cnidarian cell populations (21,22) and examined proliferation during development and regeneration (23,24). For example, gastrodermal cells are slower to proliferate than epidermal cells, which must rapidly regenerate new mucocytes and venomous cnidocytes for defense and prey capture.…”

“…As a result of these challenges, there have been only a few studies performed in situ within symbiotic anthozoan tissues that have examined the proliferation of either the cnidarian hosts (47)(48)(49)53), their symbionts (54,55), or both partners (23). Many more symbiont proliferation studies have been performed at an organismal level after substantial manipulations such as macerations or homogenization (40,44,45,(56)(57)(58)(59)(60)(61).…”

Competition and succession among coral endosymbionts

“…One explanation is that a host is not a static habitat. Changes in the host environment, distribution of symbiont cells among tissues, and/or nutrient sharing can occur as hosts grow (Lecointe, Domart‐Coulon, Paris, & Meibom, ) which may alter the competitive hierarchy. Furthermore, while the small size of recruits limited our ability to assess both symbiont genetics and host tissue mass simultaneously, differences in recruit growth among treatments may have fed‐back into competitive outcomes.…”

“…One explanation is that a host is not a static habitat. Changes in the host environment, distribution of symbiont cells among tissues, and/or nutrient sharing can occur as hosts grow (Lecointe, Domart-Coulon, Paris, & Meibom, 2016) which may alter the competitive hierarchy.…”