Symbiotic microalgae of the family Symbiodiniaceae, sometimes referred to as zooxanthellae, engage in trophic symbioses with corals and many other marine organisms. These mutualistic partnerships, in which the microalgae live as endosymbionts inside the host tissue and provide their host with sugars and other organic nutrients in exchange for protection and inorganic nutrients, play a pivotal role in sustaining the productivity and diversity of coral reefs. In fact, these symbioses are of such fundamental importance for coral reefs that symbiodiniaceans are considered keystone species in these important ecosystems and have been referred to as the “engines of the reef”. Commonly less known is that parallel to evolving intricate symbiotic life histories, many symbiodiniaceans preserved the ability to live as free-living cells outside of their hosts. These environmental populations represent an important pool from which hosts acquire their symbionts and are increasingly recognised for maintaining the functional diversity of host-symbiont associations. However, beyond comprehending their reef ecological significance, little is known about the biology of free-living symbiodiniaceans. Benthic habitats, especially reef sands, appear to be hotspots for symbiodiniaceans but again, how these benthic populations live and how they are adapted to this habitat has remained elusive for decades.
An unexpected new impulse for the study of benthic symbiodiniaceans came from our discovery that in culture these dinoflagellates commonly form calcifying bacterial-algal communities that precipitate sand grain-like calcium carbonate deposits and encase themselves as viable endolithic cells. The formation of these microbialites, we termed symbiolites, provided first circumstantial evidence for the existence of a constructed endolithic niche of symbiodiniaceans. Subsequently, also direct support for this hypothesis emerged, as we discovered diverse endolithic symbiodiniacean communities in reef sands at Heron Island, Great Barrier Reef, Australia, via a metabarcoding approach.
The discovery of endolithic symbiodiniaceans represents a breakthrough in uncovering the life history of symbiodiniaceans in benthic reef habitats. It also fundamentally changes our understanding of the wider biology and ecology of these microalgae, as e.g. the endolithic niche is known to protect from negative influences such as ultraviolet radiation (UVR), providing symbiodiniaceans with a previously unknown protective environment on the reef. The existence of endolithic symbiodiniaceans also offers new conceptual perspectives on the constructed endolithic niche itself and suggests that symbiodiniaceans could play a previously unknown role in the microbial calcification of reef sediments, a process that is induced by the effect of microbial activity such as microalgal photosynthesis on the calcium carbonate system in seawater and that leads to the net-growth of reef sand grains. It is therefore alarming that the carbonate reef sands that harbour endolithic symbiodiniaceans are predicted to become net-dissolving due to ocean acidification (OA) well within the next century, threatening the newly discovered endolithic niche of these microalgae before its significance is fully explored.
The aims of this project fall into three lines of investigation. One is to identify potential functions of living in a constructed endolithic niche, by studying the photobiology of symbiolites and of natural reef sand grains experimentally under UVR in vitro. Another line is to experimentally test in situ, on the reef, if the mineral precipitation mechanisms that allow symbiodiniaceans to produce symbiolites in vitro also drive their entry into the endolithic niche in reef sands; to assess if these mechanisms vary seasonally with changes in light and temperature; and to address the pressing question of whether predicted OA could prevent symbiodiniaceans from entering the endolithic niche altogether by impeding the underlying pH-related mineral precipitation mechanisms. Parallel, we aim to characterise the bacterial communities and their dynamics in order to evaluate their role in the symbiodiniacean-induced calcification process in situ with that in culture. As a third line of investigation, we aim to identify novel symbiodiniacean taxa in endolithic reef sand communities in order to enable future studies on their functional diversity and potential niche adaptations. The results of these lines of investigation will provide important new resources and insights into the function of the endolithic niche; the processes that underpin the establishing of the endolithic niche; the physicochemical and biological factors that influence these processes; and how they will change in more acidic oceans of the future. Combined, this represents a concerted push to explore a novel microbial frontier within coral reefs and its significance in these threatened ecosystems.
