Zooxanthellae

What are zooxanthellae? Until recently, all unicellular microalgae of yellow or brownish color found in animals or protists were customarily referred to as ‘zooxanthellae’, an antiquated term coined in the late 1800s. Animals that depend on photo-symbionts for their well-being were said to be zooxanthellate. In recent decades, advances in light and electron microscopy, combined with emerging molecular–genetic evidence, led to the realization that these photosynthetic symbionts represented many unrelated phyla of microeukaryotes. However, the large majority of ‘zooxanthellae’ are mutualistic dinoflagellates in the order Dinophyceae found in many shallow-water invertebrates (notably reef-forming corals), and in a few kinds of unicellular forams and ciliates. Dinoflagellates are a large and diverse group noted for their importance in plankton communities, as agents of harmful algal blooms (e.g., red tides) and in creating bioluminescence in the ocean. They share a recent common ancestor with the largely endoparasitic phylum Apicomplexa, some of which cause diseases such as malaria and toxoplasmosis. In the second half of the 20th Century most dinoflagellate zooxanthellae were formally classified in the genus Symbiodinium; and originally thought to comprise one widespread species, Symbiodinium microadriaticum. However, the substantial genetic divergence between phylogenetic clades and large differences in their genomic compositions led to recent reorganization into multiple genera (currently nine) within the family Symbiodiniaceae, while other dinoflagellate orders and families contain symbiotic species, the family Symbiodiniaceae (order Suessiales) is by far the most geographically widespread and ecologically important. Why are symbiodiniacean zooxanthellae important? Reef-building corals are ultimately reliant on the sun’s radiance for their survival and growth. These stony corals, as well as many other non-reef forming species, depend on nutrients from the photosynthetic activities of their resident dinoflagellates. These small symbionts (ranging from 5–13 μm) occur in host tissues at densities numbering millions of cells per square centimeter. In most cases, about 20 to 50 of organic compounds (glucose, amino acids, etc.) produced by these algae are delivered to their hosts as fuel for metabolically expensive processes such as tissue growth, and for reef corals in particular, constructing calcium carbonate skeletons. It is estimated that these nutrients fulfill much of the daily metabolic needs for most hosts. Further, these animals also acquire food by actively feeding on prey and particulates, and the byproducts of digestion and respiration (i.e., inorganic compounds) are absorbed rapidly by the symbionts for their own cellular maintenance and growth. Ultimately, this intimate mutualism is the basis for the existence of all shallow-water coral reefs on Earth — and explains why these systems are so productive in nutrient-poor waters. How ecologically diverse and geographically widespread are Symbiodiniaceae? Numerous invertebrate phyla, including the Cnidaria (e.g., reef corals, sea anemones, sea fans, jellyfish), Mollusca (e.g. giant clams), Porifera (sponges), and Platyhelminthes (flat worms), as well as some ciliates and foraminifera (soritids), harbor symbiodiniacean species. These hosts occur in shallow marine habitats ranging from tropical to temperate latitudes. There are likely hundreds of undescribed species in the family Symbiodiniaceae, each with distinct ecological attributes and geographic distributions, including species that are host-specific and regionally endemic to those that associate with many kinds of hosts across vast areas of ocean like the Indo-Pacific. The genus Cladocopium alone probably comprises hundreds of species. The host-as-habitat lifestyle appears to exert strong selection pressure generating many host-specialized symbionts, especially during adaptive radiations lasting many thousands or millions of years (see below). While it is true that not all symbiotic dinoflagellates are Symbiodiniaceae, it is also true that not all Symbiodiniaceae are symbiotic. Certain species from several different genera are exclusively free-living and therefore non-symbiotic. Over the evolutionary history of this family, there are lineages (both species and genera) that have apparently lost the capacity to form mutualistic endosymbioses, but it remains unclear as to the nature of their ecology and how they may contribute to marine microbial food webs. How long have their mutualisms existed? The evolutionary history of mutualisms involving Symbiodiniaceae extends back to the very origins of dinoflagellates and the corals responsible for building reefs today. Extant dinoflagellate orders originated during a major adaptive radiation over 200 million years ago, coinciding with a time when modern reef-building corals began to diversify and occupy warm coastal habitats in great abundance. Molecular clock estimates place the origins of the most ancestral lineage of Symbiodiniaceae in the early to mid-Jurassic period, when corals reached their peak rates of diversification following a long recovery from the end-Triassic mass extinction. Therefore, the origin of modern coral reef ecosystems began in the Mesozoic era facilitated by the emergence of animal–dinoflagellate mutualisms. By proxy, non-fossilizing Cnidaria and other invertebrate lineages must have evolved their symbioses at some point over this large span of time. The broader implication is that these partnerships have endured an immense span of geological time and large changes in the Earth’s climate. Who controls the mutualism? It is unclear how much the host influences control over its symbionts, and vice versa. Ultimately, both partners likely share in regulating the mutualism. We still know very little about the underlying cellular/biochemical exchanges and communication between animal and algal cells. These partnerships are particularly complicated because, unlike the multitude of symbioses between animals and bacteria, the constituents of this mutualism are both eukaryotic (most other endosymbiotic eukaryotes are parasites or pathogens; e.g., Apicomplexa). There is little indication that the host necessarily has direct control over the identity of the residing symbiont. Host ‘flexibility’ in nature is limited to a small number of compatible symbiont species whose abundance in host individuals is governed by prevailing external environmental conditions. Indeed, some partner pairings can be manipulated artificially by moving colonies to new habitats, or subjecting them to prolonged thermal stress. Given the intracellular nature of the relationship, the host cell’s plasma membrane and cytoplasm, as well as the surrounding host-derived symbiosome membrane, constitute a barrier limiting the symbiont cell’s access to the outside world (Figure 1). In this physical sense, the host exerts ‘control’ over the symbiont. Nutrient availability can ‘regulate’ the symbiont’s population densities, but evidence of the host’s ability to actively modulate symbiont nutrition remains equivocal. However, the symbiont likely has its own means of influencing the host. The symbiont cell has twice as many genes as the host cell, and its genome is an order of magnitude larger. Moreover, dinoflagellates generate a variety of secondary metabolites. How the expression of large numbers of genes and the release of biologically active compounds interact with, for example, the host cell’s innate immune system is largely unknown. The origins of this mutualism likely evolved out of what was initially a parasitism. Therefore, present-day symbionts likely possess mechanisms for evading cellular digestion and host immune responses. With a few exceptions, individual reef corals harbor a single dominant symbiodiniacean species. Moreover this ‘resident symbiont population’ is often mono-clonal, originating from a single symbiont cell proliferating through mitotic division to dominate the entire host colony as the animal itself buds polyps and grows larger. In colonies where more than one symbiont is co-abundant, the other dominant symbiont is almost always a member of a different genus. Nevertheless, barring episodes of severe stress, the more common one–host–clone: one–symbiont–clone relationship remains stable for years and possibly over the life of the animal. Which symbionts are important to reef corals imperiled by climate warming? Sea-surface heat waves create worrying episodes of widespread coral beaching (i.e., colony whitening from losing their pigmented symbionts) and mass mortality across many reefs (Figure 1). High (and sometimes low) temperatures destabilize these symbioses, and the loss in symbiont physiological integrity is often to blame when these partnerships fall apart. Corals with stress-adapted symbionts are more tolerant of warming episodes and less likely to ‘bleach’ and die. Therefore, when forecasting the responses of reef corals to global warming, the ecological attributes and physiological capabilities of each symbiont species must be considered. Studying coral communities that persist in extreme habitats, such as warm inshore environments (e.g., the rock islands of Palau) and shallow seas (e.g., the Persian–Arabian Gulf), provides insight into the possible make-up and viability of coral–algal mutualisms in a warmer future. For example, we know that small numbers of host-generalist and host-specialized symbiont species that are tolerant of environmental stressors typically dominate coral populations found in these extreme environments. We have also learned that the low symbiont diversity observed in these habitats reflects phylogenetic patterns, which suggest that major climate shifts over geological time drove bottlenecks in symbiont diversity (more so than for hosts) and favored the geographic spread and ecological success of only a few symbionts that were better adapted to the new prevailing environment. Over time, these symbionts diversified into numerous species as populations became reproductively isolated as a consequence of ecological specialization and geographical separation. Adaptive radiations of this sort appear to have occurred in different ocean basins during the recent Pliocene and Pleistocene epochs. The comparatively fast warming rates of today, however, may limit the extent to which these mutualisms can respond, both ecologically and evolutionarily, as they have done in the past. More research is needed to better predict the outcomes of climate change on these symbionts and their hosts.