Symbiodinium is a genus of dinoflagellates that encompasses the largest and most prevalent group of endosymbiotic dinoflagellates known and have photosymbiotic relationships with many species. These unicellular microalgae commonly reside in the endoderm of tropical cnidarians such as corals, sea anemones, and jellyfish, where the products of their photosynthetic processing are exchanged in the host for inorganic molecules. They are also harbored by various species of demosponges, flatworms, mollusks such as the giant clams, foraminifera (soritids), and some ciliates. Generally, these dinoflagellates enter the host cell through phagocytosis, persist as intracellular symbionts, reproduce, and disperse to the environment. The exception is in most mollusks, where these symbionts are intercellular (between the cells). Cnidarians that are associated with Symbiodinium occur mostly in warm oligotrophic (nutrient-poor), marine environments where they are often the dominant constituents of benthic communities. These dinoflagellates are therefore among the most abundant eukaryotic microbes found in coral reef ecosystems.
Symbiodinium are colloquially called zooxanthellae, and animals symbiotic with algae in this genus are said to be "zooxanthellate". The term was loosely used to refer to any golden-brown endosymbionts, including diatoms and other dinoflagellates. Continued use of the term in the scientific literature is discouraged because of the confusion caused by overly generalizing taxonomically diverse symbiotic relationships.
In 2018, the systematics of Symbiodiniaceae was revised, and the distinct clades have been reassigned into seven genera. Following this revision, the name Symbiodinium is now sensu stricto a genus name for only species that were previously classified as Clade A. The other clades were reclassified as distinct genera (see Molecular Systematics below).
Intracellular symbionts
Many Symbiodinium species are known primarily for their role as mutualistic endosymbionts. In hosts, they usually occur in high densities, ranging from hundreds of thousands to millions per square centimeter. The successful culturing of swimming gymnodinioid cells from coral led to the discovery that "zooxanthellae" were actually dinoflagellates. Each Symbiodinium cell is coccoid in hospite (living in a host cell) and surrounded by a membrane that originates from the host cell plasmalemma during phagocytosis. This membrane probably undergoes some modification to its protein content, which functions to limit or prevent phago-lysosome fusion. The vacuole structure containing the symbiont is therefore termed the symbiosome. A single symbiont cell occupies each symbiosome. It is unclear how this membrane expands to accommodate a dividing symbiont cell. Under normal conditions, symbiont and host cells exchange organic and inorganic molecules that enable the growth and proliferation of both partners.
Natural services and economic value Symbiodinium is one of the most studied symbionts. Their mutualistic relationships with reef-building corals form the basis of a highly diverse and productive ecosystem. Coral reefs have economic benefits – valued at hundreds of billions of dollars each year – in the form of ornamental, subsistence and commercial fisheries, tourism and recreation, coastal protection from storms, a source of bioactive compounds for pharmaceutical development, and more.
Coral bleaching
The study of Symbiodinium biology is driven largely by a desire to understand global coral reef decline. A chief mechanism for widespread reef degradation has been stress-induced coral bleaching caused by unusually high seawater temperature. Bleaching is the disassociation of the coral and the symbiont and/or loss of chlorophyll within the alga, resulting in a precipitous loss in the animal's pigmentation. Many Symbiodinium-cnidarian associations are affected by sustained elevation of sea surface temperatures, but may also result from exposure to high irradiance levels (including UVR), extreme low temperatures, low salinity and other factors. The bleached state is associated with decreased host calcification, increased disease susceptibility and, if prolonged, partial or total mortality. The magnitude of mortality from a single bleaching event can be global in scale as it was in 2015. These episodes are predicted to become more common and severe as temperatures worldwide continue to rise. The physiology of a resident Symbiodinium species often regulates the bleaching susceptibility of a coral. Therefore, a significant amount of research has focused on characterizing the physiological basis of thermal tolerance and in identifying the ecology and distribution of thermally tolerant symbiont species.
The symbiosis Symbodinium-coral could provide higher resistance to multiple stress (desiccation, high UVR) to the coral holobiont through its mycosporine-like amino acids (MAAs). The concentration of MAAs increases with stress and ROS in Symbodinium. These UV-absorbing MAAs may also support light-harvesting pigments during photosynthesis, be source of nitrogen storage and for reproduction. More than half of the Symbodinium taxa contain MAAs.
Symbiodinium trenchii is a stress-tolerant species and is able to form mutualistic relationships with many species of coral. It is present in small numbers in coral globally and is common in the Andaman Sea, where the water is about 4 °C (7 °F) warmer than in other parts of the Indian Ocean. In the Caribbean Sea in late 2005, water temperature was elevated for several months and it was found that S. trenchii, a symbiont not normally abundant, took up residence in many corals in which it had not previously been observed. Those corals did not bleach. Two years later, it had largely been replaced as a symbiont by the species normally found in the Caribbean.
Symbiodinium thermophilum was recently found to make up the bulk of the algal population inside the corals of the Persian Gulf. It is also present in the Gulf of Oman and the Red Sea, at a much lower concentration. Coral that hosted this species was able to tolerate the waters of the Persian Gulf, much hotter than the of coral reefs globally.
Molecular systematics
The advent of DNA sequence comparison initiated a rebirth in the ordering and naming of all organisms. The application of this methodology helped overturn the long-held belief that (traditional understood) Symbiodinium comprised a single genus, a process which began in earnest with the morphological, physiological, and biochemical comparisons of cultured isolates. Currently, genetic markers are exclusively used to describe ecological patterns and deduce evolutionary relationships among morphologically cryptic members of this group. Foremost in the molecular systematics of Symbiodinium is to resolve ecologically relevant units of diversity (i.e. species).
Phylogenetic disparity among "clades" The earliest ribosomal gene sequence data indicated that Symbiodinium had lineages whose genetic divergence was similar to that seen in other dinoflagellates from different genera, families, and even orders. This large phylogenetic disparity among clades A, B, C, etc. was confirmed by analyses of the sequences of the mitochondrial gene coding for cytochrome c oxidase subunit I (CO1) among Dinophyceae. Most of these clade groupings comprise numerous reproductively isolated, genetically distinct lineages (see 'Species diversity'), exhibiting different ecological and biogeographic distributions (see 'Geographic distributions and patterns of 'diversity').
Recently (2018), these distinct clades within the family of Symbiodiniaceae have been reassigned, although not exclusively, into seven genera: Symbiodinium (understood sensu stricto, i. e. clade A), Breviolum (clade B), Cladocopium (clade C), Durusdinium (clade D), Effrenium (clade E), Fugacium (clade F), and Gerakladium (clade G).
Species diversity
The recognition of species diversity in this genus remained problematic for many decades due to the challenges of identifying morphological and biochemical traits useful for diagnosing species. Presently, phylogenetic, ecological, and population genetic data can be more rapidly acquired to resolve Symbiodinium into separate entities that are consistent with Biological, Evolutionary, and Ecological Species Concepts. Most genetics-based measures of diversity have been estimated from the analysis of one genetic marker (e. g. LSU, ITS2, or cp23S), yet in recent studies these and other markers were analyzed in combination. The high concordance found among nuclear, mitochondrial and chloroplast DNA argues that a hierarchical phylogenetic scheme, combined with ecological and population genetic data, can unambiguously recognize and assign nomenclature to reproductively isolated lineages, i.e. species.
The analysis of additional phylogenetic markers show that some Symbiodinium that were initially identified by slight differences in ITS sequences may comprise members of the same species whereas, in other cases, two or more genetically divergent lineages can possess the same ancestral ITS sequence. When analysed in the context of the major species concepts, the majority of ITS2 sequence data provide a reasonable proxy for species diversity. Currently, ITS2 types number in the hundreds, but most communities of symbiotic cnidaria around the world still require comprehensive sampling. Furthermore, there appears to be a large number of unique species found in association with equally diverse species assemblages of soritid foraminifera, as well as many other Symbiodinium that are exclusively free-living and found in varied, often benthic, habitats. Given the potential species diversity of these ecologically cryptic Symbiodinium, the total species number may never be accurately assessed.
Clone diversity and population genetics Through the use of microsatellite markers, multilocus genotypes identifying a single clonal line of Symbiodinium can be resolved from samples of host tissue. It appears that most individual colonies harbor a single multilocus genotype (i.e. clone). Extensive sampling within colonies confirms that many colonies harbor a homogeneous (clonal) Symbiodinium population. Additional genotypes do occur in some colonies, yet rarely more than two or three are found. When present in the same colony, multiple clones often exhibit narrow zones of overlap. Colonies adjacent to each other on a reef may harbor identical clones, but across the host population the clone diversity of a particular Symbiodinium species is potentially large and comprises recombinant genotypes that are the product of sexual recombination. A clone tends to remain dominant in a colony over many months and years, but may be occasionally displaced or replaced. The few studies examining clone dispersal find that most genotypes have limited geographic distributions, but that dispersal and gene flow is likely influenced by host life history and mode of symbiont acquisition (e. g. horizontal vs. vertical).
Species diversity, ecology, and biogeography Geographic distributions and patterns of diversity
Symbiodinium are perhaps the best group for studying micro-eukaryote physiology and ecology for several reasons. Firstly, available phylogenetic and population genetic markers allow for detailed examination of their genetic diversity over broad spatial and temporal scales. Also, large quantities of Symbiodinium cells are readily obtained through the collection of hosts that harbor them. Lastly, their association with animals provides an additional axis by which to compare and contrast ecological distributions.