Clarifying the Taxonomy of Zooxanthellae

Clades to Genera

​Technically the term “zooxanthellae” has no taxonomic meaning, but it is used colloquially to describe the symbiotic golden-colored dinoflagellates that reside within animals (such as corals, anemones, clams, etc.). Zooxanthellae’s small size (the majority are <11 µm in diameter) and similar morphology have made them difficult to study and catalogue, as it is inordinately challenging to distinguish between different species of zooxanthellae without relying on genetic testing (LaJeunesse et al., 2018; Muller-Parker et al., 2015; Toller et al., 2001a).
 
Up until 2018, zooxanthellae were all classified as members of the family Symbiodinium. Members of this family were sorted into “clades” to help differentiate and organize the various zooxanthellae. Seven main clades (i.e., clades A-G) were established, and zooxanthellae were catalogued first by clade and then by “sub-clade” (i.e. “type” or “strain”) using alpha-numeric designations. For example, the designation “A1” indicated that the zooxanthella belonged to clade "A" and sub-clade "1" (LaJeunesse et al., 2018).
 
In 2018, LaJeunesse et al. released a paper redefining these loose clades into seven official genera under the newly established family name: Symbiodiniaceae. In recent years, refinement of DNA analyses revealed that the clades of zooxanthellae were more genetically diverse than previously recognized and that these clades warranted being reclassified as unique new genera in order to help better describe and organize members of the family. The original family name of “Symbiodinium” was repurposed for labeling the new genus that was designated to encompass members specifically of the former clade A. The genera representing the former clades B-G were designated as follows: Breviolum, Cladocopium, Durusdinium, Effrenium, Fugacium, and Gerakladium. Below we describe some of the main characteristics of each of these genera.

The Seven Genera of Symbiodiniaceae

Symbiodinium

Symbiodinium (formerly clade A) is comprised mainly of opportunists and generalists that are shallow-water specialists (LaJeunesse, 2002; LaJeunesse et al., 2018; Toller et al., 2001b). Compared to most other genera of Symbiodiniaceae, members of Symbiodinium are relatively hardy (Riddle, 2016) and under the right conditions they can multiply quickly (Toller et al., 2001b). Symbiodinium are known to produce significant quantities of mycosporine-like amino acids (MMAs) which act as a UV-absorbing “sunscreen” for them, protecting them from damaging UV rays. This adaptation has given Symbiodinium a competitive advantage in high-light environments. Because of this, Symbiodinium is usually found thriving in shallow water, high-light ecosystems (LaJeunesse, 2002; LaJeunesse et al., 2018; Muller-Parker et al., 2015). Symbiodinium is commonly found in symbioses with corals, as well as with clams, anemones, and zoanthids (Muller-Parker et al., 2015; Riddle, 2016). While this genus is globally distributed, it is most commonly found in the Caribbean (LaJeunesse et al., 2018; Riddle, 2016). The name Symbiodinium means “living together” and “whirling” (LaJeunesse et al., 2018).

Breviolum

Breviolum (formerly clade B) is comprised of narrowly adapted specialists that thrive mainly in Caribbean reef environments. While still relatively hardy and resistant to bleaching episodes, this genus is less environmentally tolerant and slower growing than members of Symbiodinium (LaJeunesse et al., 2018; Riddle, 2016; Toller et al., 2001b; ). Breviolum associates primarily with corals but is also commonly found in symbioses with other hosts such as gorgonians and anemones (LaJeunesse et al., 2018; Muller-Parker et al., 2015; Riddle, 2016). Members of Breviolum are some of the smallest Symbiodiniaceae, and their name reflects this, meaning “short” or “small ones” (LaJeunesse et al., 2018).

Cladocopium

Cladocopium (formerly clade C) is the most abundant and broadly distributed genus of Symbiodiniaceae. In addition to being the most abundant genus of Symbiodiniaceae, members of this genus are also the most physiologically diverse. Because of this, Cladocopium associates with a large number of different hosts (LaJeunesse et al., 2018). Similarly to Symbiodinium and Breviolum, Cladocopium prefers tropical reef environments; however, some members of this genus have proven to be better adapted to living in deeper water environments than most members of either Symbiodinium or Breviolum (LaJeunesse et al., 2009; Riddle, 2016; Toller et al., 2001b). While most commonly associated with Indo-Pacific corals, Cladocopium can be found globally in symbioses with corals, clams, ciliates, flatworms, and sponges, among other hosts (LaJeunesse, 2002; LaJeunesse et al., 2018; Muller-Parker et al., 2015; Riddle, 2016). The name Cladocopium means “branch” and “plenty” (LaJeunesse et al., 2018).

Durusdinium

Durusdinium (formerly clade D; also formerly described as clade E in research by Toller et al.) is comprised of stress-resistant and opportunistic generalists (Toller et al., 2001b). Research has found Durusdinium to be exceptionally tolerant to environmental stressors, including fluctuations in temperature, salinity, nutrients, sediments, turbidity, air exposure, rainfall, and light intensity (LaJeunesse et al., 2018; Muller-Parker et al., 2015; Toller et al., 2001​a). Durusdinium is commonly found in symbioses with corals, especially those corals settled in less than favorable environments, like nearshore coastal reefs, coastal lagoons, and tidal pools where conditions are harsher (Mashini et al., 2015; Muller-Parker et al., 2015; Toller et al., 2001a; Toller et al., 2001b). These extremophiles have adaptations that help them tolerate these hostile conditions and in turn bolster their host’s immunity to environmental stressors (LaJeunesse et al., 2009; LaJeunesse et al., 2018). Research has shown that corals in symbioses primarily with members of Durusdinium are more likely to resist bleaching, survive through bleaching events, and recover from bleaching (Baker, 1999; Baker et al., 2004; LaJeunesse et al., 2009; LaJeunesse et al., 2018; Manzello et al., 2018, Toller et al., 2001a; Toller et al., 2001b; Wang et al., 2022). The name Durusdinium means “tough” and “whirling” (LaJeunesse et al., 2018).

Effrenium

Effrenium (formerly clade E) is comprised of just a single species: Effrenium voratum. E. voratum is unique in that it is exclusively free-living (non-symbiotic). Its cell size is also the largest in volume of all Symbiodiniaceae. The name Effrenium means “living unrestrained” (LaJeunesse et al., 2018).

Fugacium

Fugacium (formerly a sub-clade of clade F) has been found in association with Foraminifera (i.e., subphylum of single-celled protists, similar to amoebas). There are also some species of Fugacium that are non-symbiotic. Little is known about this cryptic genus of Symbiodiniaceae. The name Fugacium means “ephemeral” (LaJeunesse et al. 2018).

Gerakladium

Like Fugacium, Gerakladium (formerly a sub-clade of clade G) is another genus of Symbiodiniaceae that we still have much to learn about. It is known to form symbiotic relationships with members of Clionaida (i.e., an order of demosponges) and Antipatharia (i.e., black coral), and occasionally with members of Scleractinia (i.e., stony corals). Gerakladium has remained largely unchanged throughout the evolutionary history of Symbiodiniaceae, and its name reflects this, meaning “old” and “branch” (LaJeunesse et al., 2018).

---

References

[1] Baker, A. C. (1999). Symbiosis ecology of reef-building corals. Ph.D. dissertation. University of Miami.
 
[2] Baker, A. C., Starger, C. J., McClanahan, T. R., & Glynn, P. W. (2004). Corals' adaptive response to climate change. Nature.
 
[3] LaJeunesse, T. C. (2002). Diversity and community structure of symbiotic dinoflagellates from Caribbean coral reefs. Marine Biology.
 
[4] LaJeunesse, T. C., Smith, R. T., Finney, J., & Oxenford, H. (2009). Outbreak and persistence of opportunistic symbiotic dinoflagellates during the 2005 Caribbean mass coral 'bleaching' event. Proceedings of The Royal Society. 276(1676).
 
[5] LaJeunesse, T. C., Parkinson, J. E., Gabrielson, P. W., Jeong, H. J., Reimer, J. D., Voolstra, C. R., & Santos, S. R. (2018). Systematic revision of Symbiodiniaceae highlights the antiquity and diversity of coral endosymbionts. Current Biology, 28(16).
 
[6] Manzello, D. P., Matz, M. V., Enochs, I. C., Valentino, L., Carlton, R. D., Kolodziej, G., Serrano, X., Towle, E. K., & Jankulak, M. (2019). Role of host genetics and heat-tolerant algal symbionts in sustaining populations of the endangered coral Orbicella faveolata in the Florida Keys with ocean warming. Global Change Biology. 25(3).
 
[7] Mashini, A. G., Parsa, S., & Mostafavi, P. G. (2015). Comparison of Symbiodinium populations in corals from subtidal region and tidal pools of northern coasts of Hengam Island, Iran. Journal of Experimental Marine Biology and Ecology, 473.
 
[8] Muller-Parker, G., D’Elia, C.F., & Cook, C.B. (2015). Interactions between corals and their symbiotic algae. In: Birkeland, C. (eds) Coral Reefs in the Anthropocene.
 
[9] Riddle, D. (2016). An update on Symbiodinium species and their hosts. Advanced Aquarist.
 
[10] Toller, W. W., Rowan, R., & Knowlton, N. (2001a). Zooxanthellae of the Montastraea annularis species complex: patterns of distribution of four taxa of Symbiodinium on different reefs and across depths. Biological Bulletin, 201(3).
 
[11] Toller, W. W., Rowan, R., & Knowlton, N. (2001b). Repopulation of zooxanthellae in the Caribbean corals Montastraea annularis and M. faveolata following experimental and disease-associated bleaching. Biological Bulletin. 201(3).
 
[12] Wang, C., Zheng, X., Li, Y., Sun, D., Huang, W., & Shi, T. (2022). Symbiont shuffling dynamics associated with photodamage during temperature stress in coral symbiosis. Ecological Indicators, 145.