I love to take any opportunity I get to learn more about coral. Recently I got a chance to really deep dive into the symbiotic organisms (Symbiodinium) responsible for coral photosynthesis. I used my Biology class phylogeny paper to learn about these amazing organisms and their relationship with coral. The results of the phylogeny paper were fairly anti-climactic, but if you’re really curious, you can read it here. The things I learned about Symbiodinium, on the other hand – totally fascinating! So I’ll share the interesting stuff with you here:
Introduction
One of the many reasons coral reefs are so remarkable and unique is the symbiotic relationship between the heterotrophic coral species and the unicellular algae most commonly known as “zooxanthellae”. The term “zooxanthellae” is used to refer to an enormous and incredibly diverse group of endo-symbionts including many diatoms and dinoflagellates (LaJeunesse et al. 2012). This is confusing as it generalizes taxonomically diverse symbiotic relationships and is generally discouraged from use. (Blank & Trench 1986).
The Symbiodinium are part of the Phylum Dinophyta (Dinoflagellates) and the clade Alveolates. Because of the diversity of species and the complexity of clades and taxonomic groupings for these organisms, they are better and more accurately referred to by their genus “Symbiodinium” which encompasses an enormous group of endosymbiotic dinoflagellates. Symbiodinium organisms are a unicellular algae that are found in the endoderm of tropical cnidarians that include coral as well as a number of other species. Symbiodinium are an autotrophic organism that provides its host with essential sugars and amino-acids via photosynthesis so that the coral host can build its calcified structures. The symbiont in turn is protected and provided with a high-light environment as well as inorganic nutrients like nitrogen and carbon. This nutrient-sharing relationship is an important part of building and maintaining reef ecosystems given that they occur mostly in warm oligotrophic (nutrient-poor) marine environments. (LaJeunesse et al. 2012; Pochon, Xavier, et al. 2012).
Symbiodinium goes through two main phases in its life cycle – a mastigote stage (fig. 1a) where the cell is motile and a coccoid stage (fig. 1b) where the cell is non-motile. In the motile stage, the organism can find a host through chemotaxis towards sources of nitrogen. Once they are within the host, in their spherical coccoid stage, they replicate quickly and can dominate the cytoplasm of the host cell. (LaJeunesse et al. 2012).
Figure 1. These electron micrographs show the two stages of the Symbiodinium organism; (A) mastigote (motile cell). (B) the coccoid cell in hospite. (LaJeunesse et al. 2012).
Symbiodinium enters the host organism through phagocytosis and exists within the host tissues in vacuole-like structures called symbiosomes. During phagocytosis, the organism is surrounded by a membrane that originates from the host cell plasmalemma (Fig. 2) which may undergo some modification to its proteins in order to protect it from actually being digested. (LaJeunesse et al. 2012).
Figure 2. This is a SEM of a freeze-fractured internal mesentery from a reef coral polyp (Porites porites) that shows the distribution and density of symbiont cells within the tissue of the host. © Todd LaJeunesse. (LaJeunesse et al. 2012).
Although there is still much we don’t know about the Symbiodinium organisms, there have been significant, recent gains in knowledge about them. This is due to a desire to understand and prevent the decline of reef-building coral species. Coral bleaching is a condition defined by the dissociation of the coral and its symbiont and/or by a loss of pigmentation in the Symbiodinium agal organism. This dissociation is caused by a number of environmental stressors including high temperatures, high levels of solar irradiance, and changes in pH. When this happens, the host loses a source of nutrition and may starve, it is also more susceptible to disease, and loss of calcification. (LaJeunesse et al. 2012).
Because of the severity of bleaching events, a great deal of research has gone into better understanding the relationship between host and symbiont (LaJeunesse et al. 2012). The degree to which Symbiodinium organisms are affected by heat, light, and pH varies by species (Hoogenboom et al. 2012). A better understanding of the phylogenetic relationship between Symbiodinium species can help us better understand the group as a whole and the symbiotic relationship it shares with its hosts. Ultimately, this understanding can lead to methods for protecting and restoring coral and ultimately the entire ocean ecosystem.
Figure 3. This photo of “whitened” reef-building corals was taken off the coast of Barbados during the Fall 2005 Caribbean mass coral bleaching event. This photo illustrates a coral in the process of losing (dissociating from) its symbiont. © Hazel Oxenford. (LaJeunesse et al. 2012).
Aside from some differences in cell size, there are very few morphological characteristics that can be used to identify Symbiodinium species (S. Y. Lee et al. 2015). Because of this, genetic analysis is the primary means of species identification. Researchers have found that species diversity appears to be distributed non-randomly, can be grouped into ecological guilds with distinct habits, and is host-specific. Additionally, hosts usually only support a single Symbiodinium species – only a few cases are known where two or three symbiont species are present. ( LaJeunesse 2002).
The phylogenetic and taxonomic methods of grouping and organizing different Symbiodinium species is an evolving and growing subject. Species diversity is vast with a number of factors that can affect the distribution of species including their dispersal ability, host biogeography, and external environmental conditions. LaJeunesse et al. 2012).
References Cited
Bongaerts, Pim, et al. “Sharing the Slope: Depth Partitioning of Agariciid Corals and Associated Symbiodinium Across Shallow and Mesophotic Habitats (2-60 m) on a Caribbean Reef.” BMC Evolutionary Biology, vol. 13, 2013, pp. 205. ProQuest, https://libproxy.pcc.edu/login?url=https://www-proquest-com.libproxy.pcc.edu/scholarly-journals/sharing-slope-depth-partitioning-agariciid-corals/docview/1445010562/se-2?accountid=8042, doi:http://dx.doi.org.libproxy.pcc.edu/10.1186/1471-2148-13-205.
Correa, A.M.S., Baker, A.C. Understanding diversity in coral-algal symbiosis: a cluster-based approach to interpreting fine-scale genetic variation in the genus Symbiodinium . Coral Reefs 28, 81–93 (2009). https://doi.org/10.1007/s00338-008-0456-6
Hoogenboom MO, Campbell DA, Beraud E, DeZeeuw K, Ferrier-Page`s C (2012) Effects of Light, Food Availability and Temperature Stress on the Function of Photosystem II and Photosystem I of Coral Symbionts. PLoS ONE 7(1): e30167. doi:10.1371/journal.pone.0030167
LaJeunesse, Todd, John E. Parkinson, and Robert K. Trench. 2012. Symbiodinium. Version 04 July 2012. http://tolweb.org/Symbiodinium/126705/2012.07.04 in The Tree of Life Web Project, http://tolweb.org/
Pochon, Xavier, et al. “Identifying and Characterizing Alternative Molecular Markers for the Symbiotic and Free-Living Dinoflagellate Genus Symbiodinium.” PLoS One, vol. 7, no. 1, 2012. ProQuest, https://libproxy.pcc.edu/login?url=https://www-proquest-com.libproxy.pcc.edu/scholarly-journals/identifying-characterizing-alternative-molecular/docview/1322368153/se-2?accountid=8042, doi:http://dx.doi.org.libproxy.pcc.edu/10.1371/journal.pone.0029816.
Sung Yeon Lee, Hae Jin Jeong, Nam Seon Kang, Tae Young Jang, Se Hyeon Jang & Todd C. Lajeunesse (2015) Symbiodinium tridacnidorum sp. nov., a dinoflagellate common to Indo-Pacific giant clams, and a revised morphological description of Symbiodinium microadriaticum Freudenthal, emended Trench & Blank, European Journal of Phycology, 50:2, 155-172, DOI: 10.1080/09670262.2015.1018336
References
Aranda M, Li Y, Liew YJ, Baumgarten S, Simakov O, Wilson MC, Piel J, Ashoor H, Bougouffa S, Bajic VB, Ryu T, Ravasi T, Bayer T, Micklem G, Kim H, Bhak J, LaJeunesse TC, Voolstra CR. Genomes of coral dinoflagellate symbionts highlight evolutionary adaptations conducive to a symbiotic lifestyle. Sci Rep. 2016 Dec 22;6:39734. doi: 10.1038/srep39734. PMID: 28004835; PMCID: PMC5177918.
Daniel J. Barshis, Jason T. Ladner, Thomas A. Oliver, Stephen R. Palumbi, Lineage-Specific Transcriptional Profiles of Symbiodinium spp. Unaltered by Heat Stress in a Coral Host, Molecular Biology and Evolution, Volume 31, Issue 6, June 2014, Pages 1343–1352, https://doi.org/10.1093/molbev/msu107
Hiroko Yokouchi, Haruko Takeyama, Hideaki Miyashita, Tadashi Maruyama, Tadashi Matsunaga, In situ identification of symbiotic dinoflagellates, the genus Symbiodinium with fluorescence-labeled rRNA-targeted oligonucleotide probes, Journal of Microbiological Methods, Volume 53, Issue 3, 2003, Pages 327-334, ISSN 0167-7012, https://doi.org/10.1016/S0167-7012(02)00250-6. (https://www.sciencedirect.com/science/article/pii/S0167701202002506)
Howells EJ, Beltran VH, Larsen NW, Bay LK, Willis BL, et al. (2012) Coral thermal tolerance shaped by local adaptation of photosymbionts. Nature Clim Change 2: 116–120.
Kate M. Quigley, Sarah W. Davies, Carly D. Kenkel, Bette L. Willis, Mikhail V. Matz, Line K. Bay. “Deep-Sequencing Method for Quantifying Background Abundances of Symbiodinium Types: Exploring the Rare Symbiodinium Biosphere in Reef-Building Corals.”
Michael Stat, Andrew C. Baker, David G. Bourne, Adrienne M.S. Correa, Zac Forsman, Megan J. Huggett, Xavier Pochon, Derek Skillings, Robert J. Toonen, Madeleine J.H. van Oppen, Ruth D. Gates, Chapter One – Molecular Delineation of Species in the Coral Holobiont, Editor(s): Michael Lesser, Advances in Marine Biology, Academic Press, Volume 63, 2012, Pages 1-65, ISSN 0065-2881, ISBN 9780123942821, https://doi.org/10.1016/B978-0-12-394282-1.00001-6. (https://www.sciencedirect.com/science/article/pii/B9780123942821000016)
Michael Stat, Andrew C. Baker, David G. Bourne, Adrienne M.S. Correa, Zac Forsman, Megan J. Huggett, Xavier Pochon, Derek Skillings, Robert J. Toonen, Madeleine J.H. van Oppen, Ruth D. Gates, Chapter One – Molecular Delineation of Species in the Coral Holobiont, Editor(s): Michael Lesser, Advances in Marine Biology, Academic Press, Volume 63, 2012, Pages 1-65, ISSN 0065-2881, ISBN 9780123942821, https://doi.org/10.1016/B978-0-12-394282-1.00001-6. (https://www.sciencedirect.com/science/article/pii/B9780123942821000016)
Michele X. Weber, Mónica Medina, Chapter Four – The Role of Microalgal Symbionts (Symbiodinium) in Holobiont Physiology, Editor(s): Gwenaël Piganeau, Advances in Botanical Research, Academic Press, Volume 64, 2012, Pages 119-140, ISSN 0065-2296, ISBN 9780123914996, https://doi.org/10.1016/B978-0-12-391499-6.00004-9. (https://www.sciencedirect.com/science/article/pii/B9780123914996000049)
LaJeunesse et al., Systematic Revision of Symbiodiniaceae Highlights the Antiquity and Diversity of Coral Endosymbionts, Current Biology (2018), https://doi.org/10.1016/j.cub.2018.07.008
LaJeunesse, .T. Diversity and community structure of symbiotic dinoflagellates from Caribbean coral reefs. Marine Biology 141, 387–400 (2002). https://doi.org/10.1007/s00227-002-0829-2
Lajeunesse, Todd C., Parkinson, John E., Reimer, James D., A Genetics-based Description Of Symbiodinium Minutum sp. Nov. And S. Psygmophilum Sp. Nov. (dinophyceae), Two Dinoflagellates Symbiotic With Cnidaria, Department of Biology, The Pennsylvania State University, University Park, Pennsylvania, 16802, USA, DOI: 10.1111/j.1529-8817.2012.01217.x
Liew YJ, Li Y, Baumgarten S, Voolstra CR, Aranda M (2017) Condition-specific RNA editing in the coral symbiont Symbiodinium microadriaticum. PLoS Genet 13(2): e1006619. https://doi.org/10.1371/journal.pgen.1006619
Quigley, Kate M., et al. “Deep-Sequencing Method for Quantifying Background Abundances of Symbiodinium Types: Exploring the Rare Symbiodinium Biosphere in Reef-Building Corals.” PLoS One, vol. 9, no. 4, 2014. ProQuest, https://libproxy.pcc.edu/login?url=https://www-proquest-com.libproxy.pcc.edu/scholarly-journals/deep-sequencing-method-quantifying-background/docview/1515291632/se-2?accountid=8042, doi:http://dx.doi.org.libproxy.pcc.edu/10.1371/journal.pone.0094297.
Wepfer, Patricia H. et al. “Metacommunity ecology of Symbiodiniaceae hosted by the coral Galaxea fascicularis.” Marine Ecology Progress Series 633 (2020): 71-87.
Erica Lauer Vose 