Introduction to Symbiodinium

Many of the invertebrate organisms that inhabit reefs form a symbiosis with unicellular algae of the genus Symbiodinium. While the host organisms can be giant clams, anemone’s, soft corals, fire corals and hydroids the best known association is formed with hard or ‘scleractinian’ corals. The symbionts live inside the endodermal layer of their host and provide the majority of daily energy requirements (Muscatine and Porter 1977). As a result corals cannot survive prolonged loss of the symbionts during episodes of stress without impacting their survival. While many factors threaten the persistence of coral reefs, increasing sea surface temperature (SST) disrupting the symbiosis (aka coral bleaching) is regarded as a primary threat and has caused substantial mortality of reef invertebrates over the last two decades (Hoegh-Guldberg 1999; Hughes et al. 2003; Pandolfi et al. 2003).

Significance

Symbiodinium has received a lot of research attention in the past decade stimulated by the need to understand coral reef deterioration. On the Great Barrier Reef (GBR) alone at least 25 studies involved Symbiodinium diversity. With the rapid accumulation of information, it is becoming increasingly difficult to assess newly acquired Symbiodinium data in light of previous studies and compare it to established patterns of host-symbiont specificity. Therefore, we developed the SymbioGBR database, which endeavors to compile all currently available sequence and host-association data of Symbiodinium reported for the GBR into a single relational database that is accessible as a web-based application.

Database description

SymbioGBR allows users to query Symbiodinium types (ITS1/ITS2) or sequences, and invertebrate host species to explore their reported associations. In addition it includes information of other regions such as 18S, cp23S and the single-copy marker psbAncr, allowing cross-referencing between single-copy and multi-copy markers. The database will be continuously updated and expanded. Finally, as the database is based on the collection details of individual specimens, such host-symbiont associations can be assessed quantitatively and viewed in an environmental (e.g., depth) and geographic context (e.g., latitude).

Symbiodinium phylogeny

The genus Symbiodinium consists of nine broad genetic clades, A-I (Pochon and Gates 2010), each of which contain various genetically and ecologically distinct types or sub-clades (van Oppen et al. 2001; Iglesias-Prieto et al. 2004; LaJeunesse et al. 2004a; LaJeunesse et al. 2004b; Warner et al. 2006; Pochon et al. 2007; Sampayo et al. 2007; Frade et al. 2008). While inter-clade differences are substantial genetic distances within Symbiodinium clades are small, sometimes only a few base pairs. Yet these small differences can relate to distinct functional characteristics that influence traits like photosynthetic efficiency, growth and thermal tolerance of the host (Iglesias-Prieto et al. 2004; Little et al. 2004; Berkelmans and van Oppen 2006). The identification of physiological differences in heat stress tolerance and bleaching susceptibility between Symbiodinium types at the subcladal level combined with rising SST’s underline the importance of understanding Symbiodinium diversity and its geographic range.

Temperature tolerance

Symbiodinium types D1, D1-4 (previously known as D1a: see nomenclature section), C1, C8/a and C78 and C15 have been found to be more resistant to heat stress (Rowan 2004; van Oppen et al. 2005; Berkelmans and van Oppen 2006; Jones et al. 2008; Sampayo et al. 2008; Fitt et al. 2009). Having these genetic varieties of Symbiodinium may be beneficial to the host in terms of surviving thermal stress and mass coral bleaching. However, this advantage may also incur physiological trade-offs such as reduced photosynthetic efficiency (Rowan 2004) and growth rates(Little et al. 2004), or an increased susceptibility to pathogenic infections(Littman et al. 2009). It is important to emphasize that clade level designations such as clade C versus D, which are often used to indicate bleaching susceptible versus more temperature tolerant Symbiodinium, should be interpreted with care since not all types within a clade respond equally to stress.

References

Berkelmans R, van Oppen MJH (2006) The role of zooxanthellae in the thermal tolerance of corals: a 'nugget of hope' for coral reefs in an era of climate change. P R Soc B 273:2305-2312

Fitt WK, Gates RD, Hoegh-Guldberg O, Bythell JC, Jatkar A, Grottoli AG, Gomez M, Fisher P, Lajuenesse TC, Pantos O, Iglesias-Prieto R, Franklin DJ, Rodrigues LJ, Torregiani JM, van Woesik R, Lesser MP (2009) Response of two species of Indo-Pacific corals, Porites cylindrica and Stylophora pistillata, to short-term thermal stress: The host does matter in determining the tolerance of corals to bleaching. J Exp Mar Biol Ecol 373:102-110

Frade PR, De Jongh F, Vermeulen F, Van Bleijswijk J, Bak RPM (2008) Variation in symbiont distribution between closely related coral species over large depth ranges. Molecular Ecology 17:691-703

Hoegh-Guldberg O (1999) Climate change, coral bleaching and the future of the world's coral reefs. Mar Freshwater Res 50:839-866

Hughes TP, Baird AH, Bellwood DR, Card M, Connolly SR, Folke C, Grosberg R, Hoegh-Guldberg O, Jackson JBC, Kleypas J, Lough JM, Marshall P, Nystrom M, Palumbi SR, Pandolfi JM, Rosen B, Roughgarden J (2003) Climate change, human impacts, and the resilience of coral reefs. Science 301:929-933

Iglesias-Prieto R, Beltran VH, LaJeunesse TC, Reyes-Bonilla H, Thome PE (2004) Different algal symbionts explain the vertical distribution of dominant reef corals in the eastern Pacific. Proceedings of the Royal Society of London Series B-Biological Sciences 271:1757-1763

Jones AM, Berkelmans R, van Oppen MJH, Mieog JC, Sinclair W (2008) A community change in the algal endosymbionts of a scleractinian coral following a natural bleaching event: field evidence of acclimatization. P R Soc B 275:1359-1365

LaJeunesse TC, Thornhill DJ, Cox EF, Stanton FG, Fitt WK, Schmidt GW (2004a) High diversity and host specificity observed among symbiotic dinoflagellates in reef coral communities from Hawaii. Coral Reefs 23:596-603

LaJeunesse TC, Bhagooli R, Hidaka M, DeVantier L, Done T, Schmidt GW, Fitt WK, Hoegh-Guldberg O (2004b) Closely related Symbiodinium spp. differ in relative dominance in coral reef host communities across environmental, latitudinal and biogeographic gradients. Mar Ecol-Prog Ser 284:147-161

Little AF, van Oppen MJH, Willis BL (2004) Flexibility in algal endosymbioses shapes growth in reef corals. Science 304:1492-1494

Littman RA, Willis BL, Bourne DG (2009) Bacterial communities of juvenile corals infected with different Symbiodinium (dinoflagellate) clades. Mar Ecol-Prog Ser 389:45-59

Muscatine L, Porter JW (1977) Reef Corals - Mutualistic Symbioses Adapted to Nutrient-Poor Environments. Bioscience 27:454-460

Pandolfi JM, Bradbury RH, Sala E, Hughes TP, Bjorndal KA, Cooke RG, McArdle D, McClenachan L, Newman MJH, Paredes G, Warner RR, Jackson JBC (2003) Global trajectories of the long-term decline of coral reef ecosystems. Science 301:955-958

Pochon X, Gates RD (2010) A new Symbiodinium clade (Dinophyceae) from soritid foraminifera in Hawai'i. Molecular Phylogenetics and Evolution 56:492-497

Pochon X, Garcia-Cuetos L, Baker AC, Castella E, Pawlowski J (2007) One-year survey of a single Micronesian reef reveals extraordinarily rich diversity of Symbiodinium types in soritid foraminifera. Coral Reefs 26:867-882 Rowan R (2004) Coral bleaching - Thermal adaptation in reef coral symbionts. Nature 430:742-742

Sampayo EM, Franceschinis L, Hoegh-Guldberg O, Dove S (2007) Niche partitioning of closely related symbiotic dinoflagellates. Mol Ecol 16:3721-3733

Sampayo EM, Ridgway T, Bongaerts P, Hoegh-Guldberg O (2008) Bleaching susceptibility and mortality of corals are determined by fine-scale differences in symbiont type. P Natl Acad Sci USA 105:10444-10449

van Oppen MJH, Mahiny AJ, Done TJ (2005) Geographic distribution of zooxanthella types in three coral species on the Great Barrier Reef sampled after the 2002 bleaching event. Coral Reefs 24:482-487

van Oppen MJH, Palstra FP, Piquet AMT, Miller DJ (2001) Patterns of coral-dinoflagellate associations in Acropora: significance of local availability and physiology of Symbiodinium strains and host-symbiont selectivity (vol 268, pg 1759, 2001). P R Soc B 268:2617-2617

Warner ME, LaJeunesse TC, Robison JD, Thur RM (2006) The ecological distribution and comparative photobiology of symbiotic dinoflagellates from reef corals in Belize: Potential implications for coral bleaching. Limnol Oceanogr 51:1887-1897

Links

Symbiodinium Wikipedia Page (http://en.wikipedia.org/wiki/Symbiodinium)
Symbiodinium Database of the Santos Lab (http://www.auburn.edu/~santosr/sd2_ged.htm)
GeoSymbio (https://sites.google.com/site/geosymbio)
Symbiodinium transcriptome sequences Medina Lab (http://medinalab.org/zoox/)
Blast Alignment search tool: (http://blast.ncbi.nlm.nih.gov/Blast.cgi)



Please reference as: Tonk L*, Bongaerts P*, Sampayo EM, Hoegh-Guldberg O (2013) SymbioGBR: a web-based database of
Symbiodinium associated with cnidarian hosts on the Great Barrier Reef.
BMC Ecology 13:7