Durusdinium: The ‘Superior’ Symbiont?

‘Shuffling’ and ‘Switching’ Symbionts

​Most corals form mutualistic relationships with multiple species of algal symbionts (or zooxanthellae) and are flexible in the species of zooxanthellae that they host (Baker et al., 2004; Muller-Parker et al., 2015; Toller et al., 2001​a; Toller et al., 2001b). Up until the last couple of decades, it was thought that corals could not ‘shuffle’ (enable a background zooxanthella strain to become dominant) or ‘switch’ (uptake new zooxanthellae from the environment via indirect transmission) between symbionts without first undergoing a bleaching event (thus expelling the current dominant zooxanthellae), but recent research has dispelled this theory -- demonstrating that corals can ‘shuffle’ or ‘switch’ between different symbionts at will and as necessary to accommodate their needs and better adapt to their environments -- no bleaching event required (Huang et al., 2020; LaJeunesse et al., 2009). Each symbiont has unique adaptations and tolerances to various environmental conditions; therefore, ‘shuffling’ or ‘switching’ out symbionts can be highly advantageous for a host (Muller-Parker et al., 2015). For instance, if the host coral becomes exposed to higher temperatures, the coral may elect to ‘shuffle’ or ‘switch’ its current dominant symbiont for a different symbiont that is more tolerant of thermal stress (LaJeunesse et al., 2009).

Durusdinium: The ‘Superior’ Symbiont?

​First described as Clade E (Toller et al., 2001a), and later reclassified as Clade D, finally in 2018 this clade of symbionts was designated as its own genus: Durusdinium of the family Symbiodiniaceae (LaJeunesse et al., 2018). Durusdinium has recently garnered lots of attention because of its ‘superior’ adaptations in the face of adversity. The name Durusdinium means “tough” and “whirling” (LaJeunesse et al., 2018), and, unlike other genera of Symbiodiniaceae commonly associated with corals (e.g., Breviolum and Cladocopium), members of Durusdinium are generalist extremophiles and are 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; Toller et al., 2001b). ​Because of its exceptional ability to tolerate a multitude of environmental stressors, Durusdinium is commonly found in symbioses with hosts that are settled in less than favorable environments, like nearshore coastal reefs, coastal lagoons, and tidal pools where conditions are harsher and bleaching events are more common (Mashini et al., 2015; Muller-Parker et al., 2015; Toller et al., 2001a; Toller et al., 2001b).

Microscopic image of Durusdinium trenchii ​
​© Aquaholic Aquaculture

Microscopic image of Durusdinium trenchii 
​© Aquaholic Aquaculture

Durusdinium and Increased Host Immunity

​Recent research has analyzed how Durusdinium’s remarkable adaptations influence the immunity of its host, examining host-zooxanthella associations and their effect on survivability during conditions of substantial stress (e.g., significant thermal variability, el Niño events, disease, major fluctuations in turbidity, light, nutrients, etc.). Recurringly, the literature illustrates a correlation between the presence of Durusdinium and the tenacity of the host, with hosts predominated by Durusdinium being better adapted to tolerate an array of environmental stressors and, therefore, superior at resisting bleaching (Baker et al., 2004, LaJeunesse et al., 2009, LaJeunesse et al., 2018; Manzello et al., 2018, Toller et al, 2001a, Wang et al., 2022).

​A noteworthy study by Baker et al. (2004) analyzed symbiont populations in coral hosts following a major bleaching event in the Indo-Pacific caused by the 1997-98 El Niño—Southern Oscillation (ENSO). Interestingly, they found that the coral colonies that survived the bleaching event were predominated by members of Durusdinium, lending credit to the theory that the tenacious adaptations of Durusdinium not only help the symbiont tolerate hostile conditions, but in turn bolster their host’s immunity to environmental stressors (Baker et al., 2004; LaJeunesse et al., 2009; LaJeunesse et al., 2018).
 
LaJeunesse et al. (2009) found similar results when they analyzed the symbiont populations of coral hosts that survived the 2005 mass bleaching event in the Caribbean; upon analysis, LaJeunesse et al. (2009) found that many of the coral colonies that survived the bleaching event harbored amplified populations of Durusdinium. Like the corals in Baker et al.’s study (2004), these corals’ susceptibility to environmental stressors appears to have been mitigated by the presence of Durusdinium, with corals disproportionately predominated by Durusdinium having an increased ability to withstand thermal stress and hence resist dissociation (i.e., bleaching) (LaJeunesse et al., 2009; LaJeunesse et al., 2018).
 
In the same vein, Manzello et al. (2018) came to analogous conclusions upon analysis of symbiont populations in coral colonies located in the Florida Keys following record-high ocean temperature spikes in sequential years (in 2014 and 2015). Manzello et al. (2018) discovered that during the 2014-15 bleaching event, corals in the Florida Keys had shifted away from hosting specialist symbionts (e.g., Breviolum), instead being in favor of hosting more resilient symbionts, specifically members of Durusdinium (Manzello et al., 2018). Manzello et al. (2018) found a significant relationship between Durusdinium presence and resistance to coral bleaching, with greater than 90% of the corals that survived the record bleaching event being primarily colonized by Durusdinium.
 
Likewise, Toller et al. (2001a) found Durusdinium to be the predominate symbiont in Montastraea (e.g., star corals) located in Panamanian regions known for their harsh environmental conditions. At Río Cartí, San Blas (a site that suffers from heavy freshwater runoff and increased sediments caused by its nearshore location in close proximity to the mouth of the major river: Río Cartí Grande), for the corals sampled, 35 of 43 corals were predominated by Durusdinium, and Durusdinium was the sole zooxanthella present for 18 of these corals (Toller et al., 2001a). Similarly, at Bocas del Toro (a large coastal lagoon known for exceptionally high rainfall and less than favorable water quality), Durusdinium was inordinately common in the sampled corals (Toller et al., 2001a). Based off their results, Toller et al. (2001a) concluded that Durusdinium’s stress-tolerant nature enables this symbiont to endure these environmental stressors, enabling its host coral to survive despite the hostile environmental conditions (Toller et al., 2001a).
 
In recent years, Huang et al. (2020) conducted a field experiment in which they transplanted Leptoria phrygia (e.g., smooth brain coral) between two sites with significant temperature differences and monitored the corals and their symbiont populations for 12 months. As theorized, in an effort to combat bleaching, the corals acclimatized to the thermal stress by ‘shuffling’ or ‘switching’ to hardier symbionts; specifically, the corals formed stable and strong associations with members of Durusdinium as a means of preventing bleaching (Huang et al., 2020).

Durusdinium and ‘Reviving’ Hosts

​In addition to bolstering host immunity and survival rates, for hosts that succumb to bleaching, Durusdinium has also been shown to help ‘revive’ these hosts by recolonizing them and helping them recover and re-brown (i.e., recoup normal densities of zooxanthellae and regain their color) (Muller-Parker et al., 2015; Toller et al., 2001​a; Toller et al., 2001b; Wang et al., 2022).  

​In 2001, Toller et al. conducted a series of field experiments in which they simulated bleaching events in Montastraea by either transplanting them to shallow water (high light exposure) or shading them (low light exposure), and then they monitored their symbiont composition over the next several months. As predicted, the simulated bleaching event encouraged corals to associate with new zooxanthellae (Toller et al, 2001b). Many of these corals that bleached in the experiment subsequently formed new relationships with members of Durusdinium and remained repopulated by Durusdinium even 9 months post-recovery (Toller et al, 2001b). Intriguingly, even when a bleached coral still had a small reservoir of Breviolum or Cladocopium within its tissues post-bleaching, these remaining symbionts were not sufficient to prevent the establishment of new symbiont associations with members of Durusdinium in the coral’s bleached tissues (Toller et al., 2001b). Toller et al. (2001b) concluded that despite conditions of stress, Durusdinium remains a robust and thriving opportunist, and, in fact, seems to excel under these hostile environmental conditions. As such, this symbiont is adept at repopulating bleached corals and helping them recover post-bleaching (Toller et al., 2001b).
 
More recently, Wang et al. (2022) conducted a laboratory experiment on the host coral Pocillopora damicornis (e.g., cauliflower coral) in which they manipulated applied heat and cold stress and analyzed the symbiont-host relationship during both the period of applied stress and recovery. Results of their experiment concluded that when temperature was manipulated, corals lost most of their original symbionts (e.g., Cladocopium) and became predominated by Durusdinium. Their study found that Durusdinium has enhanced photochemical efficiency while its host coral is under thermal stress; this in turn improves growth via stimulating algal photosynthesis and carbon translocation to the host coral, making Durusdinium the preferential symbiont during conditions of thermal stress and recovery (Wang et al., 2022).

Implications for Wild Reefs

​Research has demonstrated that Durusdinium is both adept at bolstering its host’s invulnerability to bleaching, as well as repopulating a host and aiding in its recovery post-bleaching (Baker et al., 2004; Huang et al., 2020, 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 evidence suggests that we can expect wild reefs to make adaptive shifts to Durusdinium (via ‘shuffling’ and/or ‘switching’) as both a means of recovery in the unfortunate event that the host has already succumbed to bleaching, as well as a preventative mechanism for resisting future bleaching events (Baker et al., 2004). Especially as oceans continue to get warmer, we may find that Durusdinium becomes increasingly prevalent among wild reefs; especially for hosts with greater sensitivity to thermal stress, it is likely that Durusdinium will play a pivotal role in their continued survival (La Jeunesse et al., 2009).

Implications for ‘REVIVE’
and Reef Aquariums

Whether in the wild or in captivity, hosts in symbioses primarily with members of Durusdinium are more likely to resist bleaching, survive through bleaching events, and recover from bleaching (Baker et al., 2004; Huang et al., 2020, LaJeunesse et al., 2009; LaJeunesse et al., 2018; Manzello et al., 2018, Toller et al., 2001a; Toller et al., 2001b; Wang et al., 2022). When searching for strains of symbionts for our REVIVE™: Live Zooxanthellae blend, Durusdinium’s aptitude at swiftly repopulating and aiding in the recovery of bleached corals made it an ideal candidate. Furthermore, the ability of this robust extremophile to withstand and thrive in a wide array of environmental stressors makes it the perfect addition to reef aquariums where it may act as a preventative against future bleaching episodes.

Microscopic image of Durusdinium trenchii 
​© Aquaholic Aquaculture

Microscopic image of Durusdinium trenchii 
​© Aquaholic Aquaculture

Microscopic image of Durusdinium trenchii 
​© Aquaholic Aquaculture

---

References

[1] Baker, A. C., Starger, C. J., McClanahan, T. R., & Glynn, P. W. (2004). Corals' adaptive response to climate change. Nature.

[2] Huang, Y., Carballo-Bolaños, R., Kuo, C., Keshavmurthy, S., & Chen, C. A. (2020). Leptoria phrygia in Southern Taiwan shuffles and switches symbionts to resist thermal-induced bleaching. Nature. 10(7808).
 
[3] 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).
 
[4] 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).
 
[5] 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).
 
[6] 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.
 
[7] 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.
 
[8] 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).
 
[9] 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).
 
[10] 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.