Viruses: A third player in the coral algal symbiosis


Viruses are prevalent within a number of coral reef communities. Viruses and virus like particles are found in coral reef tissues, waters surrounding coral reefs, and within the tissues of endosymbiotic zooxanthellae. Viruses can infect any part of what is known as the coral holobiont. The coral holobiont includes the coral tissue, the zooxanthellae, and any prokaryotic symbionts. I think it is important to gain deeper insight into the potential of these obligate symbionts to act as mutualists. In the past, viruses have often been dismissed as solely parasitic and harmful to coral reef. However, in light of discoveries of a wide variety of viruses in both healthy corals and dying corals with no discernable differences in the size, morphology, or areas of infection between the viruses inhabiting the healthy corals and the viruses in the bleached corals, it is important to understand viruses can act as more than agents of infection (Marhaver 2008). Many researchers are beginning to look past previous biases about viruses and change their approach to viral research. Kristen L. Marhaver argues in her paper Viral communities associated with healthy and bleaching corals that the discovery of large numbers of viruses in healthy corals demands researchers to study coral viral interactions from a different perspective. She writes,“The amount of virus in coral represents a diversity of functions rather than a severity of infection”. In an age where threats to coral reef survival are increasing dramatically, the ability of viruses to act as mutualists to algal-coral symbiosis must be explored further. Corals are facing increased temperatures, decreased pH levels, and decreased carbonate ion concentrations, so it is crucial that interventions be made to help the corals tolerate such rapid and drastic changes. Could phage therapy be a potential way to help coral reefs survive some of these threats to their health and habitats?



Cyanophages and Vibriophages
Research on cyanophages and vibriophages has revealed that under certain conditions viruses have the potential to help symbiotic algae repair damaged PSII reactions centers, increase their nutrient uptake, survive heightened thermal stress, and fight off bacterial pathogens. Viruses that can perform such tasks could be highly advantageous to corals in periods of global warming and periods of heightened human disturbances.Cyanophages and Vibriophages, that are prevented from becoming solely cheaters that rob the coral algal symbiosis of the nutrients it produces, could be considered a third partner in the coral zooxanthellae symbiosis that helps keep the coral healthy and allows the symbiotic relationship to be maintained.



Cyanophages
external image Sullivan.jpg

http://www.mbari.org/seminars/2009/winter_09/Sullivan_Mar.htm


Cyanophages found in coral tissues have been found to translate and transcribe psbA genes within the coral tissues. This is an extremely important and beneficial function to be able to perform because psbA genes encode for the D1 and D2 proteins that help operate the PSII reaction center in the zooxanthellae. D1 and D2 proteins are two of the major light harvesting subunits of PSII, without them it would be impossible to obtain and energize the elections that drive the oxidation of water and create the protein gradient for ATP synthase. D1 and D2 proteins bind to Chlorophyll P680, pheophytin, and beta-carotene; these cofactors absorb photons of light that excite the electrons and act as primary electron acceptors, without them the zooxanthellae could not effectively harvest light from the sun and fix carbon during the light independent reactions of the Calvin Cycle. When PSII reaction centers in the zooxanthellae are destroyed due to photo-inhibition or thermal stress, viruses can potentially act as agents of repair (Marhaver 2008). Photosynthetic carbon fixation can be restored before the coral extrudes the zooxanthellae and bleaches, allowing the symbiotic relationship to remain intact. However in examining the role of viruses as mutual symbionts, it is important to remember their potential to act parasitic and abandon their role as mutualists. Cyanophages for example, only repair PSII reaction centers to ensure they can continue to steal energy produced from the coral algal symbiosis (van Oppen 2009).



Virus facilitated nitrogen uptake
Cyanophages not only play a role in the maintenance of the zooxanthellae’s photosynthetic activity, they also play a role in nutrient cycling. When cyanophages infect corals they introduce cyanobacteria into the coral tissue facilitating greater nitrogen uptake by the zooxanthellae. In a coral algal symbiosis, the coral receives fixed carbon from the symbiont, and the Zooxanthellae gets nitrogen and phosphate by recycling coral reef wastes. Coral reef tissues are typically nutrient poor because they are intolerant of liquid nutrient enrichment, meaning they are unable to absorb a significant amount of Nitrogen that has been released into the water column so a greater number of cyanobacteria would help increase the concentration of Nitrogen.(http://www.fisherycrisis.com/coral3.html) Higher rates of cyanophage facilitated cyanobacterial infection of the coral reef could increase the zooxanthellae's ability to aquire Nitrogen from the coral holobiont.

However cyanophages have the potential to cause harm if the cyanobacteria provide an excessive amount of Nitrogen to the zooxanthellae. With excess nutrients the zooxanthellae population grows uncontrolled and the balance of the nitrogen-carbon fluxes between the coral host and zooxanthellae is disrupted, resulting in a reduction of calcification and weakening of the coral calcareous skeleton.” (Olivieri, 1997)Coral will only benefit from increased Nitrogen uptake up to a certain threshold, after that point the fixed carbon going to the coral reef compared to the nitrogen going to the symbiont begins to affect the coral’s skeletal integrity. When there is a reduction of calcification and the coral skeleton either becomes less dense and the coral is more vulnerable to erosion, or the coral reduces the amount of energy allocated to reproduction in order to maintain its integrity and there is a reduction in fecundity.(Hoegh-Guldberg 2007)
If the skeleton is weakened the coral becomes too brittle to withstand storms and wave energy. “If rates of erosion outstrip calcification, then the structural complexity of coral reefs will diminish, reducing habitat quality and diversity.” (Hoegh-Guldberg 2007)When corals are unable to withstand erosion it puts the coastal habitats they protect at greater risk as well. Salt marshes, mangroves, and beaches all become more vulnerable to damage from waves and storms.



Vibriophages
Vibriophages have also been documented to have beneficial effects on the corals they infect. Viruses exert a significant amount of control on marine microbial communities. Vibriophages are responsible for 50% of bacterial cell death in the ocean (Marhaver 2008). By releasing toxins viruses in the coral can destroy bacterial pathogens before they kill the coral. It has been confirmed that two of the most prevalent coral diseases, red-band disease and black-band disease are caused by different species of bacteria. If different bacteria prove to be the cause of other prevalent coral diseases like white- band disease, white pox, yellow botched disease, and dark spots disease, viruses could help deter the partial coral tissue mortality caused by coral diseases. It would be extremely advantageous for corals to possess viruses that can fight off bacteria that destroy live tissue, because the loss of live coral tissues can hamper the reproductive abilities of the coral. Although most coral diseases only cause partial mortality, when coral tissue is lost to disease all the reproductive coral polyps in the tissue are lost as well.(Green and Bruckner, 2000). Coral fecundity must remain high to make sure coral growth and recruitment rates remain strong, especially at a time when environmental disturbances are becoming more prevalent. Corals communities need to maintain high recruitments rates in order to prevent being replaced by microalgal communities following warming events, acidification, and damage from erosion which are all becoming more prevalent because of the rapid increases in the amount of atmospheric CO2.


Red-band Disease (A. Bruckner)
Red-band Disease (A. Bruckner)


http://coris.noaa.gov/about/diseases/ (Click on this picture to learn more about coral diseases)

Red band disease is caused by a variety of strains of filamentous cyanobacteria. The bacteria infects the surface of the coral and forms maroon colored bands that progressively kills the outer coral tissue. Red band disease has been documented attacking massive and plating stony corals throughout the Caribbean. The exposed skeleton, left after the coral is infected provides a perfect place for macroalgae to colonize and dominate areas that were previously dominated by coral reef communities.(Green and Bruckner, 2000).

Black-band Disease (A. Bruckner)
Black-band Disease (A. Bruckner)



http://coris.noaa.gov/about/diseases/ (Click on this picture to learn more about coral diseases)


Black band disease is caused by a combination of cyanobacteria, sulfur reducing bacteria, and sulfur oxidizing bacteria. The bacteria create crescent shaped black bands on the coral. The black bands cause the living coral tissue to deteriorate. Like with red band disease, black band disease results in the accumulation of bare coral skeleton vulnerable to algae colonization. Massive reef building corals are at the greatest risk of contracting black band disease. The disease is widespread and has affected a variety of corals in different oceans across the world. “A total of 16 species have been observed with BBD in the western Atlantic, and 26 species in the Red Sea and Indo-Pacific (Green and Bruckner, 2000).”


If a coral holobiont contains viruses that kill bacteria, it may be better equipped to fight off disease causing bacteria that could kill their tissue and reduce their reproduction rates and ability to colonize.However, just like cyanophages have the potential to harm the coral so do the vibriophages.Vibriophages, in exerting control over microbial communities, may not differentiate between bacteria that are good and bacteria that are harmful. So along with killing pathogenic bacteria, vibriophages could kill bacteria that help corals fix nitrogen, obtain nutrients, and fill space (Marhaver 2008).



Involvement of viruses in the coral bleaching process.
Viruses are believed to accelerate the necrosis, apoptosis, and lysis that zoothanthellae undergo during bleaching events. Viruses have been found in the cytoplasm of zooxanthellae under stress. These viruses are thought to be responsible for the subsequent lysis of the zooxanthellae following the light induced stress events. It is yet to be determined whether or not this is mutualistic or harmful for coral reefs in this age of rising temperatures. “The expulsion of Symbiodinium cells may help corals adapt to changing environmental conditions by allowing symbiont populations to redistribute themselves.” (Lohr 2007) Viruses may help drive the expulsion of symbionts that are less tolerant to heightened temperatures allowing coral reefs to change their criteria for selection and only host clades of symbionts that can photosynthesize under higher temperatures. The capability of corals to switch symbionts as a way to adapt to changing abiotic conditions is still under investigation. If corals do in fact have the ability change their symbionts when environmental conditions change, virus may help speed up the process by inducing zooxanthellae lysing. However if the majority of corals are unable to host multiple clades of symbionts and shuffle between them, or if it is confirmed that most corals cannot adopt new symbionts from the surrounding environment, viruses will only act to accelerate the degeneration of the symbionts the coral needs to survive.



Coral Bleaching
Coral Bleaching


http://climatelab.org/Climate_Change (To learn more about the effects of climate change on corals click on the picture)

So in conclusion there is still a great deal of research and investigation that needs to be done before the role of viruses in coral algal symbiosis can be determined. The conditions under which viruses act as mutualists and aid in the maintenance of a coral algal symbiosis and the conditions under which viruses are more inclined to act solely parasitic must be explored further. Viruses can be classified as at least partial mutualists and therefore symbiotic partners in the coral zooxanthellae symbiosis because they can help repair photosystem II reaction center, help prevent the coral from contracting bacterial diseases, increase nitrogen uptake in the holobiont, and potentially help corals switch their symbionts under increased temperatures.




References
1. Davy, Sk, Sg Burchett, Al Dale, P. Davies, Je Davy, C. Muncke, O. Hoegh-Guldberg, and Wh Wilson. "Viruses: Agents of Coral Disease?" Diseases of Aquatic Organisms 69 (2006): 101-10. Print.

2. Hoegh-Guldberg, O., P. J. Mumby, A. J. Hooten, R. S. Steneck, P. Greenfield, E. Gomez, C. D. Harvell, P. F. Sale, A. J. Edwards, K. Caldeira, N. Knowlton, C. M. Eakin, R. Iglesias-Prieto, N. Muthiga, R. H. Bradbury, A. Dubi, and M. E. Hatziolos. "Coral Reefs Under Rapid Climate Change and Ocean Acidification." Science 318.5857 (2007): 1737-742. Print.

3. Lohr, J., C. B. Munn, and W. H. Wilson. "Characterization of a Latent Virus-Like Infection of Symbiotic Zooxanthellae." Applied and Environmental Microbiology 73.9 (2007): 2976-981. Print


4. Marhaver, Kristen L., Robert A. Edwards, and Forest Rohwer. "Viral Communities Associated with Healthy and Bleaching Corals." Environmental Microbiology 10.9 (2008): 2277-286. Print.


5. "NOAA's Coral Reef Information System (CoRIS) - Major Reef-building Coral Diseases." NOAA Coral Reef Information System (CoRIS) Home Page. 2 Dec. 2010. Web. 10 Apr. 2011. http://coris.noaa.gov/about/diseases/


6. Van Oppen, Madeleine J.H., Jo-Ann Leong, and Ruth D. Gates. "Coral-virus Interactions: A Double-edged Sword?" SYMBIOSIS 47 (2009): 1-8. Print.


7. Wilson, W. H., A. L. Dale, J. E. Davy, and S. K. Davy. "An Enemy Within? Observations of Virus-like Particles in Reef Corals." Coral Reefs 24.1 (2005): 145-48. Print.

8."Coral Reef Ecosystem Dynamics, Nutrient Cycling, Effects of Fishing." The Starving Ocean. Web. 27 Apr. 2011. <http://www.fisherycrisis.com/coral3.html>.