Authored by: Bailey Clear, Maggie Hawruk, Emily Ho-Nez, Stina McKenna
Coral reefs, the most productive and diverse of all ocean ecosystems, are entirely based upon on the successful symbiotic relationship between heterotrophic Anthozoans in the order Scleractinia and phototrophic dinoflagellates in the genus Symbiodinium. The coral polyps house the dinoflagellates in vacuoles within their gastrodermal issue, ensuring the algae of a permanent place in the photic zone as well as the nutrients and CO2 necessary for photosynthesis. The algae in turn provide the polyp with sugars and O2 (Venn et al, 2008). This assemblage of coral skeleton, tissue, and algal symbiont comprise the coral holobiont. Coral- algal symbiosis is a vital part of coral reef ecology. Without it, corals could not survive and reefs would shift to macroalgae-dominated environments.
Types of Symbiodinium
The algal genus that typically exhibits symbiosis with scleractinian coral hosts is Symbiodinium. Symbiodinium are unicellular, photosynthesizing dinoflagellates which have demonstrated a symbiosis with corals since the mid-Triassic. They exist in the vegetative state within membrane bound vacuoles in the coral gastrodermis (Stat et al 2006). Originally thought to be one species, Symbiodinium microadriaticum, zooxanthellae have actually been subdivided into eight clades (A-H) and 13 species. Certain environmental conditions, such as increased solar irradiance, prolonged darkness, presence of heavy metals, and elevated temperatures can act as triggers for bleaching (Douglas 2003).
Corals can acquire their algal symbionts in a number of ways. Broadcast spawning corals send out packets of egg and sperm (usually shortly after the full moon), which float to the surface of the water column where they rupture and fertilize. Brooding corals retain the zygotes after fertilization and later release planula larvae. Depending on the reproductive strategy of the coral, coral larvae acquire Symbiodinium in two different ways (Stat et al. 2006). Most frequently, brooding parental colonies of coral pass their zooxanthellae on to their offspring by way of maternal (vertical) transmission. The offspring of broadcast spawners, however, do not directly inherit symbionts. Rather, once the egg, zygote, or larva is in the water column, it can acquire Symbiodinium by way of horizontal transmission, in which they invaginate algae from the surrounding environment. However, brooding parental colonies do not always transfer zooxanthellae to their offspring and broadcast spawning colonies may acquire Symbiodinium through vertical transfer. Symbiodinium density typically ranges between one and ten million cells/cm2 coral tissue (Baker, 2003).
Coral bleaching is the process by which the symbiotic relationship of a coral host and its algal symbionts breaks down, thus causing a loss of color in the coral tissue and leaving behind white of the calcium carbonate skeleton, hence the term “bleaching.” Bleaching events can mean eventual death to the coral colony and decreased overall health of the reef. Over long periods of time or repeated bleaching events, cause a shift from coral dominated ecosystems to macroalgal dominated ones, thus disrupting the balance of organisms in the area.
Coral bleaching and algal symbiosis have been studied extensively in order to gain a better understanding of how to conserve the world’s rapidly declining coral reef ecosystems. The susceptibility of different coral and Symbiodinium species to bleaching, as well as the effects of depth and varying assemblages of Symbiodinium within coral colonies are aspects of the symbiotic relationship that must be quantified within a reef community so that conservation and restoration may be possible. With a predicted increase in the number of widespread, catastrophic bleaching events (Hoegh-Guldberg 1999), it is imperative to dissect patterns of the coral-algal symbiotic relationship.
Causes of Bleaching
Environmental stressors, such as increased seawater temperatures, irradiance, prolonged darkness, and the presence of heavy metals can act as triggers for the expulsion of zooxanthellae and therefore bleaching (Douglas 2003, Brown 1997). Under normal conditions, the photosynthetic apparatus in the Symbiodinium, consisting of photosystem II (PSII) and photosystem I (PSI) on the thylakoid membrane of the chloroplast, operates normally. It produces copious amounts of oxygen that diffuse into the host. All oxygen radicals (ROS) produced as a byproduct are neutralized by an enzymatic system (SOD and APX) to prevent mechanical damage to the cell (Weis 2008).
Temperature and Irradiance
When the coral holobiont is subjected to increased temperatures and/or irradiance, damage can be sustained in 3 locations within the chloroplast of the Symbiodinium:
1.) The D1 protein located in PSII, which is responsible for the splitting of water molecules. If the D1 protein is damaged, cellular repair systems are able to rectify the disorder; however, as temperatures continually increase, the accumulated problems begin to overwhelm the repair systems, resulting in a backup of excitation energy and dysfunction of PSII (Weis 2008).
2.) The dark reaction of photosynthesis, causing a decrease in carbon fixation, reduced consumption of ATP and NADPH and ultimately failure of PSII (Weis 2008).
3.) The thylakoid membrane, hindering electron transport in PSI and PSII, preventing the production of ATP and NADPH (Weis 2008). All previously discussed mechanisms can result in an overwhelming build up of ROS in the symbiont that can diffuse into the host tissue where damage ensues. The accumulation of damage eventually leads to the expulsion of the symbiont, resulting in bleaching (Weis 2008).
Corals exposed to prolonged darkness exhibit bleaching. The mechanisms causing this response are still uncertain; however, it is known that bleaching can result without direct damage to PSII of the Symbiodinium cells (Weis 2008, Douglas 2003). In general, because the symbiont is autotrophic, it cannot produce nutrients for itself or the coral host in the absence of sunlight. Accordingly, the presence of the symbiont is ineffective and will be eliminated by the host.
Elevated levels of heavy metals such as copper and cadmium cause bleaching in coral species such as Acropora formosa, Pocillopora damicornis, and Montiporra verrucosa. Bleaching due to the presence of iron, terpenoids, and cyanide has also been reported (Jones 1997). How metals cause coral bleaching remains unclear.
Mechanisms of Bleaching
There are several theories as to what happens when bleaching occurs. It is understood that the symbionts leave the coral host, but whether they actually exit the coral or if they are destroyed is unclear. There are five basic mechanisms that have been discussed as possibilities for the fate of coral symbionts (Weis 2008).
In Situ degradation
In situ degradation refers to the symbiont dying within the coral host cell. There are two possible causes for this death:
1.) The symbiont dies from the ROS defined above. This death, however is not an uncontrolled death but is Programmed Cell Death (PCD), a type of cell death that is carried out in a controlled manner so as to not damage the cell around it. As of yet, all cells observed with symbionts dying in situ have been experiencing PCD.
2.) The host cell actively destroys the symbiont. This may occur when a symbiont is damaged or diseased, which is evidence of an immune response by the host.
Exocytosis occurs when the host cell releases the symbiont entirely from the gastrovacular cavity. In this case, the host cell remains intact and the symbiont is also undamaged upon release back into the water column.
Apoptosis is another form of programmed cell death, however in this case the symbiont does not die within the cell. During apoptosis, the host cell shrinks down, DNA fragments and apoptotic bodies are formed on the outside of the coral cell bringing the symbiont to the outside with them. These bodies are then released, also releasing the symbiont. There are two theories on why apoptosis occurs:
1.) To mitigate tissue damage caused by ROS by simply deleting the damaged cells.
2.) The host cells sense when a symbiont has been damaged by stress or microbes and is eliminated by self destruction.
Host Cell Detachment
Detachment involves the release of the entire host cell with the symbiont still inside. This mechanism still requires some research and may actually occur after the host cell death and destabilization.
Host Cell Necrosis
Necrosis is marked by the swelling of the host cell, which will eventually burst and release all of its contents including the symbiont. This type of cell death is not a PCD and is not cellularly regulated. It is also quite different from apoptosis as it lacks apoptotic bodies and any genetic fragmentation. It is thought that necrosis occurs under severe stress when the coral can no longer exhibit enough control to execute PCD.
Fate of released symbionts
Although some symbionts appear to be released from corals in a whole and undamaged state, it seems that they do not last for long after release. Observations have shown that these symbionts usually begin to degrade quickly and are no longer viable as symbionts to new hosts shortly after release from the original host.
Consequences of Coral Bleaching
Beyond the death of the coral itself, coral bleaching has serious widespread consequences both ecologically and economically. The coral animal is a foundation species whose skeleton forms reefs, which are home to the highest density and diversity of fish and invertebrates in any ocean ecosystem. Coral reefs are the most productive marine ecosystems on Earth, but if corals bleach and die, these ecosystems experience a phase shift as macroalgae takes over, replacing the coral (Stat et al 2006). Once this happens, it is nearly impossible for the ecosystem to return to the way it was. Without the coral, the myriad of fish and invertebrate populations that depend on the reef for shelter and food will decline or disappear (Hoegh-Guldberg 1999). This, in turn, impacts organisms in higher trophic levels such as birds and mammals (Hoegh-Guldberg 1999). The negative socioeconomic ramifications are also widespread as millions of people worldwide depend on coral reef communities for food and livelihood. Coral reefs bring in well over $90 billion per year worldwide in tourism alone, while coral reef fisheries bring in over 6 million metric tons annually (Hoegh-Guldberg 1999).
Corals and Climate Change
Given that elevated temperatures have been shown to be one of the primary causes of coral bleaching, coral reef ecosystems are in very real danger given the current climate change. Global warming poses a very real, very immediate threat to the world’s coral reefs. Incidence of bleaching on reefs worldwide increases every year (Hoegh-Guldberg 1999). According to models projecting the rise in ocean temperatures, sea surface temperatures could surpass the upper limits of coral tolerances in the next 10 years (Hoegh-Guldberg 1999). Conservative models predict a 1-2°C increase in ocean temperatures by the end of this century. In the Caribbean, however, a temperature increase of just 0.1°C is accompanied by a 42% increase in incidence of bleaching (McWilliams et al 2005).
There is some hope that corals may be able to adapt to elevated ocean temperatures. Clade D symbionts are currently thought to be more bleach and stress resistant than other clades. Following a bleaching event, surviving corals are found to contain primarily clade D symbionts (Stat et al 2006). There is debate in the field as to whether corals have flexibility regarding their symbiont type and whether or not they are able to acquire more stress-tolerant clades during times of increased temperature stress (Stat et al 2006). This is known as the adaptive bleaching hypothesis (Buddemeier and Fautin 1993). The problem is that at the current rate of temperature increase, corals may not be able to adapt quickly enough (Hoegh-Guldberg 1999; McWilliams et al 2005).
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