Nowadays, global warming is a hot item. Discussed in the media, politics and society; the debate rages on. The issue of human influence on this process still divides scientists and policymakers. This question set aside, global warming continues to threaten fragile ecosystems such as coral reefs¹. About 25% of them are estimated to have been completely decimated during the last decades. Coral reef bleaching has our full attention, but what exactly do we know about this process?

The irony of symbiosis

To understand coral bleaching, we must appreciate the fact that corals are colony-forming animals, living in symbiosis with unicellular algae of the genus Symbiodinium. These so-called zooxanthellae provide up to 95% of the coral’s daily required energy^2,3,4, by means of a process we call photosynthesis. This process is known to occur in many marine species outside the coral taxa, such as jellyfish, nudibranches, anemones and tridacnid clams.

This form of symbiosis is called mutualism, being beneficial for both parties involved. This unique partnership has allowed corals to synthesize vast reefs, despite being immersed in an oligotrophic (nutrient-poor) environment. The irony is that it’s this partnership which will threaten all of the reefs in the near future.

Photosynthesis; an overview

The complete, detailed biochemical process of photosynthesis is quite complex, and beyond the scope of this article. However, let's summarize this process to provide an overview. Figure 1 schematically depicts the main components of photosynthesis, which have been called photosystem I and II. They occur in opposite order, simply because they have been discovered that way.

The essence here is that a pigment which is stored inside the zooxanthellae, called chlorophyll, absorbs the energy from the sun’s rays.  This leads to a breakdown of water (H₂O), which we call photolysis. This process produces protons and oxygen. The reaction is this:

2H₂O => 4H⁺ + O₂

As light is required for this, we call this the light-dependent reaction.

The photolysis of water also generates a flow of electrons, which produces ATP (adenosine triphosphate) and NADPH (nicotinamide adenine dinucleotide phosphate). These substances are required for the second part of the process; the Calvin cycle. This cycle of reactions eventually leads to the conversion of CO₂ to glucose, so craved by corals. As these reactions do not require light, they occur at night as well, and thus we call them the light-independent reactions.

Figure 1, right: An overview of photosynthesis; a photo-chemical motor which produces oxygen and carbohydrates (Copyright Benjamin Cummings).

When we combine all these processes, the simplified reaction becomes this:

 6CO₂ + 6H₂O --> C₆H₁₂O₆ + 6O₂

The final result is the production of carbohydrates such as glucose, and oxygen.

Radicals; toxic scavengers

Despite the fact that both the coral and the zooxanthellae happily make use of the produced glucose and O₂ (corals and zooxanthellae oxidize glucose back to H₂O and CO₂ to make ATP again, which at last provides the required metabolic energy), there is a catch.

Oxygen is toxic. Quite toxic. It reacts with a vast array of organic molecules present in coral and algal cells, damaging cell organelles (small “organs” of all living cells) and DNA stored in the cell’s nucleus. It is clear that oxygen radicals are at the basis of ageing of many organisms, including humans.

These radicals probably are the main cause of coral bleaching as well.

Fortunately, living cells have means to deal with these dangerous pests. They make use of so-called anti-oxidants such as vitamin C, E and glutathione, chemically reacting with the oxygen radicals. So, if corals can protect themselves against this nasty side-effect of photosynthesis, why do they still bleach? This is because oxygen radicals sometimes flood the coral tissue in vast numbers, and there are two known ways by which this can be induced; high irradiance and temperature. Many hobbyists are not unfamiliar with these phenomena. The misuse of metal halides has bleached corals in many aquaria. Furthermore, during summer days, many tanks are actively cooled to prevent them from reaching the bleaching threshold of about 86-88°F (approx. 30-32°C).

The mechanism behind irradiance-induced bleaching is pretty straightforward. More light means more photosynthesis, and thus more radicals. As a reaction to the flooding of coral tissue by radicals, the corals expel their symbionts. If the irradiance is elevated slowly, the corals are allowed to adapt. Producing protective pigments like a natural sun-block, they can display attractive colouration. Next to this, zooxanthellae are thought to downregulate the production of photoactive pigments such as chlorophyll a. This decreases the brown colouration of the coenosteum and polyps, thereby enhancing the sparkling colours of the photopigments.

The mechanism behind temperature-induced bleaching is less well understood. Recent molecular research has provided crucial insight into this process.

Flexible membranes are key

Recently, it has been found that photosynthesis itself is responsible for temperature-induced bleaching. The electrons which flow through the thylakoid membranes of the zooxanthellae usually produce ATP, a process in which NADP is the final electron acceptor. This flow usually is closed, however, after membrane damage, the story changes. After this damage, many electrons are taken up by oxygen, thereby producing a high concentration of O₂-radicals⁵. These radicals probably flood the coral host tissue, inducing the expulsion of the zooxanthellae. This process is called energetic uncoupling of the photosystems⁵.

 Now we reach the essence of the story; this membrane damage can be caused by high temperatures, above 86-88°F, which can be clearly visualized by electronmicroscopic photographs (figure 2). Tridacna sp., Aiptasia sp. (the well-known glass anemone), Montipora samarensis and Stylophora pistillata symbionts show different responses to elevated temperatures. At 90°F(32°C), thylakoid membranes of Aiptasia sp. and Stylophora pistillata show clear signs of disruption, which is accompanied by bleaching.

Figure 2: Electronmicroscopic photos of chloroplasts of A: Tridacna sp., B: Aiptasia sp., C: Montipora samarensis and D: Stylophora pistillata. Disruption of Aiptasia and S. pistillata thylakoid membranes is visible at 90°F, whereas membranes of Tridacna and M. Samarensis retain structural integrity at higher temperatures (modified from Tchernov et al., 2004, Copyright 2004, National Academy of Sciences, U.S.A.).

Why do these symbionts display such different responses? There are various types of zooxanthellae, which are divided into clades A to H. Tchernov et al. discovered why some symbionts are so temperature-tolerant. They found that the lipid composition of the thylakoid membranes is a key determining factor for temperature tolerance (figure 3). 

Lipids are part of cellular membranes, making them more flexible. They also play a role in signaling; instructing cells to divide, die or increase their metabolism. Tchernov et al. discovered that the ratio of specific lipids, 9-cis-octadecatetranoate (18:1) and 6,9,12,15-cis-octadecatetranoate (18:4), determines thermal stability of the thylakoid membranes. A high ratio is predictive of the thermal tolerance of a given clade of zooxanthellae. In other words, a high 18-1/18-4 ratio means that zooxanthellae are very resistant to high temperatures. These data provide crucial insights into the mechanisms of coral bleaching, and allows scientists to predict how sensitive a coral species is to elevated water temperatures.

Figure 3: Correlation between 18-1/18-4 lipidratios and thermal tolerance. Thermally tolerant zooxanthellae (grey bars) display high 18-1/18-4 lipid ratios, in contrast to non-tolerant ones (white bars) (modified from Tchernov et al, 2004, Copyright 2004, National Academy of Sciences, U.S.A.).

The plasticity of symbiosis

Recently it was found that corals can shift to new dominant types of zooxanthellae during perilous times^6,7,8,9 (figure 4). Colonies of Acropora millepora were transplanted from the relatively cool North Keppel Island to the warmer Magnetic Island on the Great Barrier Reef. The colonies were monitored for a year, and their health was scored regularly. Small fragments of the colonies were cut off to determine the type of zooxanthella clade harboured by the corals, which is done by DNA analysis. The results were surprising.

Despite the fact that most colonies deteriorated following the transplantation shock, about 40% recovered. It became clear that in less than one year after this transplantation all surviving A. millepora colonies harboured clade D zooxanthellae. Clade D is known to be thermally tolerant, preventing corals from bleaching at even 91°F(33°C). The ability of corals to switch between dominant symbiont types may have been a key feature which has prevented the demise of the reefs worldwide. This shift in endosymbiont type is called adaptive bleaching¹⁰.

It must be noted however, that it is as yet unclear whether the corals really shift to a new dominant symbiont, or that they actually adopt new symbionts from the water column. If the former is true, the symbiont type was already present in the coral host tissue, albeit in small numbers.

Figure 4: Status of Acropora millepora colonies (n=22) and their symbionts, transplanted from North Keppel Island to Magnetic Island, Great Barrier Reef. Although most colonies significantly deteriorated, about 40% recovered. After analysis these colonies were found to have switched from the C2 to the temperature-tolerant D clade zooxanthellae (modified from Berkelmans & van Oppen, 2006).

The future of coral reefs

It is now clear that the world’s reefs have seen dramatic climate changes¹¹, such as ice-ages and subsequent global warming events. This was accompanied by the extinction of many Cnidarian (and thus coral) species, as indicated by fossilized specimens. Unfortunately, the rate at which climate change occurs today is much higher than before. Anthropogenic (human) CO₂ emissions continue to accelerate global warming. Individual (marine) organisms and ecosystems will face a tremendous challenge, having to adapt to changing seasons, ocean temperatures, pH values, and so on. The total demise of the reefs has never been closer, and at least a decrease in species diversity is to be expected.  

However, time and time again, we are presented with nature’s plasticity. The ability of corals to adapt to elevated sea surface temperatures by means of endosymbiont switching provides hope, but does not guarantee their survival. If the earth’s coral reefs and all of its other ecosystems are to have a future, it is crucial that CO₂ emissions are reduced. The next decades will present the reefs with temperatures above the bleaching threshold for prolonged periods of time, and high atmospheric CO₂ concentrations will decrease ocean pH. This last fact will be a second major stress factor. The earth’s reefs are ecosystems with tremendous ecological and economical importance, which hopefully will continue to exist for millennia.

Figure 5: Zooxanthellae type is key  to survival. On the center left, an Acropora millepora colony harbouring type C2 zooxanthellae is completely bleached.  On the right,several Acropora colonies are completely intact, harbouring type D zooxanthellae. (Miall Island, Great Barrier Reef, modified from Berkelmans & van Oppen, 2008).

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