CORAL ALGAL SYMBIOSIS THEORY
‘The mutualistic relationship between corals and their dinoflagellate endosymbionts is a key factor in the evolutionary success of hermatypic (reef-building) corals’ (c.f.Muller-Parker et al., 2015). If we want to understand how coral reefs may adapt to environmental stress, we need to investigate the mechanisms that control the cooperation between the coral and the so-called zooxanthellae. First, we should review the research, to get an idea of what causes the termination of the symbiosis and expulsion of the pigmented photosynthetic algae, leading to bleaching and if not reversed, to the death of corals and entire reefs. Thereafter we can propose measures to support the coral reef in maintaining its evolutionary success and suggest ways how to test the efficiency of such measures.
An individual coral polyp can be envisaged as a double-walled sac. The inner wall is a single-cell-thin layer called the endodermis or gastrodermis, enveloping the inside of the sac, the gastrovascular cavity, which functions as the stomach of the coral. The outer wall of the sac is another single-cell-thin layer called the epidermis or ectodermis. Where it is in contact with open seawater, it is called the oral or free epidermis. The other part that forms the bottom of the sac is called the calicoblastic epidermis, which secretes calcium carbonate, and covers a stony cup, the corallite, in which the polyp can retract. Along the edge of the sac, where the outer epidermis changes into the inner gastrodermis, six, or a multiple of six, tentacles surround the mouth of the polyp. Between the inner gastrodermal and outer epidermal cell layers, one finds a thin layer of connecting substance, called the mesoglea, composed of collagen, mucopolysaccharides, and some cells.
The cells of the gastrodermis contain the zooxanthellae. The alga is enclosed within a perivacuolar membrane of the coral cell and contains a nucleus with permanently condensed chromosomes, a chloroplast with banded photosynthetic membranes, a vacuole and inclusions of starch and lipid.
GROWTH AND REPRODUCTION
The coral can bud to reproduce itself asexually and thus forms a colony of regularly spaced identical polyp clones. The polyps are linked by a common gastrovascular system, enabling the sharing of food. The secretion of calcium carbonate layers by the calicoblastic epidermis at the underside of the thin veneer of living polyps produces ultimately the massive non-living calcareous structure, the corallum, with its characteristic form and typical distribution of corallites, housing the individual polyps.
Coral fragments may grow into fully developed corals again.
The coral can also reproduce sexually.
Zooxanthellae is the general name for the golden-brown dinoflagellate algal symbionts found in animals like corals, giant clams, sponges, jellyfish, flatworms, foraminifera and sea anemones. They are 8-12 µm in diameter and reside exclusively in the membrane bound vacuoles in the gastrodermal cells of the coral. Between 1 and 6 million zooxanthellae are found per cm2 of gastrodermal layer, varying spatially and temporarily, numbers increasing in months when light intensity decreases.
Zooxanthellae belong to the genus Symbiodinium that can genetically be divided into 9 phylogenetic clades (A – I) of which 6 live in Scleractinian corals. Zooxanthellae belonging to specific clades might be geographically restricted, occur only in shallow or deep corals, or are found only in one type of coral. A given coral may harbor various zooxanthellae genotypes, some at low frequencies, while possibly different types are acquired during different environmental conditions (Baker, 2003).
Zooxanthellae, like other dinoflagellates, have different modes to satisfy their energy need, by incorporating dissolved or particulate organic matter (heterotrophy) or by photosynthesis (photoautotrophy), using characteristic dinoflagellate pigments (diadinoxanthin, peridinin) and chlorophyll a and c.
Zooxanthellae may live as dinoflagellates outside their coral host in sediment and water column (Takabayashi et al., 2012), where they alternate between the motile dinomastigote stage with two flagella and the non-motile coccoid stage as is found in the corals.
The genetic diversity of zooxanthellae suggests sexual reproduction, but only asexual reproduction of haploid vegetative cells has been observed (Santos & Coffroth, 2003).
The corals acquire their zooxanthellae in various ways and during different stages of their life. The eggs of most corals do not contain zooxanthellae, but some do, and then it appears that free zooxanthellae in the gastrovascular cavity are ingested by gastrodermal follicle cells and expelled through temporarily gaps in the mesoglea, where the mature coral oocytes incorporate them through phagocytosis (Hirose et al., 2001). Zooxanthellae may also be acquired by larvae from their parent when brooded during the early stages of development before release.
Besides this so-called vertical transmission directly from the parent, there is also horizontal indirect transmission of zooxanthellae from the surrounding seawater or sediment, where their concentration tends to be low (Takabayashi et al, 2012). The zooxanthellae may be attracted by chemical substances released by juvenile corals without symbionts and move via chemotaxis towards their future hosts. They can also be acquired by ingestion of zooplankton prey and fecal material from corallivores, containing zooxanthellae. Corals may acquire different zooxanthellae during their life as follows from comparing juvenile and adult specimen (Baker, 2003).
After corals have expelled their zooxanthellae during bleaching, they may acquire a new zooxanthellae population of unknown source with a different genetic signature, during re-population (re-browning). These zooxanthellae may improve resistance to subsequent bleaching events but may be less advantageous during return to normal conditions (Buddemeier & Fautin, 1993; Baker, 2004).
Sleractinian corals typically thrive in clear, nutrient poor seawater where they do not experience much competition from algae. Phosphorus and nitrogen levels in seawater exceeding 1 and 6 µM, respectively, stimulate zooxanthellae growth to such an extent that symbiosis may be destabilized (Annis & Cook, 2002; Godinot et al., 2013). The coral polyps can feed on suspended particulate matter that they capture from seawater, incorporate dissolved inorganic and organic compounds from seawater through their epidermal cells, but mainly get food from the zooxanthellae. These produce the organic matter from carbon dioxide and water by photosynthetic carbon fixation, acquiring the necessary nutrients such as nitrogen from coral animal waste metabolites (Szmant et al., 1990; Muscatine & Kaplan, 1994) or even from nitrogen fixing symbiotic cyanobacteria (Lesser et al., 2004). Corals may acquire nitrogen via ammonium from seawater by maintaining a very low concentration in their tissue causing a diffusive flux, enabling the zooxanthellae to assimilate the ammonium and transfer assimilated nitrogen back to the coral (Kopp et al., 2013).
The dependence of corals on carbohydrates for energy from particulate or dissolved matter retrieved directly from seawater decreases, as the amount of carbohydrates provided by the photosynthesis of the zooxanthellae increases. If carbohydrate production by photosynthesis of zooxanthellae is larger than carbohydrate destruction during respiration of zooxanthellae and corals combined, then the corals are photoautotrophic. Oxygen measurements show that the ratio of production over respiration for shallow fully photoautotrophic corals is larger than one, but smaller than one for corals receiving less light at greater depth, needing an external food source for energy.
Photosynthesis by zooxanthellae enhances calcification, the precipitation of calcium carbonate by the calicoblastic epidermis at the underside of the coral polyp, but the mechanisms are not yet fully understood. Photosynthesis may provide energy and products to facilitate calcium transport or construction of the organic matrix upon which calcium carbonate precipitates (Gattuso et al., 1999). Photosynthesis lowers the carbon dioxide concentration and raises the pH, saturating the environment with respect to calcium carbonate solubility. The resulting precipitation of aragonite releases hydrogen ions that can be used by the coral to decrease pH again, raise the solubility of carbon dioxide from carbohydrate oxidation and offer this to the zooxanthellae for continuing photosynthesis. Finally, removal of inhibitors of calcium carbonate precipitation, like phosphate (Dunn et al., 2012) and nitrate (Marubini & Davies, 1996), might play a role in enhanced calcification.
The growth rate of corals with zooxanthellae is proportional to the light intensity up to a certain level, above which more light and strong UV light have negative effects. Coral polyps can regulate light reception by contracting and opening or by using ‘sunscreen’ molecules to protect against excessive UV radiation and green fluorescent proteins to block or reflect and thus regulate light for zooxanthellae (Salih et al., 2000), supposedly also protecting from reactive oxygen species (Roth & Deheyn, 2013).
The zooxanthellae adapt to low light intensity by increasing the amount of chlorophyll and other pigments, as well as the size of the chloroplasts and number of membranes within, while decreasing these photosynthesis instruments when light intensity is higher. Coral species may show variation of zooxanthellae community with light intensity and depth (Iglesias-Pietro et al., 2004).
Temperature influences metabolism and the carbohydrate production and respiration rates of zooxanthellae and corals, adapted to the local temperature regime, latitudinally and bathymetrically varying between long-term minimum of about 18 and maximum of about 35 °C (Coles & Jokiel, 1977). Coral bleaching is thought to occur after prolonged exposure to abnormally high temperatures, 1 – 3 °C above local long-term annual maximum, depending on presence of other stress factors, such as abnormal quantity of light and nutrients (Coles & Brown, 2003).