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1 Introduction

Photosymbiotic associations between unicellular algae, cyanobacteria, and invertebrates such as corals, sea anemones, bivalves, sponges, foraminiferans, flatworms, and hydra, are found in seawater and freshwater (Muscatine, 1971; review by Trench, 1992; Stat et al., 2006; Venn et al., 2008; Table 1). The most common and prominent association is the exclusive marine symbiosis of coelenterates with zooxanthellae that are located in vacuoles (symbiosomes), usually within the host’s endoderm cells, while in other hosts, such as ascidians and tridacnids, the photosymbionts are extracellular (Trench, 1987; Yellowlees et al., 2008).

Table 1. The invertebrates, their photosymbionts, their habitat, the type of photosynthetic export products from the photosymbionts to the host, and the energy support by the photosymbiont to the host.
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The symbiotic algae are named according to their pigment color: (1) Zooxanthellae for yellow-brown algae (Brandt, 1882, 1883). They are taxonomic, belonging to the Chromophyta, which includes diatoms (= Bacillariophyta) and dinoflagellata. From the latter, they mainly belong to the genus Symbiodinium sp. Phylogenetic classification of the genus Symbiodinium contains several lineages: clade A in cnidarian and molluscan hosts; clade B in cnidarian; clade C in cnidarian, molluscan, foraminifera, and others; clade D in coral sponge foraminifera; clade E found in one sea anemone species; clade F in foraminifera and, rarely, in coral; clade G in foraminifera, sponges, octocorals, and scleractinian corals; and clade H, found only in foraminifera (Rowan and Powers, 1991; Carlos et al., 1999; Pochon and Pawlowski, 2006 (also as review)). (2) The green ones, known as zoochlorellae, belong to the chlorophytes found in sea anemones, sponges, nudibranchs, and hydra. (3) The blue-green algae, which are the cyanobacteria named zoocyanellae, are found in sponges, foraminifera, and nudibranchs (Table 1). Prochloron sp. is an obligate symbiont in didemnid ascidians (Munchhoff et al., 2007), and is also found in association with nudibranchs.

The genetic diversity within photosymbioses, specifically in Symbiodinium, is a part of the adaptation of the symbionts to the environment and seems likely to correlate to the diverse range of physiological properties in the host–symbiont assemblages (Stat et al., 2008). The host can acquire its symbionts either from its parents, such as in the case of asexual fragmentation reproduction, or from the surrounding environment. When the symbionts are transferred directly from the host to offspring, the process is known as vertical, or closed-system, transmission. However, in most species, including coral colonies that are broadcast spawners, scyphozoans, and tridacnid bivalves, each generation must acquire new zooxanthellae from the surrounding seawater or, in rare cases, from a secondary host, in a process called open-system or horizontal transmission (see Karako et al., 2002; Barneah et al., 2007a, b; Huang et al., 2008).

The morphology of the animal host, specifically in the case of cnidaria and porifera, contributes to the distribution of symbionts in their tissues. The large surface area to volume and the only two layers of tissue (ectoderm and endoderm) allow the symbionts to capture maximum light (Venn et al., 2008).

In the tissue of many anthozoans, the algal cells are arranged in a mono­layer. As a result, the reef corals average millions of dinoflagellates per square centimeter of coral-colony surface (Drew, 1972). The average cell-specific density (CSD) ranges from 1.11 to 2.1. While in some species, e.g., Stylophora pistillata, the variation in distribution of number of algae per host cell is minimal, in others, such as Condylactis gigantea, significant variation can be found (Muscatine et al., 1998). The dinoflagellates occupy most of the interior of the macerated host cells, leaving the host cytoplasm and cell membrane as a thin outer layer. As such, the symbiotic zooxanthellae in cnidarians live within an osmotically different environment from that of free-living dinoflagellates (Goiran, et al., 1997; review by Mayfield and Gates, 2007). This spatial arrangement may support diffusion and transport of CO2, bicarbonate ions, and nutrients from the environment to the algae (Muscatine et al., 1998). Marubini et al. 2008.

The symbiosis is based on fluxes of carbon and nutrients between the host, the algae, and the environment (Muscatine, 1990). This mutualistic relationship allows corals and coral-reef communities to succeed in spite of the low concentrations of nitrogen and phosphorus typical of the “blue deserts” – the oligotrophic waters surrounding the reefs (Muscatine and Porter, 1977). Both the cnidarian host and the algae are capable of ammonium assimilation from the surrounding environment, having the enzymes glutamine synthetase (GS) and glutamate dehydrogenase (Rahav et al., 1989). A variety of ammonium transporters have recently been found in Symbiodinium with similarity to bacterial transporters (Leggat et al., 2007, see below). Both partners benefit from nitrogen (N) recycling between animals and microorganisms. The host benefits because the microbial symbionts act as a sink for potentially toxic nitrogenous waste compounds, and the symbionts benefit from access to the N source for growth (Douglas, 2008).

By their photosynthesis, the symbionts provide to the host a major fraction of the metabolic requirements of the animal host (Muscatine, 1990). This dependence on photosynthesis sets depth limits to zooxanthellate corals, restricting most species to the photic depth, with reef growth and species diversity declining with light. The photic (also called euphotic) depth is usually set at 1% of subsurface light. In addition, the algae create oxidized surroundings for the coral animal. It should be noticed that harboring photosynthesizing microalgae inside the tissue, which produce upon illumination great amounts of oxygen, is an advantage while the free-radical reactive oxygen species (ROS) that are also produced can be harmful to the host (Mayfield and Gates, 2007; Merle et al., 2007.

The photosynthetic algae pass up to 95% of their photosynthetic products to their animal host (Muscatine et al., 1984) primarily as glycerol, but also in the form of peptides, amino acids, glucose sugars, complex carbohydrates, and lipids (e.g., Trench, 1979; Swanson and Hoegh-Guldberg, 1998; review by Venn et al., 2008, Table 1). Host release factor (HRF) probably controls the translocation of the photosynthetic product from the zooxanthellae to the host (Trench, 1971; Gates et al., 1995, 1999; Withers et al., 1998; Cook and Davy, 2001; Grant et al., 2006a, b; Biel et al., 2007).

In return, the algae are exposed to higher levels of nutrients from the digestion of zooplankton by the whole coral, and to higher CO2 from respiration, when compared with sea concentration. By growing in the coral tissue, indicating loss of the ability to move, the algae lose their flagellate (although it exists in culture), change their lifecycle (Freudenthal, 1962), and mainly reduce their growth rate. Existence in the tissue protects the algae from grazing by other organisms.

Several major metabolic processes exist in the holobiont: respiration by both the host and the symbionts, photosynthesis (by the zooxanthellae), and calcification in all the organisms that build skeletons, such as corals, mollusca, and foraminifera.

$$ {\text{6CO}}_{2}+12{\text{H}}_{2}\text{O}\iff {\text{C}}_{6}{\text{H}}_{12}{0}_{6}+\text{6C}{0}_{2}+6{\text{H}}_{2}0(\text{photosynthesis}\iff \text{respiration})$$
$$ {\text{H}}_{2}\text{O}+{\text{CO}}_{2}\iff {\text{H}}_{2}{\text{CO}}_{3}\iff {\text{H}}^{+}+{\text{HCO}}_{3}{}^{-}\iff 2{\text{H}}^{+}+{\text{CO}}_{3}{}^{2-}\left(\text{bicarbonate system}\right)$$
$$ {\text{Ca}}^{+}+{\text{2HCO}}_{3}{}^{-}{\iff }^{-}{\text{CaO}}_{3}+{\text{CO}}_{2}+{\text{H}}_{2}\text{O}$$
$$ {\text{Ca}}^{2+}+{\text{2HCO}}_{3}{}^{-}\iff \text{Ca}{\left({\text{HCO}}_{3}\right)}_{2}\iff {\text{CaCO}}_{3}+{\text{H}}_{2}{\text{CO}}_{3}$$
$$ {\text{Ca}}^{+2}+{\text{H}}_{2}\text{O}+{\text{CO}}_{2}\iff {\text{CaCO}}_{3}+2{\text{H}}^{+}\left(\text{calcification}\right)$$

These three processes involve diffusion and transport of molecules from the seawater inside the holobiont in the exoderm, the endoderm, the zooxanthellae, and vice versa (Gattuso, 1999). The availability of CO2 to the bicarbonate system has a major influence on the process and, in some cases, will limit them due to competition between the host and the symbionts.

In the sea anemone, Anemonia viridis, and the coral, Stylopora pistillata, the dissolved inorganic carbon (DIC) is absorbed from the seawater by the ectodermal cell layer and then transferred to the endodermal cell layer, where the zooxanthellae are located. In the latter, HCO −3 is dehydrated to CO2 and used for symbiont photosynthesis and OH−, which is secreted within the coelenteric cavity. This process leads to a functional polarization of the oral layers, with the endodermal face being alkaline. The major supply of DIC then results from a transcellular transport of HCO −3 , whereas a fraction (20%) is supplied by passive diffusion (Benazet-Tambutte et al., 1996; Furla et al., 1998, 2000a, b, Fig. 1). The HCO −3 absorption by ectodermal cells is carried out by H+ secretion and by H+-ATPase, and the formation of carbonic acid in the surrounding seawater, which is quickly dehydrated into CO2 by a membrane-bound carbonic anhydrase (CA) (Furla et al., 2000a, b). Symbiodinium sp. have high CA activity and specific transporters for the delivery of bicarbonate ions to the host cells, keeping the partial pressure of CO2 in the immediate surroundings of the symbiont cells high enough to support photosynthetic carbon fixation (Allemand et al., 1998). Corals growing in seawater at a reduced pH of 7.2 calcified at half the rate of corals at pH 8.0, indicating that coral growth is strongly dependent on the concentration of CO 2−3 ions in seawater (Marubini and Atkinson, 1999; Marubini et al., 2008).

Figure 1.
figure 1

Model of inorganic carbon uptake by cnidarians. (After Furla et al., 2000a, b).

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Environmental changes that alter the metabolite exchanges between host and symbionts and – by that – the osmolyte pool levels might cause an osmotic stress response that will be followed by ROS formation, protein damage, photo­inhibition, and even bleaching (Mayfield and Gates, 2007).

During the last decades, global climate change has caused an increase in sea temperature, pCO2, and acidification that led to zooxanthellae being expelled and/or losing their pigments, resulting in the bleaching of holobiont coloration and the death of entire reefs. These relationships between the marine microalgae/cyanobacteria and invertebrate symbiosis depend on the host genotype, the symbiont genotype, and environmental conditions. As these relationships develop during evolution time, stressful conditions such as high temperature, high light intensity, UV, and eutrophication break them down (see Stambler and Dubinsky, 2004; Grottoli et al., 2006; Stat et al., 2006; Carpenter et al., 2008; Day et al., 2008; Stambler, 2010).

2 Scleractinia – Hard Corals

Photosynthetically fixed carbon is translocated from zooxanthellae to the host. Under high-light conditions, translocation may amount to some 95% of the photosynthetic production of the zooxanthellae (Falkowski et al., 1984; Muscatine et al., 1984). The contribution of zooxanthellae to animal respiration (CZAR) is up to 100% of daily metabolic requirements, and in some cases, they provide more than the total metabolic needs of the host animal (Muscatine et al., 1981, 1984; Falkowski et al., 1984; Grottoli et al., 2006). In Pocillopora damicornis and Fungia scutaria, the CZAR is in the order of 63–69% (Muscatine et al., 1981). The energy input from photosynthesis in the coral Pocillopora eydouxi is about twice the amount that the animal needs for respiration (Davies, 1984). In the coral Porites porites, the animal used only 33% of the energy translocated from the zooxanthellae (Edmunds and Davies, 1986). In Stylophora pistillata, a product of algal photosynthesis could provide between 143% and 58% of the total carbon and energy requirements of the high- and low-irradiance-adapted colonies, respectively (Falkowski et al., 1984; Muscatine et al., 1984, Fig. 2).

Figure 2.
figure 2

Energy flow in the symbiotic association between zooxanthellae and coral. (a) High and low light for the coral Stylophora pistillata in μg C cm−2 day−1. (After Muscatine et al., 1984; Falkowski et al., 1984.) (b) A model of carbon fluxes under eutrophication conditions. (c) A model of carbon fluxes under stress conditions which cause bleaching, such as high temperature and high UV.

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This energy is used by the host for metabolism including respiration, production, planula, larvae, and mucus release. Energy in the form of translocated carbon from the symbiont often covers the necessity for the daily needs of some scleractinians (Davies, 1991), and excess carbon can be stored as lipid reserves in concentrations of 10–40% of total biomass (Edmunds and Davies, 1986; Stimson, 1987; Harland et al., 1992, 1993). Up to 50% of the photosynthetically fixed carbon exported to the host is released from the host as mucus (Crossland et al., 1980; Davies, 1984; Crossland, 1987; Wild et al., 2004).

A compound described as HRF, which stimulates the release of photosynthate from symbiotic algae, has been found in the host tissue of several symbiotic cnidarians (e.g., Muscatine, 1967; Grant et al., 2006a). The HRF controls the amount of carbon translocated from the zooxanthellae to the host. In the case of the scleractinian coral Plesiastrea versipora (Lamarck), the HRF, which has a low molecular weight, stimulates the release of glycerol from its symbiotic dinoflagellate, which can then be utilized by the animal host for its own needs. This diversion of glycerol from the algae results in a partial decrease in the algal synthesis of triacylglycerol (TG) and starch (Grant et al., 2006a).

Under oligotrophic conditions, zooxanthellae are nitrogen- and phosphorus-limited, and can multiply. Owing to the nitrogen limitation, much of the carbon fixed in photosynthesis can translocate to the host. The result is that the growth rate of the zooxanthellae is extremely slow, with doubling times as long as 70–100 days (growth rate, μ = 0.007–0.001 day−1) in the common Red Sea coral Stylophora pistillala (Falkowski et al., 1984) when compared with the much higher growth rate of zooxanthellae cultured from the coral Acropora sp. (0.33–0.48 day−1) (Taguchi and Kinzie, 2001). The mechanism for regulating algal–cnidarian symbiosis is by the expulsion of dividing algal cells and not by digestion (Baghdasarian and Muscatine, 2000). Once supplied with additional nutrients, either as ­inorganic compounds, such as ammonium and phosphate or via zooplankton consumption by the host animal (e.g., Dubinsky et al., 1990; Falkowski et al., 1993; Dubinsky and Jokiel, 1994), the zooxanthellae retain most of their photosynthetic products. This photosynthetic carbon is now utilized for the synthesis of zooxanthella biomass, accelerating their growth rates and increasing their densities up to fivefold (Dubinsky et al., 1990).

This growth results in the following adverse effects on the overall carbon and energy flux within the association: the zooxanthellae significantly reduces their photosynthetic rates per algal cell due to carbon limitation in the super-dense, multilayered algal population (Dubinsky et al., 1990). However, based on the area, photosynthesis increases when multiplied due to the increase in algal numbers. In addition to the above-described measured effect, the following two effects were also inferred: the rapidly multiplying algae retain a much higher fraction of photosynthate, rather than translocating it to the animal (Muscatine et al., 1989; Falkowski et al., 1993), and nutrient enrichment causes an imbalance in coral growth between organic tissue and carbonate skeleton (Tanaka et al., 2007). Because of these process changes under eutrophication, symbiosis breaks down (Stambler et al., 1991; Dubinsky and Stambler, 1996).

Size growth in the solitary coral Fungia concinna is not limited strictly by energy availability, but by not recognizing physiological and/or ecological constraints (Elahi and Edmunds, 2007). It might be controlled by the availability of nutrients and other components necessary for animal growth. Corals, which are heterotrophic organisms, use multiple heterotrophic inputs as food sources, including zooplankton (e.g., Sebens et al., 1996; Ferrier-Pages et al., 2003; Palardy et al., 2006), particulate organic matter (Anthony and Fabricius, 2000), and bacteria (Ferrier-Pages et al., 2003). These provide the association nutrients, such as nitrogen and phosphorus (e.g., Muscatine and Porter, 1977; Szmant-Froelich and Pilson, 1980). A high percentage of 66% of coral skeletons is based on heterotrophic inputs (Grottoli and Wellington, 1999). The ratio between the heterotrophic and auto­trophic energy contribution, which depends on the coral and zooxanthella species, changes under different conditions, such as food availability and light intensity (Porter, 1976; Falkowski and Dubinsky, 1981; Falkowski et al., 1984; Anthony and Fabricius, 2000; Palardy et al., 2005; Grottoli et al., 2006). Montipora capitata, a tropical coral, was more resilient to bleaching by increasing its food ingestion. The colonies of Montipora capitata that had been bleached started to recover, increasing the feeding rates (fivefold higher in bleached versus non-bleached), and by that, the percentage of the contribution of heterotrophically acquired carbon to daily animal respiration (CHAR) supplied more than 100% of their daily metabolic energy requirements and allowed them to survive. This was not the case with Porites compressa and Porites lobata (Grottoli et al., 2006). Metabolic changes in lipids, such as triacylglycerol, phospholipid, monoacylglycerol, diacylglycerol, and free fatty acid show that during bleaching and recovery, Montipora capitata corals switch between heterotrophy and photoautotrophy, while Porites compressa corals rely mostly on photoautotrophy (Rodrigues et al., 2008).

Coral energy balance is a function of (1) heterotrophy and phototrophy, which are influenced by bleaching status and light regime, and (2) energy losses that are also functions of temperature and light (e.g., Anthony and Connolly, 2004; Grottoli et al., 2006). The interaction between temperature, light, and feeding controls growth, zooxanthella density, and asexual reproduction (Rodolfo-Metalpa et al., 2008a, b). Chlorophyll concentrations increased under low light and temperature, probably in order to maintain a sufficient level of autotrophy (Rodolfo-Metalpa et al., 2008a). In the case of the temperate coral Cladocora caespitosa, feeding was especially important for growth at low temperatures (Rodolfo-Metalpa et al., 2008b). The translocation rate of the zooxanthellae was higher in winter than in summer (Peirano et al., 2005). It seems that at high temperature, some of the heterotrophic energy supply is used by the host for other metabolic processes, such as sexual and asexual reproduction (Rodolfo-Metalpa et al., 2008b). The glycerol translocated to the host is usually rapidly respired, although the host maintains temporally dynamic pools of both glycerol and amino acids within its tissues. In response to temperature increase, these pools decrease due to shifts in the symbiotic metabolism (Gates and Edmunds, 1999). While irradiance had no effect on the temperate coral Cladocora caespitosa, high temperature and food supply increased coral growth rates. The effect of feeding was greater for corals maintained at low temperatures, suggesting that heterotrophy is important during the cold season. At low temperatures, samples that were fed exhibited higher zooxanthella density and chlorophyll concentration. Sexual reproduction level was higher during high temperatures and zooplankton availability (Rodolfo-Metalpa et al., 2008). There is some evidence that zooxanthellae under low temperature become heterotrophic (Dimond and Carrington, 2008).

In the field, in response to temperature stress, some symbiont communities change in reef-building corals, suggesting a population-wide acclimatization to increased water temperatures, creating new, more thermally tolerant holobionts (Jones et al., 2008; Maynard et al., 2008). This change supports the adaptive bleaching hypothesis (Buddemeier et al., 2004). As Jones et al. (2008) pointed out, the advantage of more temperature tolerance might result in certain disadvantages, such as slower growth rate of the holobiont (Little et al., 2004). This could be due to a reduction in the photosynthetic rates of the new symbionts (Rowan, 2004) using more energy for zooxanthella growth and less energy reserves (Hoogenboom et al., 2006; Loram et al., 2007).

Total lipid concentrations decline in some species when zooxanthella and/or chlorophyll a concentrations are low (Rodrigues and Grottoli, 2007; Rodrigues et al., 2008). Part of the coral recovery after bleaching is due to increasing lipid concentration, mainly from heterotrophic feeding. Storage lipids depend on the coral species. While Montipora capitata corals switch between heterotrophy and photoautotrophy, Porites compressa corals rely on photoautotrophy (Rodrigues et al., 2008).

Reduced photosynthesis as a result of bleaching leads to reduced energy reserves for maintenance and growth and/or tissue biomass (see Fitt et al., 2000; Grottoli et al., 2004; Anthony and Connolly, 2007). During the course of a bleaching event, energy reserves may thus fall to the point at which resources for maintenance and growth are compromised, leading to increased risk of mortality (Anthony and Connolly, 2007).

In the coral Acropora pulchra, during algal photosynthesis, more than 70% of organic N synthesized from NO −3 by zooxanthellae is produced and immediately translocated to the host coral. The organic matter translocated to the host is similar, at least in C:N ratios, to that found in the algal cells. However, NO −3 -derived N accumulates more in the zooxanthellae when compared with the alga:coral N ratio, probably followed by a reduction in the organic matter translocated to the host with increasing NO −3 availability for the symbionts. Once incorporated, organic compounds of higher C:N ratios are consumed more rapidly than those of lower C:N ratios in both the host coral and zooxanthellae. The coral–zooxanthella symbiotic system could be highly conservative for N (Tanaka et al., 2006).

Nutrients, including nitrogen and phosphate, are a limiting factor in the oligotrophic seas (e.g., Jackson and Yellowlees, 1990). The taking up, retention, and recycling of dissolved inorganic and organic nutrients by the symbioses have contributed to the success of coral reefs in nutrient-depleted tropical seas (Muscatine and Porter, 1977).

Many aspects of the nitrogen cycle were studied (Fig. 3, Yellowlees et al., 2008). The efficiency with which nitrogen from predation was fully incorporated into the zooxanthella Oculina arbuscula was nearly 100%, when compared with only 46% for corals containing few zooxanthellae. In A. pallida, symbiont density had no effect, and N assimilation was 23–29% (Piniak et al., 2003). The host and alga are capable of ammonium assimilation from the surrounding seawater, with both possessing the enzymes GS and glutamate dehydrogenase (Rahav et al., 1989). Some ammonium transporters were found in Symbiodinium (Leggat et al., 2007). The host ammonium assimilation is high and requires a constant supply of carbon skeletons, presumably from photosynthesis, for ammonium assimilation. Some nitrogen is assimilated by Symbiodinium and transported back to the host, in particular, the essential amino acids (Wang and Douglas, 1999). Symbiodinium transporters for nitrate and nitrite have been found (Leggat et al., 2007). Symbiodinium are probably capable of utilizing nitrate as an N source (Fagoonee et al., 1999). The intact cnidarian symbiosis removes nitrate from the water column (Crossland and Barnes, 1977). Nitrate is converted to nitrite and, furthermore, to ammonium, through the action of the enzyme nitrate reductase (Leggat et al., 2007). This nitrogen can be quickly translocated to the host (Tanaka et al., 2006), presumably as amino acids (Yellowlees et al., 2008). Nitrate and ammonium can serve as nitrogen sources. The cnidarian symbioses are capable of reasonably high rates of nitrate uptake from the very low concentration in the water, although they prefer ammonium (Grover et al., 2003). Zooxanthellae may use the nitrogen for their growth and release some of it back to the host in the form of amino acids (Markell and Trench, 1993). Nitrogen fixation also occurs inside the coral by intracellular cyanobacterial symbionts that fix N2 (Lesser et al., 2004, 2007). In temperate areas where the nutrients are a less limiting factor when compared with tropical areas, the zooxanthellae probably store nitrogen for use when nutrients and food are less available (Davy et al., 2006).

Figure 3.
figure 3

Model of the nitrogen cycle in the cnidarian association based on Crossland and Barnes (1977), Rahav et al. (1989), Markell and Trench (1993), Falkowski et al. (1993), Wang and Douglas (1999), Fagoonee et al. (1999), Roberts et al. (2001), Grover et al. (2003), Lesser et al. (2004), Tanaka et al. (2006), Davy et al. (2006), Leggat et al. (2007), Lesser et al. (2007), and Yellowlees et al. (2008).

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Few studies have been carried out on phosphate, and its cycle in the holobiont is not known. Only by symbiont cnidarians, not aposymbiont cnidarians, phosphate uptake occurs. The uptake rates by intact symbiosis are higher in the light than in the dark (D’Elia, 1977).

Photosynthesis and calcification in the reef-building corals Pontes compressa, Porites porites, and Acropora sp. are affected by bicarbonate concentrations. Porites porites increases the calcification rate in response to the addition of NaHCO3, reaching saturation at 6 mM while the photosynthesis saturation is 4 mM HCO3. Acropora sp. calcification and photosynthesis are higher than those of Porites porites: photosynthesis saturates at 4 mM, while calcification continues to increase even above 8 mM HCO3 (Marubini and Atkinson, 1999; Herfort et al., 2008).

Owing to global changes, it is predicted that in the next century, pCO2 will increase by 15% (0.3 mM) the oceanic HCO −3 concentration (based on Herfort et al., 2008) and this could stimulate photosynthesis and calcification of hermatypic corals. Unfortunately, the increase in pCO2 will cause acidification of the seawater, which will cause a decrease in coral growth calcification, decalcification of the coral, coral death, and might irreversibly change the entire reef (Fine and Tchernov, 2007; Hoegh-Guldberg et al., 2007; Jokiel et al., 2008; Veron, 2008a, b). Coral symbiosis has developed for over 250 million years, and is usually exposed to slow changes in the environment. Bleaching events caused by increasing sea temperature already cause and will probably contribute to the death of the entire reefs (Hoegh-Guldberg, 1999, 2005; Hoegh-Guldberg et al., 2007; Veron 2008a, b). We hope that the host, the symbionts, and the holobiont will be able to adapt. Some corals are able to recover and survive bleaching. In some cases, such as in the case of Pocillopora verrucosa, bleaching sensitivity might not be associated with clade specificity (Richier et al., 2008).

Some bleached and recovering corals increase their feeding and, in that way, obtain heterotrophic carbon for daily animal respiration (CHAR) (Grottoli et al., 2006). Coral species with a heterotrophically high energy source and lipid storage capabilities during bleaching and recovery will be able to survive bleaching events over the long term, and might become the dominant coral species on reefs (Grottoli et al., 2006; Anthony and Connolly, 2007; Rodrigues et al., 2008). The ability of the host to change its energy source, together with changing the symbionts associated with the host, might prevent the total global extinction of reefs.

3 Hexacorallia – Sea Anemones

Temperate and tropical sea anemones harbor zooxanthellae and/or zoochlorellae in their tissues. In most cases, this symbiosis is similar to that in hard and soft corals (e.g., see section on coral for the N cycle, Fig. 3), but there is a unique symbiosis of the sea anemone Phyllactis (= Oulactis) flosculifera, which has developed specialized behavioral, structural, and chemical adaptation. Phyllactis (= Oulactis) flosculifera cultivates the zooxanthellae in specialized areas of the body, and then breaks them down and uses them as a source of nutrition (Steele and Goreau, 1977).

The photosynthetic products of the algae transfer to the host. For example, in the temperate sea anemone Anemonia viridis, glucose and succinate/fumarate are the important photosynthetic compounds transferred from the Symbiodinium cells to the host tissues (Whitehead and Douglas, 2003, Table 1).

The temperate sea anemones Anthopleura elegantissima and Anthopleura xanthogrammica from the northern latitudes can harvest both the zooxanthella Symbiodinium muscatinei (dinoflagellate) (LaJeunesse and Trench, 2000) and the zoochlorella Coccomyxa (chlorophyte) (Verde and McCloskey, 2002, 2007; Lewis and Muller-Parker, 2004). In the intertidal sea anemone Anthopleura elegantissima, both the zooxanthellae and zoochlorellae translocate 30% of photosynthetically fixed carbon in freshly collected anemones, although the zoochlorellae fixed and translocated less carbon than the zooxanthellae (Engebretson and Muller-Parker, 1999).

Only 50% of the photosynthetically assimilated carbon is utilized by the zooxanthellae of the sea anemone Anemonia sulcata from the Israeli Mediterranean coast, while the rest is translocated to the animal tissue. The percentage of carbon translocated to the anemone tissue is independent of light intensity and, therefore, does not depend on the total amount of fixed carbon. This translocation of the photosynthetic products from the algae to the animal tissue may provide up to 116% of the animals’ respiratory needs under natural conditions (Fig. 4). Under starvation conditions, the percent of translocation increases up to 70%. The energy contribution of zooxanthellae to the anemone allows its survival and maintenance under starvation conditions, but for growth, the anemone also needs essential nutrients, such as nitrogen and phosphate, which have to be obtained through predation (Stambler and Dubinsky, 1987). The CZAR in Anemonia viridis from different locations along the coast of Ireland is 140.6–142.9% at 1.5 m on sunny days, but less than 100% under low light. Zooxanthellae of the sea anemones Cereus pedunculatus, Anthopleura ballii, and Anemonia viridis at 1.5 m on sunny days, requires 1.80–5.89% of the carbon fixed in photosynthesis for respiration and growth, and translocates 94.11–98.20% to the host. At 9 m on cloudy days, zooxanthellae use 38–88% of the fixed photosynthesis carbon, leaving 12–62% for translocation.

Figure 4.
figure 4

Energy flow in the symbiotic association between zooxanthellae and Anemonia sulcata in cal g−1 wet weight day−1 (After Stambler and Dubinsky, 1987).

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The CZAR is measured at 72.6% in Anthopleura ballii and 72.1% in Cereus pedunculatus, at 1.5 m on sunny days, and decreases to just 2.1% and 0.7%, respectively, at 9 m on cloudy days (Davy et al., 1996). In the anemone Anthopleura elegantissima from the low-intertidal, the CZAR is 34–42%, decreasing to 17% in high-intertidal anemones (Zamer and Shick, 1987). In the dark, starved anemones lose weight at a higher rate than in the light (Smith, 1939; Taylor, 1969; Tytler and Davies, 1986). In the anemone Anthopleura elegantissima, it is 34–56% when starved, but only 8–9% in fed animals (Fitt et al., 1982). Generally, a translocation rate of more than 90% in both tropical and temperate zooxanthellate anemones is found under well-light conditions (Muller-Parker and Davy, 2001).

Irradiance regulates both the photophysiology and metabolism of this alga–sea anemone association. Regardless of light intensity, algal densities remain stable for Anthopleura elegantissima, harboring zooxanthellae or zoochlorellae. Net photosynthesis, the potential carbon contribution of the algae to animal respiration (CZAR), and the mitotic indices of both the symbionts, vary with light intensity, with no change in the chlorophyll per algal cell. Zooxanthella photosynthetic rates are consistently higher than those of zoochlorellae (McCloskey et al., 1996; Verde and McCloskey, 2002). No matter which algae are associated with the sea anemone, net photosynthesis is always higher during spring and summer. In addition, the zooxanthella net photosynthesis is higher than that of the zoochlorellae. Anemone respiration is also higher during the spring and summer. As a result, the CZAR does not show a clear relationship with season; however, the CZAR for zooxanthella anemone is greater than for zoochlorella anemone (Verde and McCloskey, 2007). Lower zooxanthella growth rates, higher photosynthetic rates, and CZAR give an advantage to the Anthopleura elegantissima association with zooxanthellae at high-light intensity when compared with zoochlorellae, and can be seen by the higher densities of zooxanthellate anemone in the shallow water, while Anthopleura elegantissima with zoochlorellae is found primarily under low-light conditions in shaded habitats (McCloskey et al., 1996; Verde and McCloskey, 2002). In the sea anemone Aiptasia pulchella, zooxanthellae become heterotrophic under low-light conditions (Steen, 1987). Changes in CZAR, with environmental variation, were found in other symbioses, such as in the zoanthid Isozoanthus sulcatus. In the zoanthid, the translocation rate exceeded 95% under high- and low-light conditions, while the CZAR was 181.5% at 1.5 m on sunny days, but less than 100% at 9 m on cloudy days (Davy et al., 1996).

Owing to temperature increase, bleaching events were observed in the Mediterranean Sea anemones Anemonia sulcata var. smaragdina and Anemonia rustica. Both the species lost 90% of their zooxanthellae (Leutenegger et al., 2007). Aposymbiont anemones depend on heterotrophic feeding.

Condylactis gigantean, which are similar genetic individuals, harbor either Symbiodinium clades A or B, which are functionally different. At 25°C, there is no significant difference in the clade photosynthesis. Temperature changes the carbon fixation rates per algal cell. For symbioses harboring clade A, the total fixation rates are higher at 30°C when compared with 25°C, while the opposite is found for symbioses harboring clade B. Clade A incorporation of algal photosynthetic carbon into animal lipids and amino acid pools is significantly higher when compared with clade B. This difference may be due to the difference in the amount of compounds translocated to the animal tissues or a difference in the metabolic processing of the mobile compounds by the animals (Loram et al., 2007).

4 Octocorallia – Soft Corals

Few studies have been carried out on soft corals and their symbionts. The assumption is that the relationship between the host and the zooxanthellae is very similar to that of the hard coral and sea anemone, even though predation may play a major role in this soft-coral symbiosis. The soft coral, octocoral Sinularia ­lochmodes, controls the cell division of Symbiodinium by arresting the algae in the cell-dividing, non-motile stage via chemical signaling (Koike et al., 2004). This signal causes the translocation of the photosynthesis product from the algae to the host. In the soft coral Capnella gaboensis, photosynthetically fixed carbon by zooxanthellae is incorporated into the coral tissues as glycerol, glucose, succinate, citrate, fumarate, glycolic acid, malate, aspartate, glycine, serine, and alanine. In this case, about 10% of the total fixation was translocation (Farrant et al., 1987).

5 Mollusca, Bivalvia, Clams

The giant clam family Tridacnidae contains large numbers of Symbiodinium sp. The zooxanthellae, which live in the clam’s siphonal mantle (hypertrophied siphonal tissues), are important for its nutrition. The existence of zooxanthellae in the mantle tissue demands its exposure to light and causes the clams to be permanently sessile. This increases the risk of attracting predators and causes the development of a very unique system of light sensors and a mechanism for retraction of the mantle tissue, allowing closing of the shell valves against the predators. In another photosymbiotic bivalve, Corculum cardissa, which harvests Symbiodinium corculorum zooxanthellae, the algae are also located in a zooxanthellal tubular system that is associated with the hemocoel and is similar to that seen in the tridacnine clams (Farmer et al., 2001).

Tridacnidae zooxanthellae live within a branched, tubular structure that has no direct connection to the hemolymph. The fact that there is no connection between the hemolymph and the stomach via the tubes associated with the zooxanthellae prevents digestive enzymes from entering the hemolymphatic system. The entire branched tubular system associated with the zooxanthellae communicates with the stomach via a single opening, which is visible in clams that are only a few weeks old. This would appear to explain the initial entry of zooxanthellae into the mantle. While it is unlikely that intracellular digestion occurs in the zooxanthellal tube, the epithelial cells of the zooxanthellal tube might have been misidentified as hemocytes engulfing algal cells (Norton et al., 1992).

On the one hand, healthy zooxanthellae observed in the Tridacna stomach (Fitt et al., 1986) pass through the intestine and rectum and are released in the feces; thus, these algae, by a still unknown mechanism, are able to resist host digestion (Trench et al., 1981). This route is also available for the mass expulsion of zooxanthellae from clams exposed to elevated environmental temperatures (Estacion and Braley, 1988). On the other hand, there are some indications that some zooxanthellae in the clams Tridacna derasa are digested by host clams (Maruyama and Heslinga, 1997). Although in the zooxanthellal tubes, zooxanthellae usually have intact ultrastructures, suggesting that they are photosynthetically active, the stomach always contains degraded zooxanthellae that were probably discharged from the zooxanthellal tube. In four Tridacna species, symbiotic algae are capable of providing 2–4 times more carbon than required by the host for respiration. The CZAR increases with clam size in all species, except in Hippopush hippopus, which has a comparatively high and more constant CZAR of 340%. The lowest CZAR value is 186% in the smallest Tridacna squamosa (Klumpp and Griffith, 1994). In the Red Sea, similar CZARs of 186% in Tridacna maxima and 151% in Tridacna squamosa were found (Jantzen et al., 2008).

Degraded zooxanthellae are always found in the stomach of veligers and Tridacna crocea, Tridacna derassa, and Tridacna squamosa. They seem to be digested with other stomach contents, such as diatoms. Giant clams probably digest zooxanthellae directly, and ingest the secreted photosynthates from them. Thus, the giant clams probably utilize the zooxanthellae not only as photosymbionts, but also, directly, as foods. There may be a selection mechanism to discharge unhealthy zooxanthellae from the mantle into the stomach. In addition to zooxanthellae, digested diatoms and other unidentified digested materials in the stomach suggest that filter-feeding also contributes to giant-clam nutrition. However, symbiosis with zooxanthellae supplies the host with a photosynthetic product, while the digestion of zooxanthellae may also supply nutrients for the giant clams (Hirose et al., 2006).

The advantage of having zooxanthellae in the tissue of a giant clam such as Tridacna crocea, is the receiving of glucose release by the zooxanthellae (Ishikura et al., 1999). The glucose release is controlled by the host release factor (Muscatine, 1967). The zooxanthellae supply as much as 100% of the daily respiratory carbon requirements of the clam Tridacna gigas (Fisher et al., 1985) and more than 50% of the carbon resources required by other host clams (Trench et al., 1981; Klumpp and Lucas, 1994).

Zooxanthellae in giant clams use CO2 as the primary source of their ­carbonate while the symbionts in corals use bicarbonate (Leggat et al., 2000; but see Furla et al., 2000a, b, Fig. 1).

6 Mollusca, Nudibranchs, Sea Slugs

Photosymbiosis is found in the gastropod. Live photosynthetic dinoflagellates are also found in the hepatopancreas and gonads of the Red Sea snail Strombus tricornis. They are found within the upper whorls of the snail’s shell, where light penetration is 5–15% of the incident light reaching the shell (Berner et al., 1986). However, in this taxonomy group, most of the symbiosis is found in nudibranchia, where the light is not blocked by a shell.

Nudibranchia are associated with zooxanthella Symbiodinium, zoochlorellae, and Prochloron. The nudibranchs take up the algae through their prey, mostly by feeding on soft corals, and, in some cases, also on hard corals. Stable symbiosis and long-term retention of zooxanthellae are found with Aeolidoidea and Dendronotoidea (Burghardt et al., 2008). In the aeolid nudibranch Aeolidia papillosa, zooxanthellae and zoochlorellae obtained by the ingestion of Anthopleura elegantissima remain photosynthetically active within the cerata, and it is likely that they derive some benefit from these algae. The zooxanthellae and zoochlorellae may survive the nudibranch cerata as heterotrophic (Mcfarland and Muller-Parker, 1993). In other nudibranchs, even after 200 days of starvation, the number of zooxanthellae is high and dividing zooxanthellae detected (Burghardt et al., 2008). Burghardt et al. (2008) suggest that the uptake of zooxanthellae via the prey and the ensuing enhancement of cryptic appearance might represent the beginning of the evolution of nudibranch–zooxanthellae symbioses. A branched digestive gland has a larger surface area for the exchange of metabolites and gases, with large exposure to the light due to body and transparent ceras wall. This allows high photosynthetic utilization (Burghardt et al., 2008). The additional products produced by the symbionts allow the slugs to survive with food shortages lasting from weeks to months (see in Burghardt et al., 2008).

Sacoglossan mollusks maintain photosynthetic plastidin/chloroplast in their cells, a phenomenon known as kleptoplasty (Waugh and Clark, 1986). The sacoglossans incorporate the chloroplasts into their digestive cells through phagocytotic feeding (e.g., Rumpho et al., 2000; Evertsen et al., 2007; Casalduero and Muniain, 2008). Functional chloroplasts photosynthesize inside the mollusk cells and produce oxygen, carbohydrates, lipids, and proteins (Greene and Muscatine, 1972; Trench et al., 1972). The ability to retain functional chloroplasts (RFC) varies among seven sacoglossans from the Indo-Pacific and Mediterranean Seas: Plakobranchus ocellatus – 11 months, Elysia timida – 3 months, and Elysia sp., Elysia tomentosa, Thuridilla carlsoni, Thuridilla lineolata, and Elysiella pusill – 15 days. The variations are based on the quantum yield of charge separation in photosystem II in dark acclimated cells measured by pulse amplitude modulated (PAM) fluorometry (Evertsen et al., 2007). The survival rates of Elysia timida, after being kept in the dark for 28 days, are up to 30% lower when compared with the rates of those that are kept in the light, and exhibit size decrease, even though chlorophyll concentration values are similar in both the cases. The kleptoplasts provide the mollusks energy at the primary metabolism level to compensate for a shortage in food (Casalduero and Muniain, 2008). The exposed area of the parapodia of Elysia timida responds to light, ensuring optimum irradiance to be reached by the chloroplasts. Under low light, E. timida unfolds the parapodia (Rahat and Monselise, 1979; Monselise and Rahat, 1980). Sacoglossans may regulate light intensity, and by that, control the photosynthesis rate and prevent pigment degradation (Casalduero and Muniain, 2008).

7 Foraminifera

Endosymbiotic algae and chloroplasts are found in 3 orders and 11 families of foraminifera host:

  1. 1.

    Alveolinidae, Amphisteginidae, Calcarinidae, and Numulitidae host diatoms.

  2. 2.

    Soritacea host a variety of different algal types: (a) Peneroplidae host symbiont rhodophytes; (b) Archaiasinae host chlorophytes; and (c) Soritinae host dinoflagellates, cyanobacteria, and haptophytes (review by Lee (2006). In a single foraminiferal sub-family, Soritinae, a great diversity of Symbiodinium genotypes (clades C, D, F, G, and H) is found. Based on the molecular clock method of Symbiodinium rDNA sequences, the Symbiodinium genus originated in early Eocene, and the majority of extant lineages diversified since mid-Miocene, about 15 million years ago (mya) (Pochon and Pawlowski, 2006).

  3. 3.

    Globigerinidae host dinoflagellates and chrysophytes.

  4. 4.

    Candeinidae, Pulleniatinidae, Hastigerinidae, and Globorotaliidae host chrysophytes (review by Lee, 2006).

Peneroplis planatus does not grow if starved. It grows slowly in the dark when fed. It acquires most of its carbon and energy for growth from food and cannot grow solely on carbon compounds that are fixed, transformed, and released by its endosymbiotic algae (Faber and Lee, 1991).

While corals contain about l–2% organic matter (Erez, 1978), they are much higher in foraminifera. In Amphistegina lobifera, the host, the symbiont host organic matter, and the skeleton contain approximately 7%, 20%, and 73% of the total carbon, respectively; in Amphisorus hemprichii, the numbers are 5%, 16%, and 79%, respectively. As corals contain the least amount of organic carbon per unit of inorganic (calcareous) carbon when compared with foraminifera, they need to take up fewer nutrients in the form of nitrogen or phosphorous compounds from their surroundings. Translocation from symbionts to Amphistegina lobifera, a perforate species, and to the imperforate species Amphisorus hemprichii host is sufficient to account for the increase in their biomass (Kuile and Erez, 1991).

8 Sponges

Tropical and temperate sponges (Porifera), which are filter-feeding organisms, harbor photosynthetic symbionts. Hosts include Demospongiae and Calcarea (Diaz, 1996). The symbionts include cyanobacteria, rhodophytes, diatoms, dinoflagellates, chlorophytes, and cryptomonads. Polar sponges are associated with diatoms. Freshwater sponges often contain endosymbiotic microalgae, primarily zoochlorellae (see Wilkinson, 1992; Taylor et al., 2007; Usher, 2008), while the marine sponges harbor diverse and abundant microbial communities (Lee et al., 2001; Taylor et al., 2007).

Based on sequencing analysis, it seems that the symbionts are transferred by a combination of vertical and horizontal symbiont transmissions. Some symbionts are passed down from an ancestral sponge, while others are obtained contemporaneously from seawater (Taylor et al., 2007).

The density of cyanobacteria in the sponge is proportional to the number of sponge cells; the symbiont population is probably controlled by the sponge. The control mechanisms might include sponges that consume excess symbionts, eject symbionts under stress, and use the photosynthetic product by the host sponge (Wilkinson, 1992). The photosymbionts are restricted to sponge surface cell layers where they are exposed to maximum light (Beer and Ilan, 1998). Phototrophic cyanosponges have characteristics of flattened morphology with a large surface area on which photosynthesis can take place (Wilkinson, 1983), while cyanosponges have a smaller surface area-to-volume ratio. These sponges, which rely on heterotrophic feeding for more than half of their energy requirements, are referred to as mixotrophic (Usher, 2008).

The cyanobacterial symbionts may protect sponges by providing a sunscreen and might also benefit from the possible production of UV-screening substances (e.g., mycosporine-like amino acids (MAAs)) against UV radiation, permitting the holobiont to grow in shallow water (Steindler et al., 2002; Usher, 2008).

The activity of the cell-signal HRF in a sponge with algal symbionts is probably the cause of translocation from the algae to the sponge. Haliclona cymiformis HRF stimulates the release of glycerol from Symbiodinium, but does not stimulate glycerol release by its own symbionts, red macroalgae, Rhodophyta, Ceratodictyon spongiosum (Grant et al., 2006b).

The photosynthate product of the cyanobacteria translocates to the host in the marine association mainly as glycerol, while glucose produced by a chlorella-like green alga was passed to its freshwater sponge. The photosynthetic product of the cyanobacterial symbionts can supply up to 50% of the energy requirements of the host (Wilkinson, 1983). In the Great Barrier Reef, sponges may derive much of their nutrition from photosynthetic symbionts at depths of 15–30 m. Some sponges limit their depth distribution according to the availability of light for photosynthesis (Cheshire and Wilkinson, 1991).

The energy contribution of other photosynthetic associates (diatoms, dinoflagellates, and phototrophic sulfur bacteria) to the sponge is less clear (Taylor et al., 2007). The metabolism of the Mediterranean sponge Cliona viridis, associated with dinoflagellates (zooxanthellae), depends on the photosynthetic activity of these symbionts (Schonberg et al., 2005). The growth of Cliona viridis is greater under light conditions when compared with those grown under dark conditions (Rosell and Uriz, 1992). It was suggested that during air exposure at low tide, intertidal sponges are unable to filter-feed and may be more dependent on the energy from the autotrophic symbionts (Steindler et al., 2002).

The N cycle in the sponge includes assimilation of particulate organic nitrogen (PON) from seawater, ammonia oxidation, nitrite oxidation, and denitrification (Fig. 5, Taylor et al., 2007). Cyanobacterial symbionts in sponge may contribute to the N budgets of the sponge via atmospheric N2 fixation (Wilkinson and Fay, 1979; Taylor et al., 2007). This is very important for sponge-growing under oligotrophic conditions. It may explain the fact that on tropical reefs, typically 30–50% (and sometimes 80–90%) of the sponges are cyanosponges (Wilkinson, 1992).

Figure 5.
figure 5

Model of inorganic carbon uptake by sponges. (After Taylor et al., 2007.)

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The benefits of symbiosis to cyanobacteria are that it provides an acceptable growing environment. The sponges provide a solid substrate and access to higher levels of ammonium and phosphorus than those occurring in the ocean. Protection from predation by flagellates and ciliates may be another benefit to the cyanobacteria that are embedded in the host tissue (Usher, 2008).

9 Future

The origin of photosymbiosis is about 200–250 mya (Wood, 1998, 1999; Karako et al., 2002). The genus Symbiodinium spp. (clade A) was facilitated by a cooler seasonal global climate during the Eocene period ∼50 mya, which promoted regional differences and biodiversity, including the appearance of many modern coral families of scleractinian corals. Clades E, G, and D appeared around 40 mya, and clade B appeared in the early Oligocene ∼26 mya, during a warming trend (see Pochon and Pawlowski, 2006). During the last few years, it seems that clade D has had a higher tolerance to thermal stress than clade C, suggesting that corals harboring clade D are more resilient to coral bleaching events, becoming dominant after a bleaching event (Rowan, 2004; Jones et al., 2008). The evolutionary history of Symbiodinium suggests that a long-term increase in water temperature may significantly reduce Symbiodinium diversity, constituting a serious threat for the survival and diversity of coral-reef ecosystems (Pochon and Pawlowski, 2006).

Symbiosis that is based on trading energy for strategic material is well adapted to tropical oligotrophic water. During these millions of years, the relationship in the association developed through the process of evolution created one of the most impressive biodiverse biological structures of the world, the Great Barrier Reef, which represents our planet even from satellite view.

Since the Industrial Revolution, the increase in ocean temperature and the elevation in the level of pCO2, which are followed by pH decrease in addition to eutrophication and local pressure, are a major stress and threat to these ­associations (see in Carpenter et al., 2008; Stambler, 2010). These increases have already led to worldwide damage, bleaching, and death of entire reefs. The extinction risk is now much greater than it was before recent massive bleaching events. Some scientists estimate up to 60% coral mortality globally within the next few decades, and extinction of corals reefs in this century (Hoegh-Guldberg, 1999, 2005; Hoegh-Guldberg et al., 2007; Veron, 2008a, b). We must all do as much as possible to protect these associations, so that corals will be able to adapt to global and local changes.