Osmoregulation in Anthozoan–Dinoflagellate Symbiosis


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Osmoregulation in Anthozoan–Dinoflagellate Symbiosis

Endosymbiosis creates a unique osmotic circumstance. Hosts are not only responsible for balancing their internal osmolarity with respect to the external environment, but they must also maintain a compatible osmotic environment for their endosymbionts, which may themselves contribute to the net osmolarity of the host cell through molecular fluxes and/or exchange. Cnidarian hosts that harbor intracellular dinoflagellates (zooxanthellae) are excellent examples of such a symbiosis. These associations are characterized by the exchange of osmotically active compounds, but they are temporally stable under normal environmental conditions indicating that these osmotically driven exchanges are effectively and rapidly regulated. Although we have some knowledge about how asymbiotic anthozoans and algae osmoregulate, our understanding of the physiological mechanisms involved in regulating an intact anthozoan–dinoflagellate symbiosis is poor. Large-scale expulsion of endosymbiotic zooxanthellae, or bleaching, is currently considered to be one of the greatest threats to coral reefs worldwide. To date, there has been little consideration of the osmotic scenarios that occur when these symbioses are exposed to the conditions that normally elicit bleaching, such as increased seawater temperatures and UV radiation. Here we review what is known about osmoregulation and osmotic stress in anthozoans and dinoflagellates and discuss the osmotic implications of exposure to environmental stress in these globally distributed and ecologically important symbioses.

1. Osmoregulation in endosymbiosis: a unique physiological scenario

Anthozoan–dinoflagellate symbioses represent challenging and unique osmoregulatory scenarios. The host contains from one to eight intracellular symbionts of different physiological ages within a specific compartment inside its gastrodermal cells and maintains a dialogue with its dinoflagellate inhabitants that is characterized by an exchange of metabolites (Muscatine and Cernichiari, 1969; Muscatine et al., 1998). As a result, the host must balance its extracellular osmolarity with an intracellular environment that is influenced by both its own metabolism and that of its symbionts. The symbiont’s extracellular milieu is defined by the activities of the host cell, that of other symbionts within the host cell, and the host’s ability to ameliorate extracellular osmotic pressures (Fig. 1). In this sense, zooxanthellae can be seen as highly osmotically
active organelles.

It has been demonstrated that symbiotic zooxanthellae live within an osmotically different environment from that of freeliving dinoflagellates (Goiran et al., 1997). However, the processes by which this compatible osmotic environment is established and maintained are not currently understood. While the osmoregulatory components of both bacteria-fish organ symbioses (Dunlap, 1985) and nematode parasites in human
digestive tracts (Fusé et al., 1993) have been researched, endosymbiotic zooxanthellae within anthozoan cells have never been examined in this context. Understanding the osmotic relationship between dinoflagellate symbionts and host anthozoans, which include both corals and sea anemones, will help us better understand both the maintenance and the breakdown of these important symbioses.

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