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Life in the mangroves swamps is very harsh and challenging. Animals and plants must be able to adapt to the various environmental conditions in order to survive and many have shown strategies to either avoid stresses or to tolerate them. Ammonia toxicity in the mangroves is one key stressor that affects organisms. Yet, through the adoptions of various strategies, the giant mudskipper has shown to be one of the few animals that are able to overcome this stress and exploit the mangrove habitat.
The giant mudskipper, Periophthalmodon schlosseri (Family: Gobbidae) is one of the largest mudskippers found living in the mangrove swamps of South East Asia (Murdy, 1989; Ip et al., 1990). Being located along the intertidal coastline, the mangrove swamps experience harsh and ever-changing environmental conditions (Tan et al., 2007). Due to the regular inundation of seawater in the mangrove swamp, the soil substrate is often waterlogged and contains varying levels of salinity. The waterlogged soil causes anoxic and hypoxic conditions as it prevents the effective diffusion of oxygen, thereby reducing the concentration and availability of oxygen for mangrove organisms. Furthermore, environmental conditions in the mangrove swamp change in relation with the daily tide cycle (Tan et al., 2007). The ebb and flow of tides causes the mangrove swamp to be exposed to air twice daily, thus changing the environment from an aquatic into a terrestrial system. Therefore, allowing only well-adapted amphibious animals such as the giant mudskipper to survive in these harsh and ever-changing conditions. (Clayton, 1993)
Leading an amphibious life comes at a high cost as organisms must be physically and physiologically adapted to life in both aquatic and terrestrial systems. An aquatic fish that emerges out of water will have to face a wide range of terrestrial stresses. The giant mudskipper has shown to be physically and physiologically adapted to deal with those stresses (Harris, 1960; Kok et al, 1998; Peng et al., 1998; Sayer, 2005). Desiccation is one terrestrial stressor that will often occur during periods of low tide, when the mangrove swamp is exposed to the sun and wind (Sayer, 2005). Temperatures and evaporation rates are higher at the exposed surfaces and thus amphibious fishes have to be resistant and resilient to water loss. Also, amphibious fishes face the problems of land respiration and potential blood acidosis through accumulation of metabolic carbon dioxide in the body (Graham, 1997). Furthermore, without water as a supporting medium, amphibious fish must be well adapted for terrestrial locomotion (Sayer, 2005). Lastly, the ability of an amphibious fish to excrete nitrogenous waste is adversely affected when it is out of water, and the accumulation of ammonia over time poses severe detrimental effects, thus making ammonia toxicity a key terrestrial stressor (Kormanik and Cameron, 1981; Ip et al., 2004a).
P. schlosseri is ammoniotelic (Ip et al., 1993) and produces nitrogenous waste products such as ammonia in the liver or white muscle through the process of transdeamination (Wilkie, 1997). Ammonia is then excreted through the gills and into the water medium via diffusion and protein transporters (Wilkie, 1997). During periods of aerial exposure, the excretion of ammonia in the giant mudskipper is affected or reduced due to a lack of water as an excretory medium (Morii et al., 1978; Iwata et al., 1981; Kormanik and Cameron, 1981; Ip et al., 2004). In addition, the increase in terrestrial locomotion will cause a significant production of ammonia in the white muscle through adenylate deamination (Wilkie, 1997). Conversion of accumulated ammonia to urea via the ornithine-urea cycle is also prevented by the low activity of the enzyme, carbamyl phosphate synthetase (Lim et al., 2001). Furthermore, an accumulation of ammonia in the surrounding environment will affect the mudskipper's excretory capabilities (Ip et al., 2004b). Hence, there will be an overall buildup of endogenous ammonia over time.
The increase in internal ammonia will result in increasing toxicity which will cause several detrimental effects. Firstly, prolong exposure to ammonia causes drastic changes to gill tissues which increases the susceptibility to disease manifestation and the consequent failure in the respiratory system (Smart, 1976).
Secondly, high ammonia level may cause the death of an individual through suffocation. When in solution, ammonia reversibly forms ammonium ions which are able to activate and positively alter the enzymatic affinity of phosphofructokinase for its substrate molecules of fructose-6-phosphate and adenosine triphosphates (Kuhn et al., 1974), therefore increasing the rate of glycolysis (De Leockler, 1964). The increasing amount of hydrogen ions produced from glycolysis is neutralized by bicarbonate ions found in the blood (Sousa and Meade, 1977). The removal of bicarbonate ions in the blood affects the ratio between bicarbonate and partial pressure of carbon dioxide, thus reducing the pH and causing acidosis (Sousa and Meade, 1977). Acidosis may induce suffocation and the consequent death of the individual due to reduced oxygen affinity and lower oxygen saturation levels in blood hemoglobin (Root and Irving, 1943; Sousa and Meade, 1977).
Thirdly, high levels of ammonia will interfere with vital enzymatic reactions in the Krebs cycle which disrupts energy production (Arillo et al., 1981). The resulting decrease in energy lowers the activity of an individual, thereby affecting rate of food consumption and potential growth (Beamish and Tandler, 1990). Over time, the lack of food will weaken the fish and expose it to diseases which may ultimately result in death.
Fourthly, the rising level of cortisol as ammonia stress accumulates (Spotte and Anderson, 1989) exposes the fish to bacterial and fungal diseases (Pickering and Pottinger, 1989). Cortisol, a stress hormone (corticosteroid), has widespread effects that help restore homeostasis (Pickering and Pottinger, 1989), yet its involvement in the suppression of the immune system (Ellsaesser and Clem, 1987) increases the susceptibility to infection and potential death.
Fifthly, intoxication of ammonia will result in apoptosis (programmed cell death). Ammonium ions in solution have the ability to replace potassium ions and affect membrane potential (Binstock and Lecar, 1969). Therefore, a depolarization of the neural membrane by ammonium ions will cause the activation of N-methyl-D-aspartate (NMDA) receptors (a type of glutamate receptor) and an influx of calcium ions into the cell (Hermenegildo et al., 2000). Consequently, the calcium-dependent enzymes are activated by the increased intracellular calcium ions and drive a chain of reactions between mitochondria and the endoplasmic reticulum that eventually causes apoptosis (programmed cell death) (Boehning et al., 2003).
In order to overcome the harmful effect of ammonia toxicity on land, the giant mudskipper has adapted several physical and physiological traits to tolerate endogenous ammonia, reduce ammonia production and ensure optimal ammonia excretion. The giant mudskipper is tolerant of high levels of ammonia due to a greater ability of converting toxic ammonia into non-toxic free amino acids (Peng et al., 1998). Significant amounts of detoxification occur in the brain to prevent any irreversible damage from occurring (Mommsen and Walsh, 1991). Part of the detoxification process involves the incorporation of ammonia into α-ketoglutarate to form glutamate through the enzyme, glutamate dehydrogenase (Arillo et al., 1981; Peng et al., 1998). Glutamate together with ammonia is then subsequently converted to glutamine with glutamine synthetase as a catalyst (Arillo et al., 1981; Peng et al., 1998). Increase in endogenous ammonia concentration causes an increase in activities of glutamate dehydrogenase and glutamine synthetase which in turn maintain ammonia concentration at a non lethal limit (Peng et al., 1998).
One of the main sources of energy for a fish is through the proteolysis of proteins and the subsequent catabolism of the released amino acids (Moon and Johnston, 1981). The degradation of amino acids produces ammonia as a by-product, thus contributing to the buildup of endogenous ammonia (Mommsen and Walsh, 1992). Terrestrial exposure of the giant mudskipper will therefore cause a further rise in endogenous ammonia to lethal levels. In light of such a situation, it is necessary for the giant mudskipper to lower the rate of endogenous ammonia accumulation through the reduction of amino acid catabolism (Lim et al., 2001).
The amount of free amino acids available for catabolism is determined by the rates at which they are produced and broken down. During periods of ammonia stress in a dark environment, the amount of total free amino acids in P. schlosseri has shown to significantly decrease, thus indicating a decrease in proteolysis and in turn, a reduction in amino acid catabolism (Lim et al., 2001). However in environments experiencing alternate light and darkness, the amount of total free amino acids has shown to increase significantly (Ip et al., 2001). In periods of light, the mudskipper has an increase in activity and thus causes a rise in the rate of proteolysis and the amount of total free amino acids (Ip et al., 2001). Despite that, the rate of amino acids catabolism is low, thus reducing the accumulation of endogenous ammonia (Ip et al., 2001).
Regardless of the fact that the above-mentioned mechanism aids in slowing down ammonia accumulation, the giant mudskipper faces a constraint as the mechanism also prohibit the generation of energy through amino acids. The giant mudskipper leads a highly active lifestyle, thus it will require a large amount of energy in order to support its terrestrial activities (Kok et al., 1998). Therefore, a mechanism that allows the generation of energy via protein breakdown yet reduces ammonia production is required.
Through the process of partial amino acid catabolism, P. schlosseri is able to utilize free amino acids to obtain energy for its terrestrial activities (Ip et al., 2001). The increase in activity of the mudskipper results in an increase in the rate of proteolysis and the subsequent rise in free amino acids (Ip et al., 2001). Free amino acids that are converted into glutamate can undergo transamination with pyruvate to produce α-ketoglutarate and alanine through the facilitation of alanine aminotransferase (Ip et al., 2001). The transfer of the amino group from an amino acid to an alpha-keto acid in the process of transamination prevents the release of toxic ammonia, thus minimizing ammonia accumulation. α-Ketoglutarate then enters the Krebs cycle and undergoes partial oxidation to form malate which is subsequently converted into pyruvate by malic enzyme (Ip et at., 2001). The regenerated pyruvate is then available for further transamination reactions to produce more α-ketoglutarate.
The incomplete catabolism of α-ketoglutarate in the Krebs cycle generates a lesser amount of adenosine triphosphate (ATP) compared to that of complete catabolism (Ip et al., 2001). Yet during periods of ammonia stress, partial amino acid catabolism is an effective mechanism of allowing the giant mudskipper to obtain energy without excessive ammonia accumulation. However, this mechanism is not effective in ammonia detoxification as large amount of ammonia is still stored as alanine produced from the process of transamination.
The detoxification of ammonia is dependent on the ammonia diffusion gradient from the blood to the surrounding film of water on the epithelial. When the concentration of exogenous ammonia is lower than endogenous ammonia, ammonia in the body is able to readily diffuse out of the gills and into the surrounding water covering the gills (Wilkie, 1997). However, when the concentration of exogenous ammonia is high, the favorable ammonia gradient from blood-to-water is affected and there will be an inward diffusion of ammonia instead (Wilkie, 1997). Consequently, the giant mudskipper has adopted a method of active excretion of ammonium ions against a concentration gradient (Randall et al., 1999) and this method is also effective during aerial exposure (Chew et al., 2007). Diffusion and active excretion occur via densely packed mitochondria-rich cells in the gill epithelium (Wilson et al., 1999, 2000).
In order to enter the mitochondria-rich cells, ammonia in the blood has to be transported across the basolateral membrane through diffusion (Wilkie, 1997) or active transport by sodium-potassium ATPase (Randall et al., 1999). Ammonium ions are able to replace potassium ions (Binstock and Lecar, 1969) and bind to potassium ion binding sites on the ATPase. Due to the sodium-potassium pump, a sodium ion gradient is generated across the basolateral membrane. This gradient drives the sodium-potassium-chloride cotransporter and in the process, it is possible that ammonium ions are transported into the cell in place of potassium (Wilson et al., 2000). Carbonic anhydrase in the mitochondria-rich cells causes the conversion of carbon dioxide into bicarbonate, releasing hydrogen ions in the process. Available ammonia in the cells will be protonated by the hydrogen ions to form ammonium (Wilson et al., 2000). Accumulated ammonium ions are then transported across the apical membrane and excreted out of the cells via a sodium-hydrogen exchanger (Randall et al., 1999). The bicarbonate products are not reabsorbed into the body as they will affect the bicarbonate-carbon dioxide ratio and cause alkalosis (Sousa and Meade, 1977). Thus, bicarbonate is excreted across the apical membrane through cystic fibrosis transmembrane regulator-like anion channels and into the film of water surrounding the gills (Wilson et al., 2000). The presence of bicarbonate in the film of water acts as a buffer for the excreted ammonium ions (Wilson et al., 2000), thus allowing the excretion of more ammonium or even hydrogen ions which will in turn facilitate the excretion process (Ip et al., 2004).
Excreted ammonium can readily be converted back into ammonia which can diffuse back into the mudskipper. The occurrence of such a situation will decrease the efficiency of ammonia excretion, thus wasting large amounts of energy used for the excretion process (Ip et al., 2004). P. schlosseri is able to prevent the back diffusion of ammonia by excreting hydrogen ions into the surrounding water layer on the epithelium via V-ATPase (Hydrogen ion-translocating enzymes) (Ip et al., 2004). The surplus concentration of hydrogen ions in the water will prevent the dissociation of ammonium into ammonia, therefore preventing the back flow of ammonia (Ip et al., 2004). Acid and ammonia excretion occur in the head region, thus allowing both processes to work in tandem to ensure a high efficiency in ammonia detoxification (Ip et al., 2004). Moreover, due to this acid excretion process, the excretion of ammonia in giant mudskipper is not affected by alkaline environmental pH which is a characteristic of water in the mangroves (Chew et al., 2003).
Another strategy of preventing ammonia toxicity is through the reduction of skin permeability to ammonia. The skin of the giant mudskipper has a low permeability to ammonia (Ip et al., 2004) as compared to oxygen and carbon dioxide (Clayton, 1993). Due to the low membrane fluidity of skin cells, ammonia is not able to diffuse across and enter the body of the mudskipper (Lande et al., 1995). The membrane of the giant mudskipper has a high level of cholesterol, phosphatidylcholine and saturated fatty acids (Ip et al., 2004). Cholesterol increases membrane orderliness by restricting the movement of phospholipids (Hochachka and Somero, 2002). Phosphatidylcholine causes the formation of straight chain phospholipids, thus allowing the clustering of phospholipids and the increase in stability (Hochachka and Somero, 2002). Saturated fatty acids do not contain a kink in their conformation, thus allowing the straight chains to interact with each other and subsequently increase Van der Waals forces and stability (Hochachka and Somero, 2002). Taken together, the fluidity of the membrane is greatly reduced and its stability prevents the diffusion of ammonia across the membrane.
In conclusion, life in the mangrove swamps poses great challenges for the many organisms living there. In addition to dealing with the ever-changing environmental conditions, the plants and animals have to be adapted to life in two very distinct habitats. Out of the many terrestrial stresses, ammonia toxicity has shown to be a key stressor for aquatic organisms like the giant mudskipper. With the intention of overcoming the detrimental effects of ammonia toxicity, the giant mudskipper has adapted several physical and physiological traits. During aerial exposure, P. schlosseri is able to tolerate high levels of ammonia, obtain energy through partial amino acid catabolism yet minimize ammonia production, excrete endogenous ammonia and reduce permeability of its skin to ammonia. As such, the giant mudskipper is known to be one of the few animals that are able to exploit this harsh and challenging niche of the mangrove swamps and its survival skills remain the key to understanding the evolution of life from the sea to the land.