Pressure and Membranes
The sol–gel state of lipids, or their fluidity, has the potential to be profoundly altered by pressure, as it is with temperature. In fact, high pressure and low temperature have similar effects on membrane lipids: both tend to make them more crystalline, i.e. less fluid (Hazel and Williams 1990). Solutions to the problems posed by the ordering effects of hydrostatic pressure and low temperature are solved in a similar manner. In both cases, membrane lipids increase the incidence of double bonds, or their “kinkiness,” to increase fluidity.
Evidence supporting the contention that the membranes of deep‐sea species are more fluid than those of their shallower dwelling counterparts is more sparse than would be ideal (cf. Hazel and Williams 1990), but it is present, nonetheless. In a benchmark publication from 1984, Cossins and MacDonald found that membrane lipids isolated from the brains of a suite of fishes dwelling between 200 and 4800 m showed significant increases in fluidity with depth consistent with homeoviscous adaptation. Evidence was not conclusive for lipids isolated from other organs, notably liver and kidney, due largely to variability between samples, but trends were similar.
Further evidence supporting membrane adaptation to pressure comes from study of membrane‐bound enzymes, notably the ion‐pumping enzyme Na‐K ATPase, an important player in the osmoregulation of fishes. Gibbs and Somero (1989, 1990) first tested the pressure sensitivity of enzymes from fishes dwelling in a variety of habitats: shallow‐warm, shallow‐cold, hydrothermal vent (deep‐warm), and deep cold (Figure 2.21). As might be expected, they found that the order of pressure sensitivity (highest to lowest) was shallow‐warm, shallow‐cold, deep‐warm, and deep‐cold. The investigators then manipulated the membrane environment of the Na+ K+ ATPase to assess the influence of the membrane fraction on enzyme activity. They found that enzyme from a warm‐shallow species (the barracuda Sphyraena) placed in a membrane environment derived from the cold deep‐dwelling fish Coryphaenoides armatus was less pressure‐sensitive than the enzyme of a cold‐shallow species (the sablefish Anoplopoma fimbria) that was introduced into a highly ordered lipid environment derived from chicken eggs. In contrast, when enzymes from the three species were introduced into the same lipid environment, one derived from the deep‐cold species, Coryphaenoides armatus, the order of pressure sensitivity remained as stated above: warm‐shallow, cold‐shallow, and cold‐deep. The results of Gibbs and Somero provide evidence that membrane fluidity influences the function of membrane‐bound enzymes and also that changes in enzyme structure play an important role in adaptation to pressure.
Figure 2.21 Effects of lipid substitution on the pressure responses of Na+, K+‐ATPase of three species of fish from different depth‐temperature habitats. Native membrane lipids were removed and replaced with (a) chicken egg phosphatidylcholine or (b) phospholipids prepared from the gill of the abyssal grenadier Coryphaenoides armatus. Filled symbols indicate pressure responses before lipid substitution; open symbols were assays after substitution. Circle symbols represent Coryphaenoides armatus (deep sea, cold habitat); square symbols represent the sablefish Anoplopoma fimbria (shallow, cold habitat); triangles represent the barracuda Sphyraena barracuda (shallow, warm habitat).
Source: Gibbs (1997), figure 6 (p. 257). Reproduced with the permission of Academic Press.
Oxygen
At all depths of the ocean, oxygen is removed from the water column as organisms respire and organic matter is biochemically degraded. Wave action, mixing, and photosynthetic processes replenish the lost oxygen in the upper mixed layer, but a zone of minimum oxygen forms at intermediate depth in all the world’s oceans. The severity of oxygen depletion in the minimum zones varies considerably, with values of dissolved oxygen ranging from 0 ml l−1 (zero) in the Arabian Sea (Hitchcock et al. 1997) to about 4 ml l−1 in the Antarctic (Smith et al. 1999) (see Chapter 1 for plots of O2 vs. depth).
The major factors contributing to the persistence of oxygen minimum zones are global circulation patterns that result in the water at mid‐depths being out of contact with the atmosphere for hundreds of years. In areas where the water column is well‐stratified and rates of primary production are high, oxygen minima are especially severe. Dissolved oxygen values reach 0 ml l−1 and stay near zero for hundreds of meters of water depth. Examples of such regions are the Arabian Sea, Bay of Bengal, Cariaco Basin, Philippine region, the northwest Pacific margin, and the eastern tropical Pacific. Hypoxic conditions in those areas extend from the bottom of the mixed layer to about 1500 m depth.
Although the oxygen concentration in oxygen minimum zones can be <0.2 ml l−1, large populations of organisms can reside there. Those organisms include the decapods, mysids, and copepods and even large populations of midwater (mesopelagic) fishes (Gjøsaeter 1984).
Organisms that inhabit oxygen minima exhibit a range of adaptations for dealing with hypoxic conditions. These adaptations include behavior, such as diel vertical migration out of the layer, in addition to unusual morphological and physiological characteristics (Wishner et al. 2000). Childress and Seibel (1998) have proposed three modes of adaptation to the oxygen minimum: (i) development of mechanisms for efficient removal of oxygen from water; (ii) reduction of metabolic rates; and (iii) use of anaerobic metabolism to compensate for the difference between aerobic metabolism and total metabolic needs. The use of anaerobic metabolism may occur on a sustained basis, during periods of high metabolic demand, or during transient periods spent in the oxygen minimum layer by vertical migrators.
The decreased food energy available in the deep sea (Vinogradov 1970) favors an aerobic existence where there is sufficient oxygen to be utilized. However, an oxygen minimum such as that in the Arabian Sea, where oxygen drops to zero, constrains species to an anaerobic existence while resident within it. Anaerobiosis poses a special problem to vertebrates. With the exception of breath‐hold divers such as marine mammals and turtles, most vertebrates, including fish, rely exclusively on aerobic metabolism and only switch to locally active anaerobic pathways during periods of increased activity or ambient low oxygen levels. For example, tuna white muscle is very well adapted for anaerobiosis, which is used during burst swimming (Hochachka 1980).
The main anaerobic pathway used by vertebrates is glycolysis, resulting in lactate production (Withers 1992). However, two major problems arise with use of the glycolytic pathway. First, the energy yield is very low, only 2 ATP per glucose as opposed to 38 ATP per glucose from aerobic metabolism. Second, the accumulation of lactate is potentially harmful to the organism. Build‐up of lactate can lead to osmotic imbalance, acidosis, and, ultimately, inhibition of glycolysis (Withers 1992).