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Evolutionary Adaptation of Membranes to Temperature (Membrane Fluidity/Synaptosomes/Thermal Tolerance/Fatty Acids/Phospholipids) A

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Evolutionary Adaptation of Membranes to Temperature (Membrane Fluidity/Synaptosomes/Thermal Tolerance/Fatty Acids/Phospholipids) A Proc. Natl. Acad. Sci. USA Vol. 75, No. 4, pp. 2040-2043, April 1978 Physiological Sciences Evolutionary adaptation of membranes to temperature (membrane fluidity/synaptosomes/thermal tolerance/fatty acids/phospholipids) A. R. COSSINS* AND C. L. PROSSER Department of Physiology and Biophysics, University of Illinois, Urbana, Illinois 61801 Contributed by C. Ladd Prosser, January 16,1978 ABSTRACT The "fluidity" of brain synaptosomal mem- branes were used because resistance adaptation to temperature brane preparations of arctic and hot-springs fish species, two in fishes is in large part due to maintenance of synaptic function temperate water fish species acclimated to different seasonal temperatures, and two mammals was estimated using the flu- after acclimation to hot or cold temperatures (7). orescence polarization technique. At all measurement tem- peratures, the fluidity decreased in the order: arctic sculpin, MATERIALS AND METHODS 50-acclimated goldfish, 250-acclimated goldfish, desert pupfish, Animals. Arctic sculpin [Myoxocephalus verrucosus (Bean), and rat. This correlated with increasing adaptation or body (i.e., tentative identification, 27-30 cm length] were caught near St. cellular) temperatures of 0°, 50, 250, 340, and 370 and suggested a partial compensation of membrane fluidity for environmental George Island in the Bering Sea at approximately -0.3' and temperature that occurs over the evolutionary time period as maintained in the laboratory in artificial sea water at 0 + 10. well as during laboratory (seasonal) acclimation. Evolutionary Desert pupfish (Cyprinodon nevadensis, 3-4 cm) were reared adaptation of relatively stenothermal species to constant ther- at approximately 280 from stocks originally obtained from mal environments resulted in a more complete compensation Saratoga Springs, Death Valley National Monument, California. than laboratory (seasonal) acclimation. Each compensation is On arrival in Illinois they were kept at 280 for 2 days and slowly accompanied by differences in the saturation of membrane ± kept phosphoglycerides. At increased cellular temperatures the warmed over a 4-day period to 34 0.50, where they were proportion of saturated fatty acids increased and the unsatu- for 7 days before sacrifice. Goldfish were obtained commer- ration index decreased; the correlation between these indices cially and acclimated for at least 21 days, some at 50, others at and the measured expression of membrane dynamic structure 250 (4). Green sunfish-bluegill hybrids (Lepomis sp.) were was highly significant. It is concluded that the homeoviscous obtained from Illinois ponds and were acclimated to 50 or to compensation of synaptic membrane function is an important 250 for at least 21 days. Rats and hamsters were from laboratory component of temperature adaptation. stock. hydro- Preparation of Brain Synaptosomes. Brain synaptosomes Biological membranes resemble a two-dimensional, were prepared by differential and discontinuous sucrose gra- phobic fluid whose dynamic nature has important consequences dient centrifugation as described previously (4). for a number of membrane-associated functional properties (1). Membrane Fluidity. The fluidity of brain synaptosomal A variety of organisms possess the ability to modulate the flu- membranes was estimated using the fluorescence polarization idity of their constituent cellular membranes in compensation technique with 1,6-diphenyl-1,3,5-hexatriene (Aldrich "puriss" for the direct effects of altered environmental temperature, a grade) as fluorescence probe (4, 8, 9). Results are expressed as phenomenon termed "homeoviscous adaptation" (2). In Te- polarization of fluorescence; an increased value indicating a trahymena (3) and the synaptosomal membranes of the goldfish reduced rate of probe motion and by inference a more re- Carassius auratus (4), partial compensation is achieved after strictive hydrophobic environment (4). laboratory acclimation at different temperatures, but it is Fatty Acid Analysis. Synaptosomal lipids were extracted, somewhat less than that required to maintain a constant "flu- the major phosphoglyceride fractions were purified by two- idity" at all environmental temperatures; partial compensation dimensional thin-layer chromatography, and their constituent may be associated with the eurythermal properties of these all animals. Bacterial membranes show a complete compensation fatty acids were analyzed by gas-liquid chromatography, (2, 5). as described previously (4). Fishes that inhabit relatively constant thermal environments, RESULTS particularly such extremes as polar seas or thermal springs, may be expected to exhibit a more complete homeoviscous adap- Arrhenius plots of polarization for brain synaptosome prepa- tation because for them the maintenance of a eurythermal rations of the arctic sculpin, 5°- and 250-acclimated goldfish, ability has no evolutionary significance. Indeed, stenothermal desert pupfish, and rat are presented in Fig. 1. The experiments species often exhibit a high degree of adaptation to their re- on the arctic sculpin and desert pupfish were performed si- spective environments such that they perish at temperatures multaneously with analyses of 5°- and 25°-acclimated goldfish, only slightly removed from normal (6). To test the hypothesis respectively, in an effort to reduce the effects of minor differ- of homeoviscous adaptation, we present here comparative ences of preparative technique upon the comparison. The data studies of the fluidity and biochemical composition of synap- for rat synaptosomes have been reported previously (4) and tosomal membranes isolated from fish that live in arctic or have been included for comparative purposes. The curves hot-springs environments, other fish adapted to a wide range clearly show (a) an increased value of polarization (and by in- of temperatures, and rat and hamster. Synaptosomal mem- ference of membrane order) with reduced measurement temperature and (b) a shift of the curves upwards and to the The costs of publication of this article were defrayed in part by the left with higher acclimation, habitat, or body (i.e., cellular) payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U. S. C. §1734 solely to indicate * Present address: Department of Zoology, University of Liverpool, this fact. Box 147, Liverpool, England. 2040 Downloaded by guest on September 27, 2021 Physiological Sciences: Cossins and Prosser Proc. Natl. Acad. Sci. USA 75 (1978) 2041 Temperature, OC 0.32 E 0.30_ \_ 0. P 0.28 - *4.co 0.26_\_ .LN -6 0.24 -x c 0o (L N 0.22 - .- 'aCI 0 10 20 30 40 Cell temperature, 0C FIG. 2. Effect of adaptation or acclimation at different temper- atures upon membrane viscosity expressed as polarization measured at their respective acclimation, environmental, or body (i.e., cellular) temperatures. Arctic sculpin (a), goldfish (0), green sunfish-bluegill hybrid (-), desert pupfish (X), rat (0), and hamster (1). Each point represents an individual animal. relative estimate of the number of olefinic bonds in each phospholipid class. Despite differences in the dietary regimen of the various organisms and perhaps in desaturating ability, there was an unmistakable trend towards increased fatty acid 1000/Temperature, K unsaturation with the lower cell temperatures, particularly in FIG. 1. Arrhenius plots of polarization for diphenylhexatriene the incorporated into synaptosomal choline phosphoglycerides, where there was an increased membrane preparations of various proportion of unsaturated fatty acids as well as an increase in fish species and rat. Arctic sculpin (0°, 0, *); 50-acclimated goldfish (50, A, &, v); 250-acclimated goldfish (250, 0); desert pupfish (340, the average number of olefinic bonds per unsaturated fatty 0); rat (370, X). Each symbol represents a separate preparation. acid. In the ethanolamine phosphoglyceride fraction the satu- ration ratio decreased with lower cell temperature, but this was temperature. Thus, over the entire temperature range, sy- not associated with consistent effects upon the unsaturation naptosomal membranes of the arctic sculpin were more fluid index. Fig. 3 presents the correlation between membrane flu- than those of 50-acclimated goldfish, and the synaptosomal idity as expressed by polarization with the saturation ratio for membranes of the desert pupfish had a fluidity between those ethanolamine phosphoglyceride and choline phosphoglyceride. of 250-acclimated goldfish and the rat. In all phospholipid classes the saturation ratio exhibited a more These results are summarized in Fig. 2, together with those significant and extensive correlation with polarization than did obtained earlier for 5°-, 15°-, and 250-acclimated goldfish (4), the unsaturation index, as shown in earlier observations (10). as a plot of polarization value for each animal at its respective cellular temperature (i.e., acclimated or body temperature) 0.32 against its cellular temperature. Thermal acclimation of gold- 0.30 fish and green sunfish-bluegill hybrids resulted in a partial compensation of synaptosomal AA membrane fluidity for changes iP40.28 i E in environmental temperature, because the estimated mem- (r=0.947) brane fluidity (as expressed by polarization values) was not 00.26 Ratio oaturatedu(rad PC identical at each of the various acclimation temperatures but 0.970) .N was relatively constant at temperature extremes (Fig. 2). The 0O.24 . polarization values for the arctic sculpin at 00 were slightly 0~ lower
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