Evolutionary adaptation of membranes to temperature.

Abstract

The "fluidity" of brain synaptosomal membrane preparations of arctic and hot-springs fish species, two temperate water fish species acclimated to different seasonal temperatures, and two mammals was estimated using the fluorescence polarization technique. At all measurement temperatures, the fluidity decreased in the order: arctic sculpin, 50-acclimated goldfish, 250-acclimated goldfish, desert pupfish, and rat. This correlated with increasing adaptation or body (i.e., cellular) temperatures of 0°, 50, 250, 340, and 370 and suggested a partial compensation of membrane fluidity for environmental temperature that occurs over the evolutionary time period as well as during laboratory (seasonal) acclimation. Evolutionary adaptation of relatively stenothermal species to constant thermal environments resulted in a more complete compensation than laboratory (seasonal) acclimation. Each compensation is accompanied by differences in the saturation of membrane phosphoglycerides. At increased cellular temperatures the proportion of saturated fatty acids increased and the unsaturation index decreased; the correlation between these indices and the measured expression of membrane dynamic structure was highly significant. It is concluded that the homeoviscous compensation of synaptic membrane function is an important component of temperature adaptation.Biological membranes resemble a two-dimensional, hydrophobic fluid whose dynamic nature has important consequences for a number of membrane-associated functional properties (1). A variety of organisms possess the ability to modulate the fluidity of their constituent cellular membranes in compensation for the direct effects of altered environmental temperature, a phenomenon termed "homeoviscous adaptation" (2). In Tetrahymena (3) and the synaptosomal membranes of the goldfish Carassius auratus (4), partial compensation is achieved after laboratory acclimation at different temperatures, but it is somewhat less than that required to maintain a constant "fluidity" at all environmental temperatures; partial compensation may be associated with the eurythermal properties of these animals. Bacterial membranes show a complete compensation (2, 5).Fishes that inhabit relatively constant thermal environments, particularly such extremes as polar seas or thermal springs, may be expected to exhibit a more complete homeoviscous adaptation because for them the maintenance of a eurythermal ability has no evolutionary significance. Indeed, stenothermal species often exhibit a high degree of adaptation to their respective environments such that they perish at temperatures only slightly removed from normal (6). To test the hypothesis of homeoviscous adaptation, we present here comparative studies of the fluidity and biochemical composition of synaptosomal membranes isolated from fish that live in arctic or hot-springs environments, other fish adapted to a wide range of temperatures, and rat and hamster. Synaptosomal memThe costs of publication of this article were defrayed in part by the pay...

Molecular and structural composition of phospholipid membranes in livers of marine and freshwater fish in relation to temperature.

“…Phospholipids from specific membranes of an Arctic marine fish proved more unsaturated than those of subtropical freshwater fish, and these differences were reflected in the microviscosity ofthese structures (8). The present article compares the liver phospholipid compositions of a number of marine and freshwater fish, and a feasible mechanism is proposed to explain the adaptational phenomena at a membrane structural level.…”

Mammalian phospholipid homeostasis: Homeoviscous adaptation deconstructed by lipidomic data driven modelling

“…The most compelling evidence for this mechanism stems from data where the ratio sats/unsats follows a linear progression when plotted against the membrane fluorescence polarisation of diphenyl hexatrine (DPH) (Cossins and Prosser, 1978), for animal species adapted to different mean habitation temperatures, as reviewed (Hazel, 1995). The argument that general rule across a homologous headgroup series, increases in saturated hydrocarbon chain length increase the value of T m and increasing cis unsaturation decreases the value of T m .…”

“…In development of HVA, Sinensky (Sinensky, 1974) observed using Electron Spin Resonance (ESR) that the order parameter of E. coli membranes remained constant, determined as a function of spin probe rotational correlation time, despite their phospholipid compositions changing in response to different growth temperatures. Subsequently, evidence for HVA as a conserved evolutionary mechanism emerged (Behan-Martin et al, 1993;Cossins and Prosser, 1978) and HVA has since been reported under many other changing environmental conditions, such as in response to hydrostatic pressure (Behan et al, 1992;Macdonald, 1986, 1984), osmotic pressure (Laroche et al, 2001) , low magnetic field strength (Santoro et al, 1997) and chemicals such as PCB-153 (Gonzalez et al, 2013), mitelfosine (Rybczynska et al, 2001) and crude oil (Mazzella et al, 2005). To date evidence for HVA has been found in species across the three domains of life and it is arguably the most widely used theory to explain phospholipid compositional changes, usually through the concept of maintaining membrane fluidity or membrane viscosity.…”

Nervonic Acid (24:1n-9) is a Dominant Unsaturated Fatty Acid in the Intestinal Brush Border of Atlantic Cod

“…Previous studies have shown that the PUFA content might be expected to rise when acclimating animals to lower temperatures. 3 In studies on fish, 24,34,35 this effect was mainly seen in the content of EPA and DHA. The fatty acid content of phospholipids from seven different Atlantic cod tissues was reported in an earlier study.…”

“…On the other hand, it is generally assumed that a higher average chain length would point in the direction of warm acclimation due to the ability of longer acyl chains to pack more tightly and reduce the viscosity of the membranes. 3,35 Unlike the BLM, the BBM side of the cell can be expected to be more atypical in comparison with non-epithelial cells. It has been documented earlier that BBM shows the inverse compensation behavior compared with BLM when either rainbow trout (Oncorhynchus mykiss) or common carp (Cyprinus carpio) were acclimated to the cold, that is, the BBM was shown to become more viscous 4,6 when adapting to cold.…”