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Volution of Mammalian Endothermic Metabolism: Itochondrial Activity and Cell Composition

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Volution of Mammalian Endothermic Metabolism: Itochondrial Activity and Cell Composition volution of mammalian endothermic metabolism: itochondrial activity and cell composition A. J. HULBERT AND PAUL LEWIS ELSE Department of Biology, University of Wollongong, Wollongong, New South Wales 2500, Australia ulbert A. J., and Paul Lewis Else. Evolution of mam- m endothermic metabolism: mitochondrial activity and cell as the mammal and the central netted dragon (Amphi bolous nuchalis) as the reptile (8, 19); however, later KTo-n< & »?«hysioL 256 (Re^latory Integrative Comp when it became necessary to prepare isolated liver cells -omparedv 1 ^ ?63f6 in Amphibolous Vf ?-B0dy vitticepsC0raP°si^n and Rattus was measurednorvegicus we changed the comparison to that between the lar-er pti e and a mammal with the same weight and body rat {Rattus norvegicus) and the bearded dragon (A. vit erature). Homogenates were prepared from liver, kidney ticeps) (12). In both of these comparisons the reptile is .heart, lung, and skeletal (gastrocnemius) muscle, and the same size as the mammal and has a preferred body :hondria were isolated. Cytochrome oxidase activities of tlssu* h°m ogenates and isolated mitochondria were meas- emperature that is the same as the mammal's body temperature. These two comparisons have given almost nrif v Wa* ?5?tem content. Phospholipids were identical results, and we believe they offer an excellent £r?mletermined. J1™ MJ?The brain,bdnev' liver, and kidney,^e fatty heart, acid compositionand skeletal system for understanding the cellular basis of endoth te were significantly larger in the mammal, whereas the ermy and its associated thermogenesis. reproductive organs, lung, and digestive tract showed no The initial comparison was restricted to four tissues Oiver, kirJxiey heart, and brain) and showed that the inedSd WT™ -o0% m more SiZG-A11 protein mammaIian and phospholipid tissues than examined the re- mammal had larger internal organs, which contained ve reptilian tissue. Although the mammalian phospho- more mitochondria, and that the total mitochondrial contained significantly less total unsaturated fatty acids membrane surface area of these tissues was approxi unsaturated fatty acids were significantly more polyun- ■ mately fourfold greater in the endotherm than the ec ted than in the reptilian tissues. Tissue cytochrome'oxi- totherm (8). This was later shown to be a general differ ictivity was significantly greater in mammals when ex- d on a wet weight basis but not when expressed on a ence between mammals and reptiles and that mitochon protein basis. Mitochondrial cytochrome oxidase activitv drial membrane surface area was allometrically related protein basis) was the same in both species in liver" to body size with a similar exponent to the metabolic .and brain but in heart, lung, and skeletal muscle rate-body size relationship (10,11). More recently, it has been shown that the mammalian liver and kidney are •onona.lllmTK °ndf-iaThe implications W6re twke of these as active differences as rePtiHan in tissue considerably leakier" to sodium and potassium ions =iuon were discussed relative to the evolution of mam- than the corresponding reptilian tissues, and this greater endothermy. leakiness possibly explains in part the increased Oo consumption ofthe mammalian tissues (12). The present consumption; ectothermy; endothermy; reptiles; phos- paper extends the detailed comparison of the two lar-er ds; membrane fatty acids; tissue protein; cytochrome species and is concerned with two main questions: 1) do mitochondria from mammalian tissues have similar en- zymic activity to those from reptilian tissues; and 2) was the increase m metabolism during the evolution of mam malian endothermy associated with any major changes ate are its body size, its body temperature, and in the composition of tissues? Tit is an endotherm or an ectotherm. Many have shown that resting endotherms (mammals MATERIALS AND METHODS •as) have a level of metabolism that is approxi- four to fve times that of similar sized ectotherms y\e1her)iaNN wZ$' ^"l ^-bi^-aminoeth- Tther V6'- physiological 1,8)>. ThlS parameters difference suchis also as maximalmanifest chromechromp c (horserf * fffheart), add lecithin (EGTA)' (type salt-f^eIX-E, egg cytoyolk) ac rate, growth rate, and aerobic endurance are ed oetween the two groups (3, 4). Over the last Mcorhcaci^ (BHtT SiH r(HfES)'.^^ hydroxy toW InTk i CIC 3Cld' and reference fatty acid *££ Tn Tk6 0bttned fr0m the Si^a Chemical. f r^^f^?.^?- V; BSA) was obtained ethyl ether were from Mai- 0363-6119/89 $1.50 Copyright © 1989 the American Physiological Sc ENDOTHERMY AND CELL COMPOSITION 1. Comparison of body composition of reptile TABLE 2. Comparison of protein content of tissues wlurus vitticeps and mammal Rattus norvegicus from reptile Amphibolous vitticeps and mammal Rattus norvegicus Significance A. vitticeps R. norvegicus of Differenc Significance %. A. vitticeps R. norvegicus of Difference 9 10 weight, g 304±34 310±24 NS n 6 6 dy weight Body weight, g 340±43 321±33 NS an 0.13±0.01 0.69±0.04 P < 0.01 Protein content, er 2.84±0.42 4.21±0.11 P < 0.01 mg protein/g tissue Iney 0.41±0.04 0.89±0.04 P < 0.01 90±10 165±5 P < 0.01 art 0.29±0.01 0.40±0.01 P < 0.01 Kidney 91±5 126±7 P < 0.01 >mach 1.12±0.01 0.49±0.03 P < 0.01 53±3 105±1 P < 0.01 estines 1.51±0.10 2.04±0.15 P < 0.02 Heart 85±4 114±5 P < 0.01 0.81±0.04 0.68±0.05 NS Lung 60±5 90±7 P < 0.01 ng P < 0.02 productive 0.66±0.13 1.37±0.31 NS Skeletal muscle 81±6 120±12 in + fur 21.21±1.28 20.00±0.55 NS tissue, n, no. of 42.82±0.90 P < 0.01 Values are means ± SE measured as mg protein/g eletal muscle 34.58±1.94 animals. tier + skeleton 36.42±1.43 25.94±1.25 P < 0.01 s are means ± SE measured as percent of body weight (minus stomach contents); n, No. of animals. NS, not significant. TABLE 3. Comparison of phospholipid fatty acid composition of liver from reptile Amphibolous Kile and 6.2% in the mammal. The mammal also vitticeps and mammal Rattus norvegicus jjnificantly more skeletal muscle than the reptile, Significance ere was no significant difference between the two A. vitticeps R. norvegicus of Difference 3 in the proportion of body mass devoted to body n 5 5 rig, the lungs, and the reproductive system. The P < 0.05 Dtal of these differences (10.9% of body weight) Phospholipid content, 0.53±0.09 0.86±0.07 mg/g tissue •mpensated by a significantly greater "other" com- Fatty acid composition, t. This other component is primarily the skeleton, mol % is a much larger part of the reptile than the X, 1.8±0.2 0.8±0.3 P < 0.05 lal. 16:0 14.8±1.6 16.5±2.3 NS 16:1 1.3±0.5 0.3±0.1 NS lough the intestines were significantly larger in the 17:0 0.6±0.1 0.6±0.1 NS lal, the stomach was significantly smaller than in Xa 0.7±0.1 0.5±0.3 NS ptile, and the net result was that there was no 18:0 20.2±1.3 27.1±3.0 NS mce in the portion of body mass devoted to the 18:1" 12.6±2.7 5.3±1.4 NS ive system between the mammal and the reptile. 18:lt 3.0±0.9 2.2±0.2 NS 8.2±0.2 NS of these differences are compatible with the much 18:2 20.7±5.8 ■ level of energy metabolism in the endothermic 18:3 2.2±0.9 0.1±0.1 NS 20:4 13.7±2.0 30.6±1.0 P < 0.001 ial compared with the ectothermic reptile. The lack 20:5 2.2±0.4 0.3±0.1 P < 0.01 erence in the digestive system at first seems un- 22:4 1.0±0.2 0.7±0.1 NS The mammalian system is the more rapid digestor 22:5 2.1±0.1 1.3±0.2 P < 0.01 22:6 1.5±0.3 4.3±0.9 P < 0.05 )sorber of nutrients, and the relatively small stom- ^Unsaturated fatty acids 61.1±1.2 53.7±1.1 P < 0.005 the mammal is probably correlated with its more Unsaturation index 155±4 185±8 P < 0.01 nt mastication of food in the mouth before swal- Average chain length 18.0±0.1 18.4±0.1 P < 0.05 '. The physiological and structural digestive adap- 20:4/18:2 1.02±0.35 3.76±0.17 P < 0.001 s associated with the evolution of endothermy in Values are means ± SE; n, no. of animals. Only fatty acids that lals are excellently covered in a series of papers by constituted >0.5% of total are shown. First no. represents no. of carbon ov and co-workers (20, 21). atoms, whereas second represents no. of double bonds. Xi and X2 are unidentified fatty acids. 18:1* is oleic acid, whereas 18:1+ is cis vacenic the mammalian tissues examined had significantly acid. Unsaturation index is sum of (mol % x no. of double bonds) for protein than the corresponding reptilian tissues each fatty acid. Average chain length is sum of (mol % X no. of carbons/ j 2). The difference was remarkably consistent 100) for each fatty acid. en tissues, with the mammalian tissue having on >e 58% more protein than the same amount of lipid content presumably represents a greater amount of an tissue.
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