Water deprivation induces appetite and alters metabolic strategy in Notomys alexis : unique mechanisms for water production in the desert

Abstract

Like many desert animals, the spinifex hopping mouse, Notomys alexis, can maintain water balance without drinking water. The role of the kidney in producing a small volume of highly concentrated urine has been well-documented, but little is known about the physiological mechanisms underpinning the metabolic production of water to offset obligatory water loss. In Notomys, we found that water deprivation (WD) induced a sustained high food intake that exceeded the pre-deprivation level, which was driven by parallel changes in plasma leptin and ghrelin and the expression of orexigenic and anorectic neuropeptide genes in the hypothalamus; these changed in a direction that would stimulate appetite. As the period of WD was prolonged, body fat disappeared but body mass increased gradually, which was attributed to hepatic glycogen storage. Switching metabolic strategy from lipids to carbohydrates would enhance metabolic water production per oxygen molecule, thus providing a mechanism to minimize respiratory water loss. The changes observed in appetite control and metabolic strategy in Notomys were absent or less prominent in laboratory mice. This study reveals novel mechanisms for appetite regulation and energy metabolism that could be essential for desert rodents to survive in xeric environments.Keywords: xeric adaptation; appetite regulation; brain-gut axis; energy metabolism; oxidation water INTRODUTIONThe amazing ability of desert animals to cope with extreme heat and aridity has fascinated many researchers since the beginning of the last century, and there has been significant progress in understanding the ecology and physiology of desert animals [1 -3]. The spinifex hopping mouse, Notomys alexis, is one such animal that thrives in the Australian desert [4][5][6][7][8]. In the laboratory, Notomys can maintain normal water balance (plasma osmolality and blood volume) during total water deprivation (WD) if fed on dry seeds [7,8]. Their xeric adaptability is even greater than the well-studied kangaroo rat (Dipodomys spp.) of similar size, in which WD changes body fluid parameters to some extent [9]. Many studies have shown that Notomys have an extraordinary ability to concentrate urine up to 9370 mOsm [4,6], reduce faecal water content to less than 50 per cent [4], and reduce respiratory water loss by a nasal cooling system [10] and co-habitation in burrows [5]. However, the obligatory water loss by respiration and urine production must be balanced by water gain, which in granivorous rodents is mostly from metabolic (oxidative) water [1,2].Among substrates for oxidation, lipids (fat) produce twice the amount of oxidation water than carbohydrates (starch) per gram, but starch produces 20 per cent more water than fat per kilocalorie because of a greater demand for oxygen for fat metabolism [1]. Thus, starch is a better substrate than fat for water production in a dry environment, where respiratory water loss needs to be minimized. Protein produces the least amount of oxidation water per gram and necessitates renal water ...

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