Lipidomics Reveals Mitochondrial Membrane Remodeling Associated with Acute Thermoregulation in a Rodent with a Wide Thermoneutral Zone

Abstract

Mongolian gerbils (Meriones unguiculatus) have high physiological flexibility in response to acute temperature changes, and have the widest thermoneutral zone (TNZ, 26.5-38.9 °C) reported among small mammals. At the upper critical temperature (T(uc), 38.9 °C), body temperatures of gerbils were significantly increased (39-41 °C) while metabolic rates were maintained at the basal level. In contrast, below the lower critical temperature (T(lc), 26.5 °C), metabolism was elevated and body temperature stable. Rapid changes in mitochondrial membrane lipidome were hypothesized to play an important role during acute thermoregulation of gerbils. Taking advantage of a recent lipidomic technique, we examined changes in the membrane phospholipids environment and free fatty acids (FFA) production in mitochondria between 38 and 27 °C (in the TNZ), and between 27 and 16 °C (below the TNZ). At 38 °C, acute heat stress elicited distinct remodeling in mitochondrial membrane lipidome which related to a potential decrease in mitochondrial respiration and membrane fluidity compared to 27 °C. At 16 °C, a sharply decreased unsaturation index and increased chain lengths were detected in mitochondrial FFA production both in muscle and brown adipose tissue. Our results suggest that mitochondrial membrane lipid remodeling may stabilize membrane function and activity of respiration related membrane protein to maintain a stable metabolic rate at T(uc), and improve heat production by decomposing less fluid fatty acid conjugates of membrane lipids under acute cold exposure. These data therefore imply an important role of membrane remodeling during acute thermoregulation in a non-hibernating endotherm.

Expression of Genes Controlling Unsaturated Fatty Acids Biosynthesis and Oil Deposition in Developing Seeds of Sacha Inchi (Plukenetia volubilis L.)

“…Molar percentage (mol%) of each fatty acid was calculated as (100 9 mol FA)/(sum of mol FA for all FA). Unsaturation index (UI) was calculated as in Pan et al [25].…”

Implication of metabolomic profiles to wide thermoneutral zone in Mongolian gerbils (Meriones unguiculatus)

“…Basal metabolic rate were measured as oxygen consumption by using an open-flow respiration system (TSE Labmaster Calorimetry System, Germany) (Pan et al 2014). The metabolic trials were carried out between 08:00 and 18:00 hours to avoid the potential effect of circadian rhythm.…”

“…These areas experience large daily temperature fluctuations in summer, from 3 °C at night to 52 °C at noon (Wang et al 2000;Li & Wang 2005;Zhang & Wang 2007;Liu et al 2013). The gerbils have a broad thermoneutral zone with the highest upper critical temperature among reported rodents: 30-40 °C as reported by Robinson (1959); 26-38 °C by Wang et al (2000); and 26.5-38.9 °C by Pan et al (2014). This wide thermoneutral zone is related to a high tolerance for acute heat exposure (Schwimmer & Haim 2009;Gordon 2012).…”

“…At the biochemical level, the metabolic rate is regulated by specific metabolic pathways such as the tricaboxylic (TCA) cycle and oxidative phosphorylation (Hulbert & Else 2005;Ksiazek et al 2009;Konarzewski & Ksiazek 2013). Rapid mitochondrial membrane lipid remodeling during acute heat exposure at 38 °C occurs in gerbils in order to maintain oxidative phosphorylation processes and the basal metabolic rate (BMR); even their core temperature is elevated to 40 °C (Pan et al 2014). However, whether other metabolic pathways related to energy metabolism or aerobic respiration are utilized by Mongolian gerbils to maintain BMR within the thermoneutral zone under acute heat exposure remains unknown.…”

“…Based on our previous lipidomic work on the wide thermoneutral zone and high upper critical temperature of Mongolian gerbils (Pan et al 2014), gerbils rapidly remodel the membrane lipid under 3-h heat exposure at the upper critical temperature (38 °C) to maintain their metabolic rate with an elevated core temperature. In the present study, we hypothesized that metabolic pathways related to energy metabolism and the LMWA system would remain constant with an invariant metabolic rate in the wide thermoneutral zone of Mongolian gerbils.…”