Metabolic adaptation of two pig muscles to cold rearing conditions

Abstract

Cold environment represents an external stress modulating animal growth and energy use. At muscle level, adaptation to cold conditions potentially involves energy homeostasis regulation gauged by the adenosine monophosphate (AMP)-activated protein kinase (AMPK). Our study aimed at evaluating the bare effects of short- and long-term cold exposure on growth performance, carcass traits, and metabolic characteristics of the oxidative semispinalis (SS) muscle and glycolytic LM and to evaluate the reversibility of short-term effects, with a special emphasis on AMPK activity. A total of 84 pigs fed ad libitum and individually housed were submitted after weaning to either Cold (from 23 ± 1 to 15 ± 3°C) or thermoneutral (T; from 28 ± 1 to 23 ± 1°C) temperature up to 24.7 ± 1.6 kg BW (25 BW). Twelve Cold and 12 T piglets were then slaughtered the same day. Eighteen remaining Cold piglets were reared at 12 ± 2°C (CC) whereas 18 Cold and 24 T piglets were reared at 23 ± 4°C (CT and TT, respectively) and slaughtered at 114.3 ± 5.9 kg (115 BW). The LM and SS samples were analyzed to determine glycolytic potential (GP), activities of lactate dehydrogenase (LDH), citrate synthase (CS), and β-hydroxy-acyl-CoA dehydrogenase (HAD) and to quantify AMPK phosphorylation Threonine 172 phosphorylated form of AMPK α1+α2 isoforms (pAMPK) / total AMPK α1+α2 isoforms (AMPK). Despite a greater ADFI (P < 0.001), Cold piglets exhibited less ADG (P < 0.001) and body fatness (P < 0.03) attesting an acute adaptation to a short-term cold exposure. A long-term cold adaptation evaluated on 115 BW pigs increased ADFI (P < 0.001) but did not influence ADG and carcass lean meat content. Cold environment influenced the dynamic of muscle metabolism in a muscle type dependent manner corresponding to an earlier and acute adaptation in SS from 8 kg onward and a belated adaptation in LM from 25 BW to 115 BW. Cold exposure was associated with a progressive increase of muscle oxidative capacity, first in the SS with greater HAD (P = 0.002) and CS activities (P = 0.03) at 25 BW and then both in SS and LM at 115 BW (P < 0.001). Conversely, in LM of CC pigs, increased GP (P < 0.001) and LDH activity (P = 0.03) were observed in addition to increased CS and HAD activities, highlighting the ability of LM to increase both its glycolytic and oxidative metabolism and to diversify its energy substrates. Pigs from CC group exhibited also less pAMPK/AMPK (P < 0.01) specifically in red SS muscle, denoting a reduced metabolic stress of this muscle after a long-term cold adaptation.