Comprehensive evaluation of the metabolic effects of insect meal from Tenebrio molitor L. in growing pigs by transcriptomics, metabolomics and lipidomics

Abstract

Abstract Background The hypothesis was tested that insect meal (IM) as protein source influences intermediary metabolism of growing pigs. To test this, 30 male, 5-week-old crossbred pigs were randomly assigned to 3 groups of 10 pigs each with similar body weights (BW) and fed isonitrogenous diets either without (CON) or with 5% IM (IM5) or 10% IM (IM10) from Tenebrio molitor L. for 4 weeks and key metabolic tissues (liver, muscle, plasma) were analyzed using omics-techniques. Results  Most performance parameters did not differ across the groups, whereas ileal digestibilities of most amino acids were 6.7 to 15.6%-units lower in IM10 than in CON (P < 0.05). Transcriptomics of liver and skeletal muscle revealed a total of 166 and 198, respectively, transcripts differentially expressed between IM10 and CON (P < 0.05). Plasma metabolomics revealed higher concentrations of alanine, citrulline, glutamate, proline, serine, tyrosine and valine and a lower concentration of asparagine in IM10 than in CON (P < 0.05). Only one out of fourteen quantifiable amino acid metabolites, namely methionine sulfoxide (MetS), in plasma was elevated by 45% and 71% in IM5 and IM10, respectively, compared to CON (P < 0.05). Plasma concentrations of both, major carnitine/acylcarnitine species and bile acids were not different across groups. Lipidomics of liver and plasma demonstrated no differences in the concentrations of triacylglycerols, cholesterol and the main phospholipids, lysophospholipids and sphingolipids between groups. The percentages of all individual phosphatidylcholine (PC) and phosphatidylethanolamine (PE) species in the liver showed no differences between groups, except those with 6 double bonds (PC 38:6, PC 40:6, PE 38:6, PE 40:6), which were markedly lower in IM10 than in CON (P < 0.05). In line with this, the percentage of C22:6n-3 in hepatic total lipids was lower in IM10 than in the other groups (P < 0.05). Conclusions Comprehensive analyzes of the transcriptome, lipidome and metabolome of key metabolic tissues indicate that partial or complete replacement of a conventional protein source by IM in the diet has only a weak impact on the intermediary metabolism of growing pigs. Thus, it is concluded that IM from Tenebrio molitor L. can be used as a dietary source of protein in pigs without causing adverse effects on metabolism.