Dominant changes in the breast muscle lipid profiles of broiler chickens with wooden breast syndrome revealed by lipidomics analyses

Abstract

Background: Chicken is the most consumed meat worldwide and the industry has been facing challenging myopathies. Wooden breast (WB), which is often accompanied by white striping (WS), is a serious myopathy adversely affecting meat quality of breast muscles. The underlying lipid metabolic mechanism of WB affected broilers is not fully understood.

Results: A total of 150 chickens of a white-feathered, fast-growing pure line were raised and used for the selection of WB, WB + WS and control chickens. The lipids of the breast muscle, liver, and serum from different chickens were extracted and measured using ultra performance liquid chromatography (UPLC) plus Q-Exactive Orbitrap tandem mass spectrometry. In the breast, 560 lipid molecules were identified. Compared to controls, 225/225 of 560 lipid molecules (40.2%) were identified with differential abundance (DA), including 92/100 significantly increased neutral lipids and 107/98 decreased phospholipids in the WB/WB + WS groups, respectively. The content of monounsaturated fatty acids (MUFA) was significantly higher, and the polyunsaturated fatty acids (PUFA) and saturated fatty acids (SFA) were significantly lower in the affected breasts. In the liver, 434 lipid molecules were identified, and 39/61 DA lipid molecules (6.7%/14.1%) were detected in the WB and WB + WS groups, respectively. In the serum, a total of 529 lipid molecules were identified and 4/44 DA lipid molecules (0.8%/8.3%) were detected in WB and WB + WS group, respectively. Compared to controls, the content of MUFAs in the serum and breast of the WB + WS group were both significantly increased, and the content of SFAs in two tissues were both significantly decreased. Only five lipid molecules were consistently increased in both liver and serum in WB + WS group.

Conclusions: We have found for the first time that the dominant lipid profile alterations occurred in the affected breast muscle. The relative abundance of 40.2% of lipid molecules were changed and is characteristic of increased neutral lipids and decreased phospholipids in the affected breasts. Minor changes of lipid profiles in the liver and serum of the affected groups were founded. Comprehensive analysis of body lipid metabolism indicated that the abnormal lipid profile of WB breast may be independent of the liver metabolism.

Keywords: Broiler chicken; Lipid profile; Liver; Serum; Wooden breast.

Fig. 1

Histopathological observation of breast muscle in the control, WB and WB + WS groups. A, B The normal breast exhibited well-organized myofibers with a characteristic polygonal shape. C, D The WB group with irregular muscle cell morphology and myofiber degeneration and regeneration (arrows). E, F The WB + WS group with collagen deposition and dissolved myofibers (arrows)

Fig. 2

Lipid profiles in the control, WB and WB + WS chicken breast muscles. A Percentages of different lipid categories. PC, phosphatidylcholine; PE, phosphatidylethanolamine; TG, triglyceride; CL, cardiolipin; SM, sphingomyelin; FA, fatty acid; Cer, ceramides; PG, phosphatidylglycerol; PI, phosphatidylinositol; others included: CerP (1.25%), ceramide phosphate; LPC (1.07%), lysophosphatidylcholine; AcCa (0.71%), acyl carnitine; DG (0.54%), diglyceride; HexlCer (0.54%), simple Glc series; PA (0.54%), phosphatidic acid; PS (0.54%), phosphatidylserine; Co (0.36%), coenzyme; LPE (0.18%), lysophosphatidylethanolamine; LPS (0.18%), lysophosphatidylserine; SPHP (0.18%), Sphingosine phosphate. B Principal component analysis plot of lipidomics samples in the control, WB, and WB + WS groups. C Heatmap of significantly different lipid molecule categories affected by WB and WB + WS. Red cells and green cells in the heatmap represent increased and decreased lipids, respectively. D The relative differences in lipid content of different categories between the control and affected groups. LPE, LPS, PA, Cerp, PG, PI, CL, and FA were acquired in negative ion mode. Hex1Cer, AcCa, LPC, Cer, PS, SPHP, DG, Co, PE, SM, and TG were obtained in positive ion mode

Fig. 3

Shared differential abundance (DA) lipid molecules and the FA compositions in the control, WB and WB + WS chicken breast muscles. A, B The shared DA lipid molecules of TGs in affected groups with more than 2.5-fold change compared to the controls. C, D The shared DA lipid molecules of PCs and PEs in affected groups with less than 1.5-fold change compared to the controls. E Percentages of MUFAs, PUFAs, and SFAs in breast muscle FAs composition between the control and affected groups

Fig. 4

The shared differential abundance (DA) of lipid molecules between different tissues. A The shared DA lipid molecules of WB + WS groups between liver and serum. B The changing of FAs composition in breast muscle and serum when compared WB + WS groups to controls. MUFAs, monounsaturated fatty acids; PUFAs, polyunsaturated fatty acids; SFAs, saturated fatty acids (*P < 0.05, ** P < 0.01, *** P < 0.001)