Integrated meta-omics reveals the regulatory landscape involved in lipid metabolism between pig breeds

Authors: SUN, JIAJIE - South China Agricultural Univerisity; XIE, FANG - South China Agricultural Univerisity; WANG, JING - Henan Academy Of Agricultural Science; LUO, JUNYI - South China Agricultural Univerisity; CHEN, TING - South China Agricultural Univerisity; JIANG, QINGYAN - South China Agricultural Univerisity; XI, QIANYUN - South China Agricultural Univerisity; Liu, Ge - George; ZHANG, YONGLIANG - South China Agricultural Univerisity

Submitted to: Microbiome
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 12/19/2023
Publication Date: 2/20/2024
Citation: Sun, J., Xie, F., Wang, J., Luo, J., Chen, T., Jiang, Q., Xi, Q., Liu, G., Zhang, Y. 2024. Integrated meta-omics reveals the regulatory landscape involved in lipid metabolism between pig breeds. Microbiome. 12. Article e33. https://doi.org/10.1186/s40168-023-01743-3.
DOI: https://doi.org/10.1186/s40168-023-01743-3

Interpretive Summary: Complete analyses of tissues at single-cell level will benefit our understanding of genetic bases for complex traits. We provided a single cell gene expression comparisons of four lipid-related tissues between lean and fat pig breeds. These results fill our knowledge gaps and provide the foundation for incorporating new transcriptome insights into the future animal breeding program. Farmers, scientist, and policy planners who need improve animal health and production based on genome-enabled animal selection will benefit from this study.

Technical Abstract: Domesticated pigs provide the majority of meat for human consumption and also serve as an ideal animal model for biomedical research. Porcine intermuscular fat (IMF) content is essential in pork quality and associates with human health and diseases. The molecular mechanisms controlling lipid metabolism and IMF accretion across tissues in pigs, and how these changes in response to pig breeds, remain largely unknown. Here, we surveyed the tissue-resident cell types of porcine jejunum, colon, liver and longissimus dorsi muscle between Lantang (LT) and Landrace (LW) breeds by single-cell RNA sequencing, generating a dataset of 60,514 cells and 20 major subpopulations. Combining with lipidomics and metagenomics approaches, we also characterized gene signatures and determined key discriminating markers of lipid digestibility, absorption, conversion and deposition across tissues in LT and LW piglets. In the LW breed, lean-meat swine mainly exhibited breed-specific advantages in lipid absorption and oxidation for energy supply in small and large intestinal epitheliums, nascent high-density lipoprotein synthesis for reverse cholesterol transport in enterocytes and hepatocytes, bile acid formation and secretion for fat emulsification in hepatocytes, as well as intestinal-microbiota gene expression involved in lipid accumulation product. In the LT breed, obese-meat swine showed higher synthesis capacity of chylomicrons responsible for high serum triacylglycerol levels in small intestinal epitheliums, the predominant mechanisms of lipid absorption in muscle tissue, and greater intermuscular adipcytogenesis potentials from muscular fibro-adipogenic progenitor subpopulation. The findings enhanced our understanding of the cellular biology of lipid metabolism and open new avenues to improve animal production and human diseases.