Differences in meat quality between Angus cattle and Xinjiang brown cattle in association with gut microbiota and its lipid metabolism

Abstract

Gut microbiota plays important roles in mediating fat metabolic events in humans and animals. However, the differences of meat quality traits related to the lipid metabolism (MQT-LM) in association with gut microbiota involving in lipid metabolism have not been well explored between Angus cattle (AG) and Xinjiang brown cattle (BC). Ten heads of 18-month-old uncastrated male AG and BC (5 in each group) raised under the identical conditions were selected to test MQT-LM, i.e., the backfat thickness (BFT), the intramuscular fat (IMF) content, the intramuscular adipocyte areas (IAA), the eye muscle area (EMA), the muscle fiber sectional area (MFSA) and the muscle shear force after sacrifice. The gut microbiota composition and structure with its metabolic function were analyzed by means of metagenomics and metabolomics with rectal feces. The correlation of MQT-LM with the gut microbiota and its metabolites was analyzed. In comparison with AG, BC had significant lower EMA, IMF content and IAA but higher BFT and MFSA. Chao1 and ACE indexes of α-diversity were lower. β-diversity between AG and BC were significantly different. The relative abundance of Bacteroidetes, Prevotella and Blautia and Prevotella copri, Blautia wexlerae, and Ruminococcus gnavus was lower. The lipid metabolism related metabolites, i.e., succinate, oxoglutaric acid, L-aspartic acid and L-glutamic acid were lower, while GABA, L-asparagine and fumaric acid were higher. IMF was positively correlated with Prevotella copri, Blautia wexlerae and Ruminococcus gnavus, and the metabolites succinate, oxoglutaric acid, L-aspartic acid and L-glutamic acid, while negatively with GABA, L-asparagine and fumaric acid. BFT was negatively correlated with Blautia wexlerae and the metabolites succinate, L-aspartic acid and L-glutamic acid, while positively with GABA, L-asparagine and fumaric acid. Prevotella Copri, Blautia wexlerae, and Ruminococcus gnavus was all positively correlated with succinate, oxoglutaric acid, while negatively with L-asparagine and fumaric acid. In conclusion, Prevotella copri, Prevotella intermedia, Blautia wexlerae, and Ruminococcus gnavus may serve as the potential differentiated bacterial species in association with MQT-LM via their metabolites of oxoglutaric acid, succinate, fumaric acid, L-aspartic acid, L-asparagine, L-glutamic acid and GABA between BC and AG.

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“…In addition, the chemical state of myoglobin is a key factor that affects meat color ( Suman and Joseph, 2013 ). Chen et al (2022) revealed that L-aspartic acid was positively correlated with intramuscular fat concentrations, suggesting that this metabolite may determine meat quality. In practical application, aspartic acid and glutamine contribute to umami taste ( Nanda et al, 2003 ).…”

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“…Recent study reported that the F/B ratio was higher in feces of feedlot-fed Angus cattle than that in grazing cattle [ 33 ], indicating that the lower gut microbiota may influence the meat quality of cattle. In a recent study using Angus and Xinjiang brown cattle, intramuscular fat content was positively correlated with fecal Prevotella copri , Blautia wexlerae , and Ruminococcus gnavus bacterial species, and backfat thickness was negatively correlated with fecal Blautia wexlerae [ 34 ]. The relative abundance of unclassified Mogibacteriaceae and Succiniclasticum in the hindgut had a positive linear relationship with intramuscular fat content in the multibreed Angus-Brahman herd [ 35 ].…”

“…Zhang et al [ 43 ] indicated there was a strong association between fat content and lipid (ether lipid, glycerol lipid and glycerophospholipid) and carbohydrate metabolism (carbohydrate digestion and absorption, sucrose and starch, and galactose) in black Tibetan sheep. Another recent study also revealed that intramuscular fat content was positively correlated with the metabolites including succinate, oxoglutaric acid, L-aspartic acid and L-glutamic acid, and negatively correlated with GABA, L-asparagine and fumaric acid and Prevotella copri , Blautia wexlerae , and Ruminococcus gnavus [ 34 ]. Backfat thickness was negatively correlated with the metabolites including succinate, L-aspartic acid and L-glutamic acid and positively correlated with GABA, L-asparagine and fumaric acid and Blautia wexlerae [ 34 ].…”

“…Another recent study also revealed that intramuscular fat content was positively correlated with the metabolites including succinate, oxoglutaric acid, L-aspartic acid and L-glutamic acid, and negatively correlated with GABA, L-asparagine and fumaric acid and Prevotella copri , Blautia wexlerae , and Ruminococcus gnavus [ 34 ]. Backfat thickness was negatively correlated with the metabolites including succinate, L-aspartic acid and L-glutamic acid and positively correlated with GABA, L-asparagine and fumaric acid and Blautia wexlerae [ 34 ]. Metabolomic study of Japanese black beef suggested that several metabolites (decanoic acid, uric acid, elaidic acid, 3-phosphoglyceric acid) in meat were potential biomarkers of intramuscular fat to assess marbling levels [ 44 ].…”

Emerging perspectives in the gut–muscle axis: The gut microbiota and its metabolites as important modulators of meat quality

“…These reports emphasized the value of the gut microbiota in the regulation of muscle fibre characteristics and meat quality. With respect to the meat quality of cattle, most studies have focused on the association of the ruminal environment and its lipid metabolic function (Chen, Sun, et al., 2022 ; Krause et al., 2020 ; Zheng et al., 2022 ), and the potential link between the gut microbiota and muscle fibre properties has not been well explored.…”