Abstract
Ammonia, an atmospheric pollutant in the air, jeopardizes immune function, and perturbs metabolism, especially lipid metabolism, in human and animals. The roles of intestinal microbiota and its metabolites in maintaining or regulating immune function and metabolism are irreplaceable. Therefore, this study aimed to investigate how aerial ammonia exposure influences hindgut microbiota and its metabolites in a pig model. Twelve growing pigs were treated with or without aerial ammonia (35 mg/m3) for 25 days, and then microbial diversity and microbiota-derived metabolites were measured. The results demonstrated a decreasing trend in leptin (p = 0.0898) and reduced high-density lipoprotein cholesterol (HDL-C, p = 0.0006) in serum after ammonia exposure. Besides, an upward trend in hyocholic acid (HCA), lithocholic acid (LCA), hyodeoxycholic acid (HDCA) (p < 0.1); a downward trend in tauro-deoxycholic acid (TDCA, p < 0.1); and a reduced tauro-HDCA (THDCA, p < 0.05) level were found in the serum bile acid (BA) profiles after ammonia exposure. Ammonia exposure notably raised microbial alpha-diversity with higher Sobs, Shannon, or ACE index in the cecum or colon and the Chao index in the cecum (p < 0.05) and clearly exhibited a distinct microbial cluster in hindgut indicated by principal coordinate analysis (p < 0.01), indicating that ammonia exposure induced alterations of microbial community structure and composition in the hindgut. Further analysis displayed that ammonia exposure increased the number of potentially harmful bacteria, such as Negativibacillus, Alloprevotella, or Lachnospira, and decreased the number of beneficial bacteria, such as Akkermansia or Clostridium_sensu_stricto_1, in the hindgut (FDR < 0.05). Analysis of microbiota-derived metabolites in the hindgut showed that ammonia exposure increased acetate and decreased isobutyrate or isovalerate in the cecum or colon, respectively (p < 0.05). Unlike the alteration of serum BA profiles, cecal BA data showed that high ammonia exposure had a downward trend in cholic acid (CA), HCA, and LCA (p < 0.1); a downward trend in deoxycholic acid (DCA) and HDCA (p < 0.05); and an upward trend in glycol-chenodeoxycholic acid (GCDCA, p < 0.05). Mantel test and correlation analysis revealed associations between microbiota-derived metabolites and ammonia exposure-responsive cecal bacteria. Collectively, the findings illustrated that high ammonia exposure induced the dysbiotic microbiota in the hindgut, thereby affecting the production of microbiota-derived short-chain fatty acids and BAs, which play a pivotal role in the modulation of host systematic metabolism.
Highlights
Ammonia (NH3), the sole alkaline gas in the atmosphere, is the predominant source of active nitrogen
Serum Metabolites Related to Lipids and no changes in serum adiponectin, alanine aminotransferase (ALT), aspartate aminotransferase (AST), low-density lipoprotein cholesterol (LDL-C), and very low density lipoprotein (VLDL) were observed in pigs exposed to high ammonia (p > 0.05, Figures 1A–C, Supplementary Table 2), serum high-density lipoprotein cholesterol (HDL-C) was diminished (p = 0.0006, Figure 1C, Supplementary Table 2), and serum leptin had a reduced trend (p = 0.0898, Figure 1A, Supplementary Table 2) after high ammonia exposure
The results of other serum metabolites and free amino acid (AA), as described by Tang et al [16], demonstrated that high ammonia exposure increased the concentration of serum total triglycerides (TG, p = 0.0294, Supplementary Table 2) and ApoB (p = 0.0061, Supplementary Table 2).Compared with the control pigs, the serum branched-chain amino acid (BCAA) [leucine (Leu), p < 0.0001; isoleucine (Ile), p = 0.0016; valine (Val), p = 0.0047] and aromatic AA [tyrosine (Tyr), p < 0.0001; phenylalanine (Phe), p = 0.0002] were notably increased in pigs exposed to high atmospheric ammonia (Supplementary Table 2)
Summary
Ammonia (NH3), the sole alkaline gas in the atmosphere, is the predominant source of active nitrogen. Human activities (e.g., automobiles and airplane emissions) give off ammonia [3]. There is increasing attention to ammonia release over the past few decades, because of it having adverse influences on animal and human health. Pernicious effects of aerial ammonia on the formation of atmospheric particles and reduction of air visibility have been reported [4, 5]. Numerous studies have demonstrated that atmospheric ammonia has hazardous effects on many organs of animals, causing cardiac autophagy or liver apoptosis via the mitochondrial pathway or the PETEN/AKT/mTOR pathway [6,7,8], leading to respiratory tract infection and inflammation response [9], bringing about intestinal microvilli deficiency [10] and microbial disturbance in the small intestine [11], giving rise to dysfunction of immune organs [12, 13]
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