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. 2023 Sep 22;24(11):1014-1026.
doi: 10.1631/jzus.B2200621.

Effects of Aeriscardovia aeriphila on growth performance, antioxidant functions, immune responses, and gut microbiota in broiler chickens

[Article in English, Chinese]
Muhammad Zahid Farooq  1   2 , Xinkai Wang  1 , Xianghua Yan  3
Affiliations

Effects of Aeriscardovia aeriphila on growth performance, antioxidant functions, immune responses, and gut microbiota in broiler chickens

[Article in English, Chinese]
Muhammad Zahid Farooq et al. J Zhejiang Univ Sci B. .

Abstract
in English, Chinese, Chinese

Aeriscardovia aeriphila, also known as Bifidobacterium aerophilum, was first isolated from the caecal contents of pigs and the faeces of cotton-top tamarin. Bifidobacterium species play important roles in preventing intestinal infections, decreasing cholesterol levels, and stimulating the immune system. In this study, we isolated a strain of bacteria from the duodenal contents of broiler chickens, which was identified as A. aeriphila, and then evaluated the effects of A. aeriphila on growth performance, antioxidant functions, immune functions, and gut microbiota in commercial broiler chickens. Chickens were orally gavaged with A. aeriphila (1×109 CFU/mL) for 21 d. The results showed that A. aeriphila treatment significantly increased the average daily gain and reduced the feed conversion ratio (P<0.001). The levels of serum growth hormone (GH) and insulin-like growth factor 1 (IGF-1) were significantly increased following A. aeriphila treatment (P<0.05). Blood urea nitrogen and aspartate aminotransferase levels were decreased, whereas glucose and creatinine levels increased as a result of A. aeriphila treatment. Furthermore, the levels of serum antioxidant enzymes, including catalase (P<0.01), superoxide dismutase (P<0.001), and glutathione peroxidase (P<0.05), and total antioxidant capacity (P<0.05) were enhanced following A. aeriphila treatment. A. aeriphila treatment significantly increased the levels of serum immunoglobulin A (IgA) (P<0.05), IgG (P<0.01), IgM (P<0.05), interleukin-1 (IL-1) (P<0.05), IL-4 (P<0.05), and IL-10 (P<0.05). The broiler chickens in the A. aeriphila group had higher secretory IgA (SIgA) levels in the duodenum (P<0.01), jejunum (P<0.001), and cecum (P<0.001) than those in the control group. The messenger RNA (mRNA) relative expression levels of IL-10 (P<0.05) and IL-4 (P<0.001) in the intestinal mucosa of chickens were increased, while nuclear factor-‍κB (NF‍-‍κB) (P<0.001) expression was decreased in the A. aeriphila group compared to the control group. Phylum-level analysis revealed Firmicutes as the main phylum, followed by Bacteroidetes, in both groups. The data also found that Phascolarctobacterium and Barnesiella were increased in A. aeriphila-treated group. In conclusion, oral administration of A. aeriphila could improve the growth performance, serum antioxidant capacity, immune modulation, and gut health of broilers. Our findings may provide important information for the application of A. aeriphila in poultry production.

Aeriscardovia aeriphila，又名Bifidobacterium aerophilum，是从猪盲肠内容物中分离出的一种双歧杆菌。A. aeriphila在预防肠道感染、降低胆固醇水平和刺激免疫系统方面具有重要作用。本研究首先从肉鸡十二指肠肠道内容物中分离出一株菌， 经16S 测序鉴定为 A. aeriphila，然后我们评估了A. aeriphila对商用肉鸡生长性能、抗氧化功能、免疫功能和肠道菌群的影响。实验对21日龄的实验鸡进行了为期3周的灌服A. aeriphila（1×109 CFU/mL）处理。研究结果显示：A. aeriphila处理显著增加了鸡的平均日增重，降低了饲料转化率（P<0.001）。A. aeriphila处理后，血清生长激素（GH）和胰岛素样生长因子1（IGF-1）水平显著升高（P<0.05）。A. aeriphila处理降低了血尿素氮和天门冬氨酸氨基转移酶水平，增加了血糖和肌酐水平。同时，A. aeriphila处理显著提高了血清中抗氧化酶水平（包括过氧化氢酶（P<0.01）、超氧化物歧化酶（P<0.001）和谷胱甘肽过氧化物酶（P<0.05））及总抗氧化能力（P<0.05）。A. aeriphila处理显著增加了血清免疫球蛋白A（IgA）（P<0.05）、IgG（P<0.01）、IgM（P<0.05）、白细胞介素-1（IL-1）（P<0.05）、IL-4（P<0.05）和IL-10（P<0.05）的水平。与对照组相比，A. aeriphila组肉鸡在十二指肠（P<0.01）、空肠（P<0.001）和盲肠（P<0.001）中的分泌型免疫球蛋白A（SIgA）水平显著提高。在肠道黏膜（包括十二指肠、空肠和盲肠）中，A. aeriphila组鸡的IL-10（P<0.05）、IL-4（P<0.001）和NF-κB（P<0.001）信使RNA（mRNA）相对表达水平高于对照组。肠道微生物门水平分析显示，两组的差异菌群主要是厚壁菌门，其次是拟杆菌门。此外，A. aeriphila可提高肠道中Phascolarctobacterium和Barnesiella的丰度。综上所述，灌服A. aeriphila可改善肉鸡的生长性能、血清抗氧化能力、免疫调节和肠道健康。因此，本研究结果可以为A. aeriphila在家禽生产中的应用提供理论依据。.

Aeriscardovia aeriphila，又名 Bifidobacterium aerophilum，是从猪盲肠内容物中分离出的一种双歧杆菌。 A. aeriphila在预防肠道感染、降低胆固醇水平和刺激免疫系统方面具有重要作用。本研究首先从肉鸡十二指肠肠道内容物中分离出一株菌， 经16S 测序鉴定为 A. aeriphila，然后我们评估了 A. aeriphila对商用肉鸡生长性能、抗氧化功能、免疫功能和肠道菌群的影响。实验对21日龄的实验鸡进行了为期3周的灌服 A. aeriphila（1×10 9 CFU/mL）处理。研究结果显示： A. aeriphila处理显著增加了鸡的平均日增重，降低了饲料转化率（ P<0.001）。 A. aeriphila处理后，血清生长激素（GH）和胰岛素样生长因子1（IGF-1）水平显著升高（ P<0.05）。 A. aeriphila处理降低了血尿素氮和天门冬氨酸氨基转移酶水平，增加了血糖和肌酐水平。同时， A. aeriphila处理显著提高了血清中抗氧化酶水平（包括过氧化氢酶（ P<0.01）、超氧化物歧化酶（ P<0.001）和谷胱甘肽过氧化物酶（ P<0.05））及总抗氧化能力（ P<0.05）。 A. aeriphila处理显著增加了血清免疫球蛋白A（IgA）（ P<0.05）、IgG（ P<0.01）、IgM（ P<0.05）、白细胞介素-1（IL-1）（ P<0.05）、IL-4（ P<0.05）和IL-10（ P<0.05）的水平。与对照组相比， A. aeriphila组肉鸡在十二指肠（ P<0.01）、空肠（ P<0.001）和盲肠（ P<0.001）中的分泌型免疫球蛋白A（SIgA）水平显著提高。在肠道黏膜（包括十二指肠、空肠和盲肠）中， A. aeriphila组鸡的 IL-10（ P<0.05）、 IL-4（ P<0.001）和 NF-κB（ P<0.001）信使RNA（mRNA）相对表达水平高于对照组。肠道微生物门水平分析显示，两组的差异菌群主要是厚壁菌门，其次是拟杆菌门。此外， A. aeriphila可提高肠道中 Phascolarctobacterium和 Barnesiella的丰度。综上所述，灌服 A. aeriphila可改善肉鸡的生长性能、血清抗氧化能力、免疫调节和肠道健康。因此，本研究结果可以为 A. aeriphila在家禽生产中的应用提供理论依据。

Keywords: Aeriscardovia aeriphila; Chicken; Gut health; Immune function; Microbiome.

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Figures

Fig. 1
Fig. 1. Effects of Aeriscardovia aeriphila on growth performance and the levels of serum hormones in broilers. (a) Feed conversion ratio (FCR) of broilers; (b) Average daily gain (ADG) of broilers; (c) Average daily feed intake (ADFI) of broilers; (d) Serum growth hormone (GH) levels in broilers; (e) Serum insulin-like growth factor-1 (IGF-1) levels in broilers. The data are presented as mean±standard deviation (SD), with n=6 (a‍ ‒‍ c) and n=10 (d, e), and were evaluated by Student's t-test ( * P<0.05, ** P<0.01, *** P<0.001).
Fig. 2
Fig. 2. Serological analyses of the levels of serum total bilirubin (TBIL) (a), aspartate aminotransferase (AST) (b), glucose (GLU) (c), creatinine (CRE) (d), blood urea nitrogen (BUN) (e), albumin (ALB) (f), triglyceride (TG) (g), total protein (TP) (h), alanine aminotransferase (ALT) (i), and total cholesterol (TCHO) (j) in broilers. The data are presented as mean±standard deviation (SD), with n=10, and were evaluated by Student's t-test ( * P<0.05, ** P<0.01, *** P<0.001).
Fig. 3
Fig. 3. Effects of Aeriscardovia aeriphila on the redox state and antioxidant levels in broilers. The impacts of A. aeriphila on the glutathione peroxidase (GSH-Px) (a), catalase (CAT) (b), total antioxidant capacity (T-AOC) (c), and superoxide dismutase (SOD) (d) activity, and the malondialdehyde (MDA) level (e) in broilers. The results are represented as mean±standard deviation (SD), with n=10, and were evaluated by Student's t-test ( * P<0.05, ** P<0.01, *** P<0.001).
Fig. 4
Fig. 4. Effects of oral administration of Aeriscardovia aeriphila on the levels of immunoglobulins and cytokine secretion. Levels of serum immunoglobulin A (IgA) (a), IgG (b), IgM (c), interleukin-1 (IL-1) (d), IL-4 (e), IL-6 (f), IL-10 (g), transforming growth factor-‍ β (TGF‍ -‍ β) (h), and interferon-γ (IFN-γ) (i) in broilers. The results are represented as mean±standard deviation (SD), with n=10, and were evaluated by Student's t-test ( * P<0.05, ** P<0.01).
Fig. 5
Fig. 5. Levels of intestinal secretory immunoglobulin A (SIgA) and messenger RNA (mRNA) relative expression of interleukin-4 ( IL-4), IL-10, and nuclear factor-‍ κB ( NF ‍ - ‍ κB) in the control and Aeriscardovia aeriphila groups. The levels of intestinal SIgA in the duodenum (a), jejunum (b), and cecum (c) and the mRNA relative expression of IL-4 (d), IL-10 (e), and NF-κB (f) in control and A. aeriphila-treated broilers. Data are shown as mean±standard deviation (SD), with n=10, and were evaluated by Student's t-test ( * P<0.05, ** P<0.01, *** P<0.001).
Fig. 6
Fig. 6. Average proportion of each 16S sequence read attributed to each taxon in the control and Aeriscardovia aeriphila groups. (a) Species dilution curve based on operational taxonomic units (OTUs); (b) Rank curve based on OTUs; (c) Shannon dilution curve.
Fig. 7
Fig. 7. Alpha and beta diversities of operational taxonomic units (OTUs) in Aeriscardovia aeriphila and control groups. (a) Abundance-based coverage estimator (ACE) index; (b) Chao1 richness (Chao1) index; (c) Coverage; (d) Evenness; (e) Shannon index; (f) Simpson index; (g) Principal co-ordinates analysis (PCoA) of bacterial communities. Data are expressed as mean±standard deviation (SD), with n=10, and were evaluated by unpaired Student's t-test (NS: not significant; P>0.05).
Fig. 8
Fig. 8. Taxonomic compositions of gut microbiota in broilers. Gut bacterial taxonomic compositions at the phylum (a), class (b), order (c), family (d), and genus (e) levels.
Fig. 9
Fig. 9. Taxonomic differences between the control and Aeriscardovia aeriphila groups. (a) Cladogram based on the linear discriminant analysis (LDA) effect size (LEfSe) showing differentially abundant taxonomic clades with an LDA score of >4.0 between the A. aeriphila and control groups. Biomarker taxa are heighted by colored circles, and the circle diameter is relative to the abundance of biomarkers. (b) LEfSe between A. aeriphila (red) and control (green). (c, d) Boxplots representing the average proportion of each 16S sequence read attributed to each taxon at the family level (c) and at the genus level (d) (blue, control samples; red, A. aeriphila samples). Data are represented as mean±standard deviation (SD), with n=10, and were evaluated by unpaired Student's t-test ( * P<0.05, ** P<0.01). FC: fold change.
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