Abstract
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.
摘要
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。
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability statement
All data generated or analyzed during this study can be made available by the corresponding author upon reasonable request.
References
Abdulrahim SM, Haddadin MSY, Hashlamoun EAR, et al., 1996. The influence of Lactobacillus acidophilus and bacitracin on layer performance of chickens and cholesterol content of plasma and egg yolk. Br Poultry Sci, 37(2):341–346. https://doi.org/10.1080/00071669608417865
Adalsteinsdottir SA, Magnusdottir OK, Halldorsson TI, et al., 2018. Towards an individualized nutrition treatment: role of the gastrointestinal microbiome in the interplay between diet and obesity. Curr Obes Rep, 7(4):289–293. https://doi.org/10.1007/s13679-018-0321-z
Alaqaby ARA, Glaskovich AA, Kapitonova EA, et al., 2014. Study the effect of using probiotic (vetlactoflorum) on some of biochemical and immunological parameters of broiler chickens. Basrah J Vet Res, 13(1):166–179. https://doi.org/10.33762/bvetr.2014.88137
Bader J, Albin A, Stahl U, 2012. Spore-forming bacteria and their utilisation as probiotics. Benefic Microbes, 3(1):67–75. https://doi.org/10.3920/BM2011.0039
Bai SP, Wu AM, Ding XM, et al., 2013. Effects of probioticsupplemented diets on growth performance and intestinal immune characteristics of broiler chickens. Poult Sci, 92(3):663–670. https://doi.org/10.3382/ps.2012-02813
Beckman BR, Larsen DA, Moriyama S, et al., 1998. Insulin-like growth factor-I and environmental modulation of growth during smoltification of spring chinook salmon (Oncorhynchus tshawytscha). Gen Comp Endocrinol, 109(3): 325–335. https://doi.org/10.1006/gcen.1997.7036
Bian XF, Wallstrom G, Davis A, et al., 2016. Immunoproteomic profiling of antiviral antibodies in new-onset type 1 diabetes using protein arrays. Diabetes, 65(1):285–296. https://doi.org/10.2337/db15-0179
Birbrair A, Zhang T, Wang ZM, et al., 2013. Role of pericytes in skeletal muscle regeneration and fat accumulation. Stem Cells Dev, 22(16):2298–2314. https://doi.org/10.1089/scd.2012.0647
Buntyn JO, Schmidt TB, Nisbet DJ, et al., 2016. The role of direct-fed microbials in conventional livestock production. Annu Rev Anim Biosci, 4:335–355. https://doi.org/10.1146/annurev-animal-022114-111123
Cao GT, Dai B, Wang KL, et al., 2019. Bacillus licheniformis, a potential probiotic, inhibits obesity by modulating colonic microflora in C57BL/6J mice model. J Appl Microbiol, 127(3):880–888. https://doi.org/10.1111/jam.14352
Caporaso JG, Kuczynski J, Stombaugh J, et al., 2010. QIIME allows analysis of high-throughput community sequencing data. Nat Methods, 7(5):335–336. https://doi.org/10.1038/nmeth.f.303
Chen YC, Yu YH, 2020. Bacillus licheniformis-fermented products improve growth performance and the fecal microbiota community in broilers. Poult Sci, 99(3):1432–1443. https://doi.org/10.1016/j.psj.2019.10.061
Cheng GY, Hao HH, Xie SY, et al., 2014. Antibiotic alternatives: the substitution of antibiotics in animal husbandry? Front Microbiol, 5:217. https://doi.org/10.3389/fmicb.2014.00217
Das HK, Medhi AK, Islam M, 2005. Effect of probiotics on certain blood parameters and carcass characteristics of broiler chicken. Indian J Poult Sci, 40(1):83–86. https://doi.org/10.21608/epsj.2022.225224
de Boever S, Vangestel C, de Backer P, et al., 2008. Identification and validation of housekeeping genes as internal control for gene expression in an intravenous LPS inflammation model in chickens. Vet Immunol Immunopathol, 122(3–4): 312–317. https://doi.org/10.1016/j.vetimm.2007.12.002
Djouvinov D, Boicheva S, Simeonova T, et al., 2005. Effect of feeding Lactina® probiotic on performance, some blood parameters and caecal microflora of mule ducklings. Trakia J Sci, 3(2):22–28.
Edgar RC, 2013. UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods, 10(10): 996–998996–998. https://doi.org/10.1038/nmeth.2604
Edgar RC, Haas BJ, Clemente JC, et al., 2011. UCHIME improves sensitivity and speed of chimera detection. Bioinformatics, 27(16):2194–2200. https://doi.org/10.1093/bioinformatics/btr381
Ferrario C, Milani C, Mancabelli L, et al., 2016. Modulation of the eps-ome transcription of Bifidobacteria through simulation of human intestinal environment. FEMS Microbiol Ecol, 92(4):fiw056. https://doi.org/10.1093/femsec/fiw056
García-Cayuela T, Korany AM, Bustos I, et al., 2014. Adhesion abilities of dairy Lactobacillus plantarum strains showing an aggregation phenotype. Food Res Int, 57:44–50. https://doi.org/10.1016/j.foodres.2014.01.010
Hill C, Guarner F, Reid G, et al., 2014. Expert consensus document: the international scientific association for probiotics and prebiotics consensus statement on the scope and appropriate use of the term probiotic. Nat Rev Gastroenterol Hepatol, 11(8):506–514. https://doi.org/10.1038/nrgastro.2014.66
Hirayama H, Suzuki Y, Abe M, et al., 2011. Methylothermus subterraneus sp. Nov., a moderately thermophilic methanotroph isolated from a terrestrial subsurface hot aquifer. Int J Syst Evol Microbiol, 61(Pt 11):2646–2653. https://doi.org/10.1099/ijs.0.028092-0
Khalique A, Zeng D, Shoaib M, et al., 2020. Probiotics mitigating subclinical necrotic enteritis (SNE) as potential alternatives to antibiotics in poultry. Amb Express, 10:50. https://doi.org/10.1186/s13568-020-00989-6
Khan S, Roberts J, Wu SB, 2017. Reference gene selection for gene expression study in shell gland and spleen of laying hens challenged with infectious bronchitis virus. Sci Rep, 7:14271. https://doi.org/10.1038/s41598-017-14693-2
Lammers A, Wieland WH, Kruijt L, et al., 2010. Successive immunoglobulin and cytokine expression in the small intestine of juvenile chicken. Dev Comp Immunol, 34(12): 1254–1262. https://doi.org/10.1016/j.dci.2010.07.001
Lin LH, Ke FR, Zhan TT, et al., 2014. Effects of Bacillus coagulans on performance, serum biochemical indices and antioxidant function of yellow broilers. Chin J Anim Nutr, 26(12):3806–3813 (in Chinese). https://doi.org/10.3969/j.issn.1006-267x.2014.12.034
Liu JB, Yan HL, Zhang Y, et al., 2020. Effects of stale maize on growth performance, immunity, intestinal morphology and antioxidant capacity in broilers. Asian-Australas J Anim Sci, 33(4):605–614. https://doi.org/10.5713/ajas.19.0224
Liu SQ, Wang LY, Liu GH, et al., 2018. Leucine alters immunoglobulin a secretion and inflammatory cytokine expression induced by lipopolysaccharide via the nuclear factor-κB pathway in intestine of chicken embryos. Animal, 12(9): 1903–1911. https://doi.org/10.1017/S1751731117003342
Liu X, Li SR, Wang ZY, et al., 2018. Effects of dietary lipids and clostridium butyricum on chicken volatile flavour compounds. Indian J Anim Res, 52(8):1167–1173. https://doi.org/10.18805/ijar.v0iOF.6998
Liu XL, Yan H, Lv L, et al., 2012. Growth performance and meat quality of broiler chickens supplemented with Bacillus licheniformis in drinking water. Asian-Australas J Anim Sci, 25(5):682–689. https://doi.org/10.5713/ajas.2011.11334
Livak KJ, Schmittgen TD, 2001. Analysis of relative gene expression data using real-time quantitative PCR and the \({2^{ - \Delta \Delta {C_T}}}\) method. Methods, 25(4):402–408. https://doi.org/10.1006/meth.2001.1262
Livingston ML, Cowieson AJ, Crespo R, et al., 2020. Effect of broiler genetics, age, and gender on performance and blood chemistry. Heliyon, 6(7):e04400. https://doi.org/10.1016/j.heliyon.2020.e04400
Lokapirnasari WP, al Arif A, Soeharsono S, et al., 2019. Improves in external and internal egg quality of Japanese quail (Coturnix coturnix japonica) by giving lactic acid bacteria as alternative antibiotic growth promoter. Iran J Microbiol, 11(5):406–411. https://doi.org/10.18502/ijm.v11i5.1959
Louis P, Flint HJ, 2009. Diversity, metabolism and microbial ecology of butyrate-producing bacteria from the human large intestine. FEMS Microbiol Lett, 294(1):1–8. https://doi.org/10.1111/j.1574-6968.2009.01514.x
Magoč T, Salzberg SL, 2011. FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics, 27(21):2957–2963. https://doi.org/10.1093/bioinformatics/btr507
Massacci FR, Lovito C, Tofani S, et al., 2019. Dietary Saccharomyces cerevisiae boulardii CNCM I-1079 positively affects performance and intestinal ecosystem in broilers during a Campylobacter jejuni infection. Microorganisms, 7(12):596. https://doi.org/10.3390/microorganisms7120596
Mehdi Y, Létourneau-Montminy MP, Gaucher ML, et al., 2018. Use of antibiotics in broiler production: global impacts and alternatives. Anim Nutr, 4(2):170–178. https://doi.org/10.1016/j.aninu.2018.03.002
Michaelidou K, Tzovaras A, Missitzis I, et al., 2013. The expression of the CEACAM19 gene, a novel member of the CEA family, is associated with breast cancer progression. Int J Oncol, 42(5):1770–1777. https://doi.org/10.3892/ijo.2013.1860
Mohan B, Kadirvel R, Bhaskaran M, et al., 1995. Effect of probiotic supplementation on serum/yolk cholesterol and on egg shell thickness in layers. Br Poultry Sci, 36(5): 799–803. https://doi.org/10.1080/00071669508417824
Mohan B, Kadirvel R, Natarajan A, et al., 1996. Effect of probiotic supplementation on growth, nitrogen utilisation and serum cholesterol in broilers. Br Poultry Sci, 37(2):395–401. https://doi.org/10.1080/00071669608417870
Panda AK, Raju MVLN, Rama RSV, et al., 2005. The influence of supplementation of Lactobacillus sporogenes on the performance of broilers. Indian J Anim Nutr, 22(1):37–40. https://doi.org/10.2141/jpsa.43.23537-40
Panda AK, Rao SVR, Raju MVLN, et al., 2006. Dietary supplementation of Lactobacillus sporogenes on performance and serum biochemico-lipid profile of broiler chickens. J Poult Sci, 43(3):235–240. https://doi.org/10.2141/jpsa.43.235
Russell DA, Ross RP, Fitzgerald GF, et al., 2011. Metabolic activities and probiotic potential of bifidobacteria. Int J Food Microbiol, 149(1):88–105. https://doi.org/10.1016/j.ijfoodmicro.2011.06.003
Scanes CG, 2009. Perspectives on the endocrinology of poultry growth and metabolism. Gen Comp Endocrinol, 163(1–2): 24–32. https://doi.org/10.1016/j.ygcen.2009.04.013
Surai PF, Kochish II, Fisinin VI, 2017. Antioxidant systems in poultry biology: nutritional modulation of vitagenes. Eur Poult Sci, 81:1–21. https://doi.org/10.1399/eps.2017.214
Thapa BR, Walia A, 2007. Liver function tests and their interpretation. Indian J Pediatr, 74(7):663–671. https://doi.org/10.1007/s12098-007-0118-7
Vital M, Howe AC, Tiedje JM, 2014. Revealing the bacterial butyrate synthesis pathways by analyzing (meta) genomic data. mBio, 5(2):e00889–14. https://doi.org/10.1128/mBio.00889-14
Wang X., Hu Y., Zhu X, et al., 2023. Bacteroides-derived isovaleric acid enhances mucosal immunity by facilitating intestinal IgA response in broilers. J Animal Sci Biotechnol, 14:4. https://doi.org/10.1186/s40104-022-00807-y
Zheng JS, Wittouck S, Salvetti E, et al., 2020. A taxonomic note on the genus Lactobacillus: description of 23 novel genera, emended description of the genus Lactobacillus Beijerinck 1901, and union of Lactobacillaceae and Leuconostocaceae. Int J Syst Evol Microbiol, 70(4):2782–2858. https://doi.org/10.1099/ijsem.0.004107
Acknowledgments
This work was supported by the National Natural Science Foundation of China (No. 31925037). We thank Yan lab’s members for helpful discussion and critical reading of the manuscript.
Author information
Authors and Affiliations
Contributions
Muhammad Zahid FAROOQ and Xinkai WANG performed the experimental research and data analysis, wrote and edited the manuscript. Xianghua YAN contributed to the study design, data analysis, writing and editing of the manuscript. All authors have read and approved the final manuscript, and therefore, have full access to all the data in the study and take responsibility for the integrity and security of the data.
Corresponding author
Ethics declarations
Xianghua YAN is an editorial board member for Journal of Zhejiang University-SCIENCE B (Biomedicine & Biotechnology) and was not involved in the editorial review or the decision to publish this article. Muhammad Zahid FAROOQ, Xinkai WANG, and Xianghua YAN declare that they have no conflict of interest.
All experimental procedures involving chickens were approved by the Institutional Animal Care and Use Committee of Huazhong Agricultural University (approval number: HZAUCH- 2019-014).
Rights and permissions
About this article
Cite this article
Farooq, M.Z., Wang, X. & Yan, X. Effects of Aeriscardovia aeriphila on growth performance, antioxidant functions, immune responses, and gut microbiota in broiler chickens. J. Zhejiang Univ. Sci. B 24, 1014–1026 (2023). https://doi.org/10.1631/jzus.B2200621
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1631/jzus.B2200621