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Effects of Clostridium Butyricum on Growth Performance, Metabonomics

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Effects of Clostridium Butyricum on Growth Performance, Metabonomics Liang et al. BMC Microbiology (2021) 21:85 https://doi.org/10.1186/s12866-021-02143-z RESEARCH ARTICLE Open Access Effects of Clostridium butyricum on growth performance, metabonomics and intestinal microbial differences of weaned piglets Jing Liang1, Shasha Kou1, Cheng Chen1, Sayed Haidar Abbas Raza2, Sihu Wang2,XiMa1,3, Wen-Ju Zhang1* and Cunxi Nie1* Abstract Background: Weaning stress of piglets causes a huge economic loss to the pig industry. Balance and stability of the intestinal microenvironment is an effective way to reduce the occurance of stress during the weaning process. Clostridium butyricum, as a new microecological preparation, is resistant to high temperature, acid, bile salts and some antibiotics. The aim of present study is to investigate the effects of C. butyricum on the intestinal microbiota and their metabolites in weaned piglets. Results: There was no statistical significance in the growth performance and the incidence of diarrhoea among the weaned piglets treated with C. butyricum during 0–21 days experimental period. Analysis of 16S rRNA gene sequencing results showed that the operational taxonomic units (OTUs), abundance-based coverage estimator (ACE) and Chao index of the CB group were found to be significantly increased compared with the NC group (P <0.05).Bacteroidetes, Firmicutes and Tenericutes were the predominant bacterial phyla in the weaned piglets. A marked increase in the relative abundance of Megasphaera, Ruminococcaceae_NK4A214_group and Prevotellaceae_UCG-003, along with a decreased relative abundance of Ruminococcaceae_UCG-005 was observed in the CB group, when compared with the NC group (P < 0.05). With the addition of C. butyricum, a total of twenty-two significantly altered metabolites were obtained in the feces of piglets. The integrated pathway analysis by MetaboAnalyst indicated that arginine and proline metabolism; valine, leucine and isoleucine biosynthesis; and phenylalanine metabolism were the main three altered pathways, based on the topology. Furthermore, Spearman’s analysis revealed some altered gut microbiota genus such as Oscillospira, Ruminococcaceae_NK4A214_group, Megasphaera, Ruminococcaceae_UCG-005, Prevotella_2, Ruminococcaceae_UCG-002, Rikenellaceae_RC9_gut_group and Prevotellaceae_UCG-003 were associated with the alterations in the fecal metabolites (P < 0.05), indicating that C. butyricum presented a potential protective impact through gut microbiota. The intestinal metabolites changed by C. butyricum mainly involved the variation of citrulline, dicarboxylic acids, branched-chain amino acid and tryptophan metabolic pathways. Conclusions: Overall, this study strengthens the idea that the dietary C. butyricum treatment can significantly alter the intestinal microbiota and metabolite profiles of the weaned piglets, and C. butyricum can offer potential benefits for the gut health. Keywords: Clostridium butyricum, Growth performance, Intestinal microbiota, Metabolomics, Weaned piglet * Correspondence: [email protected]; [email protected] 1College of Animal Science and Technology, Shihezi University, Shihezi, Xinjiang 832003, People’s Republic of China Full list of author information is available at the end of the article © The Author(s). 2021 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Liang et al. BMC Microbiology (2021) 21:85 Page 2 of 16 Background Furthermore, we attempted to explore the possible rela- Weaning stressors are generally associated with the tionship between the bodyweight, incidence of diarrhea, changes in environment, diet, management, and separ- intestinal microbiota and metabolomics. ation from the mother that exhibit a negative impact on the growth performance and intestinal health of the Methods young animals, leading to diarrhoea, slow growth, and Animals, diet, and sampling decreased ability to resist disease [1]. Alleviating stress Ninety crossbred [(Yorkshire×Landrace) × Duroc] piglets damage caused by weaning in piglets is an urgent prob- (male: female was 45: 45) with (6.22 ± 0.24) kg of body lem to be solved. In the last few years, antibiotics have weight weaned at (28 ± 2) days of age were randomly al- acted a pivotal part in controlling the diseases in ani- located into 3 groups with 6 replicates per group and 5 mals, and improving animal growth and reproductive piglets in each replicate. They were NC group (control performance. However, antibiotics can improve the tol- diet, negative control), PC group [control diet + 0.1 g erance of pathogenic bacteria, kill beneficial bacteria, antibiotic (colistin sulphate)/kg of control diet] and CB and may cause a damage to the environment. With this group (control diet + 5 × 108 CFU C. butyricum/kg of background, the Ministry of Agriculture and Rural Af- control diet). The diets were fed in amounts that met or fairs of the People’s Republic of China in 2020 has re- exceeded National Research Council (NRC) nutrient rec- stricted the use of antibiotics as growth promoters in ommendations [28]. The C. butyricum culture was ob- animal feed. Thus, there is an urgency to find an effi- tained from the Zhejiang Huijia Bio-technology Co., Ltd. cient alternative to reduce the economic losses caused (Zhejiang, China). It was isolated from the contents of by this prohibition. Several studies have demonstrated pig intestines. The strain number was HJCB998 and pre- that the microbial ecological agents, organic acids, essen- served by China General Microbiological Culture Collec- tial oils and probiotics can act as the potential alterna- tion Center (CGMCC). Colistin sulphate was purchased tives for the use of antibiotics [2–5]. by the veterinary drug factory of Shihezi city. The com- The probiotic C. butyricum is well known gram- position and nutrient content of the control diets are positive and obligate anaerobic bacillus [6] that can col- shown in Table 1. The feeding management of piglets, onise the intestinal tract of animals [7]. As an important the measurement and calculation of average daily gain constituent of probiotics, C. butyricum has been used to (ADG), average daily feed intake (ADFI), feed to gain ra- prevent or treat the intestinal disorders of animals [8– tio (F/G) and diarrhoea incidence were followed by our 10]. Apart from the beneficial effects on intestinal tract, previous study [29]. Faecal samples of the piglets were C. butyricum addition was recently reported to promote the growth in animals [11–15], improve immune re- Table 1 Composition and nutrient levels of control diet (air- sponse [16, 17], and regulate the structure and compos- dried basis, %) ition of gut microbiota in livestock [18–20]. Gut Ingredients Content Nutrient levelsb Content microbiota affects the digestion and absorption of nutri- ents [21, 22], and the microbial metabolites associated Corn 58.60 Digestible energy (MJ/kg) 13.68 with them are known to cause majority of the biological Soybean meal 17.50 effects [23]. Expanded soybean 7.50 Crude protein 20.40 Metabolomics has an enormous potential for studying Milk powder 4.00 Lys 1.30 the functions in complex systems and expanding know- Fish meal 4.00 Met+Cys 0.78 ledge about gut microbial metabolism [24]. Metabolo- Whey power 4.30 Thr 0.87 mics has been used to study the metabolism of pigs at present [25, 26]. Although there are several studies on C. NaCl 0.30 Na 0.27 butyricum in livestock, the microbiome-metabolomics Limestone 1.22 Ca 0.95 analysis has been not extensively studied, especially in CaHPO4 1.16 Available P 0.39 the piglets. Recent studies have described the microbial DL-met 0.07 production and bioavailabilities of xenometabolites and Lys·HCL 0.35 their derivatives, which makes it important to under- Premixa 1.00 stand the influence of the microbiota on the host physi- ology [27]. Therefore, the present study was conducted Total 100.00 a in order to assess the effects of C. butyricum on the The premix provided the per kg of diet as follows: VA 8000 IU, VB1 4 mg, VB2 3.6 mg, VB5 40 mg, VB6 4 mg, VB12 0.02 mg, VD3 3000 IU, VE 20 IU, VK3 2 mg, growth performance, metabonomics and intestinal mi- biotin 0.15, folic acid 1 mg, D-pantothenic acid 11 mg, nicotinic acid 10 mg, crobial differences in weaned piglets by sequencing of antioxidant 100 mg, Cu (as copper sulfate) 10 mg, Fe (as ferrous sulfate) 80 mg, Mn (as manganese sulfate) 30 mg, Zn (as zinc sulfate) 75 mg, I (as potassium the 16S rRNA gene and a liquid chromatography-mass iodide) 0.4 mg, Se (as sodium selenite) 0.3 mg. b Digestible energy and spectrometry (LC-MS) platform based metabolomics. Available P were calculated values, while the others were measured values Liang et al. BMC Microbiology (2021) 21:85 Page 3 of 16 collected by rectal stimulation on day 21. Three piglets each sequence of 16S rRNA gene was analysed by the were randomly selected from each group, the faecal sam- Ribosomal Database Project (RDP) Classifier algorithm ples were stored in cryosurgery tubes, immediately deep- (http://rdp.cme.msu.edu/)againstthefullSILVA16S frozen in liquid nitrogen and stored at − 80 °C until fur- rRNA gene reference database (https://www.arb-silva.
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