Dietary supplementation with Lactiplantibacillus plantarum P-8 improves the growth performance and gut microbiota of weaned piglets

ABSTRACTWeaning is a stressful event in the pig life cycle. We hypothesized that probiotics could be potential alternatives to antibiotics for promoting growth and ameliorating stress in weaning piglets via gut microbiota modulation and, thus, investigated the beneficial effects of dietary probiotic...

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Main Authors: Jie Yu, Bin Zuo, Qi Li, Feiyan Zhao, Junjun Wang, Weiqiang Huang, Zhihong Sun, Yongfu Chen
Format: Article
Language:English
Published: American Society for Microbiology 2024-02-01
Series:Microbiology Spectrum
Subjects:
Online Access:https://journals.asm.org/doi/10.1128/spectrum.02345-22
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author Jie Yu
Bin Zuo
Qi Li
Feiyan Zhao
Junjun Wang
Weiqiang Huang
Zhihong Sun
Yongfu Chen
author_facet Jie Yu
Bin Zuo
Qi Li
Feiyan Zhao
Junjun Wang
Weiqiang Huang
Zhihong Sun
Yongfu Chen
author_sort Jie Yu
collection DOAJ
description ABSTRACTWeaning is a stressful event in the pig life cycle. We hypothesized that probiotics could be potential alternatives to antibiotics for promoting growth and ameliorating stress in weaning piglets via gut microbiota modulation and, thus, investigated the beneficial effects of dietary probiotic supplementation in weaning pigs. Ninety weaning piglets (Landrace × large white, 45 males and 45 females, 25 days of age) were randomized into three dietary treatments (30 piglets/treatment, divided into five replicates/treatment, i.e., six piglets/replicate) in this 28-day trial: control (C group, basal diet); probiotic [lactic acid bacteria (LAB) group, basal diet plus Lactiplantibacillus plantarum P-8]; and antibiotic (A group; basal diet plus chlortetracycline). The piglets’ growth performance [average daily gain, average daily feed intake (ADFI), and feed conversion ratio (FCR)], immune and antioxidant markers, ileal mucosal morphology, and ileal and colonic microbiomes were compared among treatment groups. Compared to the C and A groups, probiotic supplementation significantly decreased the ADFI, FCR, and ileal mucosal crypt depth while increasing the villus height-to-crypt depth ratio, hepatic glutathione peroxidase and catalase activities, and serum levels of interleukin-2. Both probiotic and antibiotic treatments modulated the piglets’ gut microbiomes, with more L. plantarum in the LAB group and more Eubacterium rectale and Limosilactobacillus reuteri in the A group. Probiotic supplementation significantly increased the relative abundance of genes encoding the acetylene, galactose, and stachyose degradation pathways, potentially enhancing nutrient absorption, energy acquisition, and growth performance. Probiotics are effective alternatives to antibiotics for promoting the health of piglets, possibly via gut microbiome modulation.IMPORTANCEWeaning impacts piglet health, performance, and mortality. Antibiotic treatment during weaning can mitigate the negative effects on growth. However, antibiotic use in livestock production contributes to the emergence of antibiotic resistance, which is a threat to global public health. This comprehensive study describes the gut microbial composition and growth performance of weaned piglets after dietary supplementation with Lactiplantibacillus plantarum P-8 or antibiotics. L. plantarum P-8 ameliorated stress and improved antioxidant capacity and growth performance in weaned piglets, accompanied by gut microbiota improvement. L. plantarum P-8 is an effective substitute for antibiotics to promote the health of weaned piglets while avoiding the global concern of drug resistance.
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spelling doaj.art-77e3e47263eb4e02ba830f5aad5d8c372024-02-06T14:04:55ZengAmerican Society for MicrobiologyMicrobiology Spectrum2165-04972024-02-0112210.1128/spectrum.02345-22Dietary supplementation with Lactiplantibacillus plantarum P-8 improves the growth performance and gut microbiota of weaned pigletsJie Yu0Bin Zuo1Qi Li2Feiyan Zhao3Junjun Wang4Weiqiang Huang5Zhihong Sun6Yongfu Chen7Key Laboratory of Dairy Biotechnology and Engineering, Ministry of Education, Inner Mongolia Agricultural University, Huhhot, ChinaState Key Laboratory of Animal Nutrition, College of Animal Science and Technology, China Agricultural University, Beijing, ChinaKey Laboratory of Dairy Biotechnology and Engineering, Ministry of Education, Inner Mongolia Agricultural University, Huhhot, ChinaKey Laboratory of Dairy Biotechnology and Engineering, Ministry of Education, Inner Mongolia Agricultural University, Huhhot, ChinaState Key Laboratory of Animal Nutrition, College of Animal Science and Technology, China Agricultural University, Beijing, ChinaKey Laboratory of Dairy Biotechnology and Engineering, Ministry of Education, Inner Mongolia Agricultural University, Huhhot, ChinaKey Laboratory of Dairy Biotechnology and Engineering, Ministry of Education, Inner Mongolia Agricultural University, Huhhot, ChinaKey Laboratory of Dairy Biotechnology and Engineering, Ministry of Education, Inner Mongolia Agricultural University, Huhhot, ChinaABSTRACTWeaning is a stressful event in the pig life cycle. We hypothesized that probiotics could be potential alternatives to antibiotics for promoting growth and ameliorating stress in weaning piglets via gut microbiota modulation and, thus, investigated the beneficial effects of dietary probiotic supplementation in weaning pigs. Ninety weaning piglets (Landrace × large white, 45 males and 45 females, 25 days of age) were randomized into three dietary treatments (30 piglets/treatment, divided into five replicates/treatment, i.e., six piglets/replicate) in this 28-day trial: control (C group, basal diet); probiotic [lactic acid bacteria (LAB) group, basal diet plus Lactiplantibacillus plantarum P-8]; and antibiotic (A group; basal diet plus chlortetracycline). The piglets’ growth performance [average daily gain, average daily feed intake (ADFI), and feed conversion ratio (FCR)], immune and antioxidant markers, ileal mucosal morphology, and ileal and colonic microbiomes were compared among treatment groups. Compared to the C and A groups, probiotic supplementation significantly decreased the ADFI, FCR, and ileal mucosal crypt depth while increasing the villus height-to-crypt depth ratio, hepatic glutathione peroxidase and catalase activities, and serum levels of interleukin-2. Both probiotic and antibiotic treatments modulated the piglets’ gut microbiomes, with more L. plantarum in the LAB group and more Eubacterium rectale and Limosilactobacillus reuteri in the A group. Probiotic supplementation significantly increased the relative abundance of genes encoding the acetylene, galactose, and stachyose degradation pathways, potentially enhancing nutrient absorption, energy acquisition, and growth performance. Probiotics are effective alternatives to antibiotics for promoting the health of piglets, possibly via gut microbiome modulation.IMPORTANCEWeaning impacts piglet health, performance, and mortality. Antibiotic treatment during weaning can mitigate the negative effects on growth. However, antibiotic use in livestock production contributes to the emergence of antibiotic resistance, which is a threat to global public health. This comprehensive study describes the gut microbial composition and growth performance of weaned piglets after dietary supplementation with Lactiplantibacillus plantarum P-8 or antibiotics. L. plantarum P-8 ameliorated stress and improved antioxidant capacity and growth performance in weaned piglets, accompanied by gut microbiota improvement. L. plantarum P-8 is an effective substitute for antibiotics to promote the health of weaned piglets while avoiding the global concern of drug resistance.https://journals.asm.org/doi/10.1128/spectrum.02345-22weaned pigletsmicrobiotaLactiplantibacillus plantarumgrowth performanceantibiotic resistance genes
spellingShingle Jie Yu
Bin Zuo
Qi Li
Feiyan Zhao
Junjun Wang
Weiqiang Huang
Zhihong Sun
Yongfu Chen
Dietary supplementation with Lactiplantibacillus plantarum P-8 improves the growth performance and gut microbiota of weaned piglets
Microbiology Spectrum
weaned piglets
microbiota
Lactiplantibacillus plantarum
growth performance
antibiotic resistance genes
title Dietary supplementation with Lactiplantibacillus plantarum P-8 improves the growth performance and gut microbiota of weaned piglets
title_full Dietary supplementation with Lactiplantibacillus plantarum P-8 improves the growth performance and gut microbiota of weaned piglets
title_fullStr Dietary supplementation with Lactiplantibacillus plantarum P-8 improves the growth performance and gut microbiota of weaned piglets
title_full_unstemmed Dietary supplementation with Lactiplantibacillus plantarum P-8 improves the growth performance and gut microbiota of weaned piglets
title_short Dietary supplementation with Lactiplantibacillus plantarum P-8 improves the growth performance and gut microbiota of weaned piglets
title_sort dietary supplementation with lactiplantibacillus plantarum p 8 improves the growth performance and gut microbiota of weaned piglets
topic weaned piglets
microbiota
Lactiplantibacillus plantarum
growth performance
antibiotic resistance genes
url https://journals.asm.org/doi/10.1128/spectrum.02345-22
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