Adaptation of Gut Microbiome to Transgenic Pigs Secreting β-Glucanase, Xylanase, and Phytase

We previously generated transgenic pigs with enhanced growth rate and reduced nutrient loss. However, the composition of their gut microbiome is unknown. In this study, we successfully generated EGFP marker-free transgenic (MF-TG) pigs with high expression levels of microbial β-glucanase, xylanase,...

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Main Authors: Jianxin Mo, Guoling Li, Guangyan Huang, Haoqiang Wang, Junsong Shi, Rong Zhou, Gengyuan Cai, Zhenfang Wu, Xianwei Zhang
Format: Article
Language:English
Published: Frontiers Media S.A. 2021-03-01
Series:Frontiers in Genetics
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fgene.2021.631071/full
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spelling doaj-bf8f288e3ac84161ba47f3d05487daab2021-03-04T17:08:00ZengFrontiers Media S.A.Frontiers in Genetics1664-80212021-03-011210.3389/fgene.2021.631071631071Adaptation of Gut Microbiome to Transgenic Pigs Secreting β-Glucanase, Xylanase, and PhytaseJianxin Mo0Guoling Li1Guangyan Huang2Haoqiang Wang3Junsong Shi4Rong Zhou5Gengyuan Cai6Gengyuan Cai7Zhenfang Wu8Zhenfang Wu9Xianwei Zhang10National Engineering Research Center for Breeding Swine Industry, Wens Foodstuff Group Co., Ltd., Yunfu, ChinaCollege of Animal Science, South China Agricultural University, Guangzhou, ChinaCollege of Animal Science, South China Agricultural University, Guangzhou, ChinaNational Engineering Research Center for Breeding Swine Industry, Wens Foodstuff Group Co., Ltd., Yunfu, ChinaNational Engineering Research Center for Breeding Swine Industry, Wens Foodstuff Group Co., Ltd., Yunfu, ChinaNational Engineering Research Center for Breeding Swine Industry, Wens Foodstuff Group Co., Ltd., Yunfu, ChinaNational Engineering Research Center for Breeding Swine Industry, Wens Foodstuff Group Co., Ltd., Yunfu, ChinaCollege of Animal Science, South China Agricultural University, Guangzhou, ChinaNational Engineering Research Center for Breeding Swine Industry, Wens Foodstuff Group Co., Ltd., Yunfu, ChinaCollege of Animal Science, South China Agricultural University, Guangzhou, ChinaNational Engineering Research Center for Breeding Swine Industry, Wens Foodstuff Group Co., Ltd., Yunfu, ChinaWe previously generated transgenic pigs with enhanced growth rate and reduced nutrient loss. However, the composition of their gut microbiome is unknown. In this study, we successfully generated EGFP marker-free transgenic (MF-TG) pigs with high expression levels of microbial β-glucanase, xylanase, and phytase in the parotid gland. We collected intestinal contents from the ileum, cecum and colon of five MF-TG and five wild-type (WT) sows and investigated the gut microbiome of the transgenic pigs via metagenomic analysis. Results showed that the levels of probiotics, such as Lactobacillus reuteri and Streptococcus, were more abundant in the cecum of the MF-TG pigs and higher than those of WT pigs. By contrast, the levels of harmful microorganisms, such as Campylobacter, Chlamydia trachomatis, and Campylobacter fetus, and various unidentified viruses, were higher in the cecum of the WT pigs than those of the MF-TG pigs. By comparing unigenes and the eggNOG database, we found that the microorganisms in the colon of the MF-TG pigs had high fractional abundance in DNA (cytosine-5)-methyltransferase 1 and serine-type D-Ala-D-Ala carboxypeptidase, whereas the aspartate carbamoyltransferase regulatory subunit and outer membrane protein pathways were enriched in the WT pigs. Moreover, the microorganisms in the cecum of the MF-TG pigs were active in GlycosylTransferase Family 8 (GT8), Glycoside Hydrolase Family 13 (GH13), and Glycoside Hydrolase Family 32 (GH32). Furthermore, the levels of numerous carbohydrases, such as glucan 1,3-beta-glucosidase, xylan 1,4-beta-xylosidase and exo-1,3-1,4-glucanase, were higher in the cecum of the MF-TG pigs than those of the WT pigs. The results indicated that intestinal microbes can change adaptively to the secretion of transgenic enzymes, thereby forming a benign cooperation with their host. This cooperation could be beneficial for improving feed efficiency.https://www.frontiersin.org/articles/10.3389/fgene.2021.631071/fulltransgenic pigsmicrobial enzymesgut microbiomemetagenomicsfeed efficiency
collection DOAJ
language English
format Article
sources DOAJ
author Jianxin Mo
Guoling Li
Guangyan Huang
Haoqiang Wang
Junsong Shi
Rong Zhou
Gengyuan Cai
Gengyuan Cai
Zhenfang Wu
Zhenfang Wu
Xianwei Zhang
spellingShingle Jianxin Mo
Guoling Li
Guangyan Huang
Haoqiang Wang
Junsong Shi
Rong Zhou
Gengyuan Cai
Gengyuan Cai
Zhenfang Wu
Zhenfang Wu
Xianwei Zhang
Adaptation of Gut Microbiome to Transgenic Pigs Secreting β-Glucanase, Xylanase, and Phytase
Frontiers in Genetics
transgenic pigs
microbial enzymes
gut microbiome
metagenomics
feed efficiency
author_facet Jianxin Mo
Guoling Li
Guangyan Huang
Haoqiang Wang
Junsong Shi
Rong Zhou
Gengyuan Cai
Gengyuan Cai
Zhenfang Wu
Zhenfang Wu
Xianwei Zhang
author_sort Jianxin Mo
title Adaptation of Gut Microbiome to Transgenic Pigs Secreting β-Glucanase, Xylanase, and Phytase
title_short Adaptation of Gut Microbiome to Transgenic Pigs Secreting β-Glucanase, Xylanase, and Phytase
title_full Adaptation of Gut Microbiome to Transgenic Pigs Secreting β-Glucanase, Xylanase, and Phytase
title_fullStr Adaptation of Gut Microbiome to Transgenic Pigs Secreting β-Glucanase, Xylanase, and Phytase
title_full_unstemmed Adaptation of Gut Microbiome to Transgenic Pigs Secreting β-Glucanase, Xylanase, and Phytase
title_sort adaptation of gut microbiome to transgenic pigs secreting β-glucanase, xylanase, and phytase
publisher Frontiers Media S.A.
series Frontiers in Genetics
issn 1664-8021
publishDate 2021-03-01
description We previously generated transgenic pigs with enhanced growth rate and reduced nutrient loss. However, the composition of their gut microbiome is unknown. In this study, we successfully generated EGFP marker-free transgenic (MF-TG) pigs with high expression levels of microbial β-glucanase, xylanase, and phytase in the parotid gland. We collected intestinal contents from the ileum, cecum and colon of five MF-TG and five wild-type (WT) sows and investigated the gut microbiome of the transgenic pigs via metagenomic analysis. Results showed that the levels of probiotics, such as Lactobacillus reuteri and Streptococcus, were more abundant in the cecum of the MF-TG pigs and higher than those of WT pigs. By contrast, the levels of harmful microorganisms, such as Campylobacter, Chlamydia trachomatis, and Campylobacter fetus, and various unidentified viruses, were higher in the cecum of the WT pigs than those of the MF-TG pigs. By comparing unigenes and the eggNOG database, we found that the microorganisms in the colon of the MF-TG pigs had high fractional abundance in DNA (cytosine-5)-methyltransferase 1 and serine-type D-Ala-D-Ala carboxypeptidase, whereas the aspartate carbamoyltransferase regulatory subunit and outer membrane protein pathways were enriched in the WT pigs. Moreover, the microorganisms in the cecum of the MF-TG pigs were active in GlycosylTransferase Family 8 (GT8), Glycoside Hydrolase Family 13 (GH13), and Glycoside Hydrolase Family 32 (GH32). Furthermore, the levels of numerous carbohydrases, such as glucan 1,3-beta-glucosidase, xylan 1,4-beta-xylosidase and exo-1,3-1,4-glucanase, were higher in the cecum of the MF-TG pigs than those of the WT pigs. The results indicated that intestinal microbes can change adaptively to the secretion of transgenic enzymes, thereby forming a benign cooperation with their host. This cooperation could be beneficial for improving feed efficiency.
topic transgenic pigs
microbial enzymes
gut microbiome
metagenomics
feed efficiency
url https://www.frontiersin.org/articles/10.3389/fgene.2021.631071/full
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