Hybridization altered the gut microbiota of pigs

Mammalian gut microbiota plays an important role in the host’s nutrient metabolism, growth, and immune regulation. Hybridization can enable a progeny to acquire superior traits of the parents, resulting in the hybridization advantage. However, studies on the effects of hybridization on the pigs’ gut...

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Main Authors: Limin Wei, Bo Zeng, Siyuan Zhang, Wei Guo, Feng Li, Jiangchao Zhao, Ying Li
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-07-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2023.1177947/full
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author Limin Wei
Limin Wei
Limin Wei
Bo Zeng
Siyuan Zhang
Wei Guo
Feng Li
Jiangchao Zhao
Ying Li
author_facet Limin Wei
Limin Wei
Limin Wei
Bo Zeng
Siyuan Zhang
Wei Guo
Feng Li
Jiangchao Zhao
Ying Li
author_sort Limin Wei
collection DOAJ
description Mammalian gut microbiota plays an important role in the host’s nutrient metabolism, growth, and immune regulation. Hybridization can enable a progeny to acquire superior traits of the parents, resulting in the hybridization advantage. However, studies on the effects of hybridization on the pigs’ gut microbiota are lacking. Therefore, this study used multi-omics technologies to compare and analyze the gut microbiota of the primary wild boar and its offspring. The 16S rRNA gene sequencing results revealed that the gut microbiota of F4 exhibited a host-like dominance phenomenon with a significant increase in the abundance of Lactobacillus and Bifidobacterium. The beta diversity of Duroc was significantly different from those of F0, F2, and F4; after the host hybridization, the similarity of the beta diversity in the progeny decreased with the decrease in the similarity of the F0 lineage. The metagenomic sequencing results showed that the significantly enriched metabolic pathways in F4, such as environmental, circulatory system, fatty acid degradation adaptation, and fatty acid biosynthesis, were similar to those in F0. Moreover, it also exhibited similar significantly enriched metabolic pathways as those in Duroc, such as carbohydrate metabolism, starch and sucrose metabolism, starch-degrading CAZymes, lactose-degrading CAZymes, and various amino acid metabolism pathways. However, the alpha-amylase-related KOs, lipid metabolism, and galactose metabolism in F4 were significantly higher than those in Duroc and F0. Non-targeted metabolome technology analysis found that several metabolites, such as docosahexaenoic acid, arachidonic acid, and citric acid were significantly enriched in the F4 pigs as compared to those in F0. Based on Spearman correlation analysis, Lactobacillus and Bifidobacterium were significantly positively correlated with these metabolites. Finally, the combined metagenomic and metabolomic analysis suggested that the metabolic pathways, such as valine, leucine, and isoleucine biosynthesis and alanine aspartate and glutamate metabolism were significantly enriched in F4 pigs. In conclusion, the gut microbiota of F4 showed a similar host “dominance” phenomenon, which provided reference data for the genetics and evolution of microbiota and the theory of microbial-assisted breeding.
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spelling doaj.art-3b603cee4a7648b1ab109a92401f4fc32023-07-03T05:21:51ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2023-07-011410.3389/fmicb.2023.11779471177947Hybridization altered the gut microbiota of pigsLimin Wei0Limin Wei1Limin Wei2Bo Zeng3Siyuan Zhang4Wei Guo5Feng Li6Jiangchao Zhao7Ying Li8Chongqing Key Laboratory of High Active Traditional Chinese Drug Delivery System, Chongqing Medical and Pharmaceutical College, Chongqing, ChinaGuangdong Provincial Key Laboratory of Animal Molecular Design and Precise Breeding, College of Life Science and Engineering, Foshan University, Foshan, ChinaCollege of Pharmacy, Chongqing Medical University, Chongqing, ChinaFarm Animal Genetic Resources Exploration and Innovation Key Laboratory of Sichuan Province, Sichuan Agricultural University, Chengdu, ChinaSchool of Laboratory Medicine/Sichuan Provincial Engineering Laboratory for Prevention and Control Technology of Veterinary Drug Residue in Animal-Origin Food, Chengdu Medical College, Chengdu, ChinaSchool of Laboratory Medicine/Sichuan Provincial Engineering Laboratory for Prevention and Control Technology of Veterinary Drug Residue in Animal-Origin Food, Chengdu Medical College, Chengdu, ChinaKey Laboratory of Southwest China Wildlife Resources Conservation (Ministry of Education), China West Normal University, Nanchong, ChinaDivision of Agriculture, Department of Animal Science, University of Arkansas, Fayetteville, AR, United StatesGuangdong Provincial Key Laboratory of Animal Molecular Design and Precise Breeding, College of Life Science and Engineering, Foshan University, Foshan, ChinaMammalian gut microbiota plays an important role in the host’s nutrient metabolism, growth, and immune regulation. Hybridization can enable a progeny to acquire superior traits of the parents, resulting in the hybridization advantage. However, studies on the effects of hybridization on the pigs’ gut microbiota are lacking. Therefore, this study used multi-omics technologies to compare and analyze the gut microbiota of the primary wild boar and its offspring. The 16S rRNA gene sequencing results revealed that the gut microbiota of F4 exhibited a host-like dominance phenomenon with a significant increase in the abundance of Lactobacillus and Bifidobacterium. The beta diversity of Duroc was significantly different from those of F0, F2, and F4; after the host hybridization, the similarity of the beta diversity in the progeny decreased with the decrease in the similarity of the F0 lineage. The metagenomic sequencing results showed that the significantly enriched metabolic pathways in F4, such as environmental, circulatory system, fatty acid degradation adaptation, and fatty acid biosynthesis, were similar to those in F0. Moreover, it also exhibited similar significantly enriched metabolic pathways as those in Duroc, such as carbohydrate metabolism, starch and sucrose metabolism, starch-degrading CAZymes, lactose-degrading CAZymes, and various amino acid metabolism pathways. However, the alpha-amylase-related KOs, lipid metabolism, and galactose metabolism in F4 were significantly higher than those in Duroc and F0. Non-targeted metabolome technology analysis found that several metabolites, such as docosahexaenoic acid, arachidonic acid, and citric acid were significantly enriched in the F4 pigs as compared to those in F0. Based on Spearman correlation analysis, Lactobacillus and Bifidobacterium were significantly positively correlated with these metabolites. Finally, the combined metagenomic and metabolomic analysis suggested that the metabolic pathways, such as valine, leucine, and isoleucine biosynthesis and alanine aspartate and glutamate metabolism were significantly enriched in F4 pigs. In conclusion, the gut microbiota of F4 showed a similar host “dominance” phenomenon, which provided reference data for the genetics and evolution of microbiota and the theory of microbial-assisted breeding.https://www.frontiersin.org/articles/10.3389/fmicb.2023.1177947/fullgut microbiotahybridizationpig16S rRNAmetagenomemetabolome
spellingShingle Limin Wei
Limin Wei
Limin Wei
Bo Zeng
Siyuan Zhang
Wei Guo
Feng Li
Jiangchao Zhao
Ying Li
Hybridization altered the gut microbiota of pigs
Frontiers in Microbiology
gut microbiota
hybridization
pig
16S rRNA
metagenome
metabolome
title Hybridization altered the gut microbiota of pigs
title_full Hybridization altered the gut microbiota of pigs
title_fullStr Hybridization altered the gut microbiota of pigs
title_full_unstemmed Hybridization altered the gut microbiota of pigs
title_short Hybridization altered the gut microbiota of pigs
title_sort hybridization altered the gut microbiota of pigs
topic gut microbiota
hybridization
pig
16S rRNA
metagenome
metabolome
url https://www.frontiersin.org/articles/10.3389/fmicb.2023.1177947/full
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