Metagenomic analysis of the intestinal microbiome reveals the potential mechanism involved in Bacillus amyloliquefaciens in treating schistosomiasis japonica in mice

ABSTRACTSchistosomiasis japonica is one of the neglected tropical diseases characterized by chronic hepatic, intestinal granulomatous inflammation and fibrosis, as well as dysbiosis of intestinal microbiome. Previously, the probiotic Bacillus amyloliquefaciens has been shown to alleviate the patholo...

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Published in:Microbiology Spectrum
Main Authors: Hao Chen, Shuaiqin Huang, Yiming Zhao, Ruizheng Sun, Jingyan Wang, Siqi Yao, Jing Huang, Zheng Yu
Format: Article
Language:English
Published: American Society for Microbiology 2024-04-01
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Online Access:https://journals.asm.org/doi/10.1128/spectrum.03735-23
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author Hao Chen
Shuaiqin Huang
Yiming Zhao
Ruizheng Sun
Jingyan Wang
Siqi Yao
Jing Huang
Zheng Yu
author_facet Hao Chen
Shuaiqin Huang
Yiming Zhao
Ruizheng Sun
Jingyan Wang
Siqi Yao
Jing Huang
Zheng Yu
author_sort Hao Chen
collection DOAJ
container_title Microbiology Spectrum
description ABSTRACTSchistosomiasis japonica is one of the neglected tropical diseases characterized by chronic hepatic, intestinal granulomatous inflammation and fibrosis, as well as dysbiosis of intestinal microbiome. Previously, the probiotic Bacillus amyloliquefaciens has been shown to alleviate the pathological injuries in mice infected with Schistosoma japonicum by improving the disturbance of the intestinal microbiota. However, the underlying mechanisms involved in this process remain unclear. In this study, metagenomics sequencing and functional analysis were employed to investigate the differential changes in taxonomic composition and functional genes of the intestinal microbiome in S. japonicum-infected mice treated with B. amyloliquefaciens. The results revealed that intervention with B. amyloliquefaciens altered the taxonomic composition of the intestinal microbiota at the species level in infected mice and significantly increased the abundance of beneficial bacteria. Moreover, the abundance of predicted genes in the intestinal microbiome was also significantly changed, and the abundance of xfp/xpk and genes translated to urease was significantly restored. Further analysis showed that Limosilactobacillus reuteri was positively correlated with several KEGG Orthology (KO) genes and metabolic reactions, which might play important roles in alleviating the pathological symptoms caused by S. japonicum infection, indicating that it has the potential to function as another effective therapeutic agent for schistosomiasis. These data suggested that treatment of murine schistosomiasis japonica by B. amyloliquefaciens might be induced by alterations in the taxonomic composition and functional gene of the intestinal microbiome in mice. We hope this study will provide adjuvant strategies and methods for the early prevention and treatment of schistosomiasis japonica.IMPORTANCETargeted interventions of probiotics on gut microbiome were used to explore the mechanism of alleviating schistosomiasis japonica. Through metagenomic analysis, there were significant changes in the composition of gut microbiota in mice infected with Schistosoma japonicum and significant increase in the abundance of beneficial bacteria after the intervention of Bacillus amyloliquefaciens. At the same time, the abundance of functional genes was found to change significantly. The abundance of genes related to urease metabolism and xfp/xpk related to D-erythrose 4-phosphate production was significantly restored, highlighting the importance of Limosilactobacillus reuteri in the recovery and abundance of predicted genes of the gut microbiome. These results indicated potential regulatory mechanism between the gene function of gut microbiome and host immune response. Our research lays the foundation for elucidating the regulatory mechanism of probiotic intervention in alleviating schistosomiasis japonica, and provides potential adjuvant treatment strategies for early prevention and treatment of schistosomiasis japonica.
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spelling doaj-art-48d1910317ae44ff8104f10efa6fb0622025-08-19T22:32:04ZengAmerican Society for MicrobiologyMicrobiology Spectrum2165-04972024-04-0112410.1128/spectrum.03735-23Metagenomic analysis of the intestinal microbiome reveals the potential mechanism involved in Bacillus amyloliquefaciens in treating schistosomiasis japonica in miceHao Chen0Shuaiqin Huang1Yiming Zhao2Ruizheng Sun3Jingyan Wang4Siqi Yao5Jing Huang6Zheng Yu7Department of Parasitology, School of Basic Medical Science, Central South University, Changsha, Hunan, ChinaDepartment of Parasitology, School of Basic Medical Science, Central South University, Changsha, Hunan, ChinaHuman Microbiome and Health Group, Department of Microbiology, School of Basic Medical Science, Central South University, Changsha, Hunan, ChinaDepartment of General Surgery, Xiangya Hospital, Central South University, Changsha, Hunan, ChinaHuman Microbiome and Health Group, Department of Microbiology, School of Basic Medical Science, Central South University, Changsha, Hunan, ChinaHuman Microbiome and Health Group, Department of Microbiology, School of Basic Medical Science, Central South University, Changsha, Hunan, ChinaDepartment of Parasitology, School of Basic Medical Science, Central South University, Changsha, Hunan, ChinaHuman Microbiome and Health Group, Department of Microbiology, School of Basic Medical Science, Central South University, Changsha, Hunan, ChinaABSTRACTSchistosomiasis japonica is one of the neglected tropical diseases characterized by chronic hepatic, intestinal granulomatous inflammation and fibrosis, as well as dysbiosis of intestinal microbiome. Previously, the probiotic Bacillus amyloliquefaciens has been shown to alleviate the pathological injuries in mice infected with Schistosoma japonicum by improving the disturbance of the intestinal microbiota. However, the underlying mechanisms involved in this process remain unclear. In this study, metagenomics sequencing and functional analysis were employed to investigate the differential changes in taxonomic composition and functional genes of the intestinal microbiome in S. japonicum-infected mice treated with B. amyloliquefaciens. The results revealed that intervention with B. amyloliquefaciens altered the taxonomic composition of the intestinal microbiota at the species level in infected mice and significantly increased the abundance of beneficial bacteria. Moreover, the abundance of predicted genes in the intestinal microbiome was also significantly changed, and the abundance of xfp/xpk and genes translated to urease was significantly restored. Further analysis showed that Limosilactobacillus reuteri was positively correlated with several KEGG Orthology (KO) genes and metabolic reactions, which might play important roles in alleviating the pathological symptoms caused by S. japonicum infection, indicating that it has the potential to function as another effective therapeutic agent for schistosomiasis. These data suggested that treatment of murine schistosomiasis japonica by B. amyloliquefaciens might be induced by alterations in the taxonomic composition and functional gene of the intestinal microbiome in mice. We hope this study will provide adjuvant strategies and methods for the early prevention and treatment of schistosomiasis japonica.IMPORTANCETargeted interventions of probiotics on gut microbiome were used to explore the mechanism of alleviating schistosomiasis japonica. Through metagenomic analysis, there were significant changes in the composition of gut microbiota in mice infected with Schistosoma japonicum and significant increase in the abundance of beneficial bacteria after the intervention of Bacillus amyloliquefaciens. At the same time, the abundance of functional genes was found to change significantly. The abundance of genes related to urease metabolism and xfp/xpk related to D-erythrose 4-phosphate production was significantly restored, highlighting the importance of Limosilactobacillus reuteri in the recovery and abundance of predicted genes of the gut microbiome. These results indicated potential regulatory mechanism between the gene function of gut microbiome and host immune response. Our research lays the foundation for elucidating the regulatory mechanism of probiotic intervention in alleviating schistosomiasis japonica, and provides potential adjuvant treatment strategies for early prevention and treatment of schistosomiasis japonica.https://journals.asm.org/doi/10.1128/spectrum.03735-23Bacillus amyloliquefaciensSchistosoma japonicumintestinal microbiomefunctional genes
spellingShingle Hao Chen
Shuaiqin Huang
Yiming Zhao
Ruizheng Sun
Jingyan Wang
Siqi Yao
Jing Huang
Zheng Yu
Metagenomic analysis of the intestinal microbiome reveals the potential mechanism involved in Bacillus amyloliquefaciens in treating schistosomiasis japonica in mice
Bacillus amyloliquefaciens
Schistosoma japonicum
intestinal microbiome
functional genes
title Metagenomic analysis of the intestinal microbiome reveals the potential mechanism involved in Bacillus amyloliquefaciens in treating schistosomiasis japonica in mice
title_full Metagenomic analysis of the intestinal microbiome reveals the potential mechanism involved in Bacillus amyloliquefaciens in treating schistosomiasis japonica in mice
title_fullStr Metagenomic analysis of the intestinal microbiome reveals the potential mechanism involved in Bacillus amyloliquefaciens in treating schistosomiasis japonica in mice
title_full_unstemmed Metagenomic analysis of the intestinal microbiome reveals the potential mechanism involved in Bacillus amyloliquefaciens in treating schistosomiasis japonica in mice
title_short Metagenomic analysis of the intestinal microbiome reveals the potential mechanism involved in Bacillus amyloliquefaciens in treating schistosomiasis japonica in mice
title_sort metagenomic analysis of the intestinal microbiome reveals the potential mechanism involved in bacillus amyloliquefaciens in treating schistosomiasis japonica in mice
topic Bacillus amyloliquefaciens
Schistosoma japonicum
intestinal microbiome
functional genes
url https://journals.asm.org/doi/10.1128/spectrum.03735-23
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