Effects of maternal Echinococcus multilocularis infection on colitis susceptibility and gut microbiota of offspring

Abstract Background Maternal immune modulation and alterations in gut microbiota due to intestinal helminth infections may be passed on to offspring. However, it remains unclear whether these effects can be transferred between maternal mice and their offspring during tissue-dwelling helminth infecti...

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Main Authors: Yihui Liu, Yang Xu, Yang Zou, Yingying Ding, Jiayun Zhang, Ying Zhang, Quanhai Pang, Shuai Wang
Format: Article
Language:English
Published: BMC 2025-07-01
Series:Parasites & Vectors
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Online Access:https://doi.org/10.1186/s13071-025-06915-8
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author Yihui Liu
Yang Xu
Yang Zou
Yingying Ding
Jiayun Zhang
Ying Zhang
Quanhai Pang
Shuai Wang
author_facet Yihui Liu
Yang Xu
Yang Zou
Yingying Ding
Jiayun Zhang
Ying Zhang
Quanhai Pang
Shuai Wang
author_sort Yihui Liu
collection DOAJ
description Abstract Background Maternal immune modulation and alterations in gut microbiota due to intestinal helminth infections may be passed on to offspring. However, it remains unclear whether these effects can be transferred between maternal mice and their offspring during tissue-dwelling helminth infections. Methods In this study, we investigated the effect of maternal infection with Echinococcus multilocularis (Emu) on offspring susceptibility to colitis and gut microbiota composition using a dextran sulfate sodium (DSS)-induced colitis model. We performed 16S ribosomal RNA (rRNA) sequencing to analyze the gut microbiota composition and microbial abundance in Emu-infected and control maternal mice, as well as their offspring. Results We found that the maternal mice infected with Emu exhibited significant resistance to colitis, characterized by increased expression of Foxp3 in colonic tissue. Conversely, this resistance phenotype was not observed in the offspring of Emu-infected maternal mice, as they showed no reduction in colitis severity and demonstrated decreased Foxp3 expression. Furthermore, the gut microbiota of Emu-infected maternal mice underwent significant changes, with an increase in genera such as Rikenella, Rikenellaceae RC9 gut group, Turicibacter, Odoribacter, and Parabacteroides, while Lactobacillus, Staphylococcus, and Bifidobacterium decreased postinfection. By contrast, their offspring exhibited a markedly distinct gut microbiota shift, characterized by significant increases in Candidatus Saccharimonas, Desulfovibrio, Helicobacter, and Odoribacter, alongside significant reductions in Muribaculum and Clostridium sensu stricto 1 when compared with the offspring of naive mice. Conclusions These findings suggest that the effects of maternal transmission concerning immune regulation and microbiota alterations in response to helminth infections may depend on species-specific factors. Graphical Abstract
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spelling doaj-art-88c5f94e3e414da19afed0d0b46f9a142025-08-20T04:01:52ZengBMCParasites & Vectors1756-33052025-07-0118111210.1186/s13071-025-06915-8Effects of maternal Echinococcus multilocularis infection on colitis susceptibility and gut microbiota of offspringYihui Liu0Yang Xu1Yang Zou2Yingying Ding3Jiayun Zhang4Ying Zhang5Quanhai Pang6Shuai Wang7College of Veterinary Medicine, Shanxi Agricultural UniversityState Key Laboratory of Animal Disease Control and Prevention, College of Veterinary Medicine, Lanzhou University, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural SciencesState Key Laboratory of Animal Disease Control and Prevention, College of Veterinary Medicine, Lanzhou University, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural SciencesState Key Laboratory of Animal Disease Control and Prevention, College of Veterinary Medicine, Lanzhou University, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural SciencesState Key Laboratory of Animal Disease Control and Prevention, College of Veterinary Medicine, Lanzhou University, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural SciencesState Key Laboratory of Animal Disease Control and Prevention, College of Veterinary Medicine, Lanzhou University, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural SciencesCollege of Veterinary Medicine, Shanxi Agricultural UniversityState Key Laboratory of Animal Disease Control and Prevention, College of Veterinary Medicine, Lanzhou University, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural SciencesAbstract Background Maternal immune modulation and alterations in gut microbiota due to intestinal helminth infections may be passed on to offspring. However, it remains unclear whether these effects can be transferred between maternal mice and their offspring during tissue-dwelling helminth infections. Methods In this study, we investigated the effect of maternal infection with Echinococcus multilocularis (Emu) on offspring susceptibility to colitis and gut microbiota composition using a dextran sulfate sodium (DSS)-induced colitis model. We performed 16S ribosomal RNA (rRNA) sequencing to analyze the gut microbiota composition and microbial abundance in Emu-infected and control maternal mice, as well as their offspring. Results We found that the maternal mice infected with Emu exhibited significant resistance to colitis, characterized by increased expression of Foxp3 in colonic tissue. Conversely, this resistance phenotype was not observed in the offspring of Emu-infected maternal mice, as they showed no reduction in colitis severity and demonstrated decreased Foxp3 expression. Furthermore, the gut microbiota of Emu-infected maternal mice underwent significant changes, with an increase in genera such as Rikenella, Rikenellaceae RC9 gut group, Turicibacter, Odoribacter, and Parabacteroides, while Lactobacillus, Staphylococcus, and Bifidobacterium decreased postinfection. By contrast, their offspring exhibited a markedly distinct gut microbiota shift, characterized by significant increases in Candidatus Saccharimonas, Desulfovibrio, Helicobacter, and Odoribacter, alongside significant reductions in Muribaculum and Clostridium sensu stricto 1 when compared with the offspring of naive mice. Conclusions These findings suggest that the effects of maternal transmission concerning immune regulation and microbiota alterations in response to helminth infections may depend on species-specific factors. Graphical Abstracthttps://doi.org/10.1186/s13071-025-06915-8Echinococcus multilocularisColitis modelFoxp3Gut microbiotaMaternal transmission
spellingShingle Yihui Liu
Yang Xu
Yang Zou
Yingying Ding
Jiayun Zhang
Ying Zhang
Quanhai Pang
Shuai Wang
Effects of maternal Echinococcus multilocularis infection on colitis susceptibility and gut microbiota of offspring
Parasites & Vectors
Echinococcus multilocularis
Colitis model
Foxp3
Gut microbiota
Maternal transmission
title Effects of maternal Echinococcus multilocularis infection on colitis susceptibility and gut microbiota of offspring
title_full Effects of maternal Echinococcus multilocularis infection on colitis susceptibility and gut microbiota of offspring
title_fullStr Effects of maternal Echinococcus multilocularis infection on colitis susceptibility and gut microbiota of offspring
title_full_unstemmed Effects of maternal Echinococcus multilocularis infection on colitis susceptibility and gut microbiota of offspring
title_short Effects of maternal Echinococcus multilocularis infection on colitis susceptibility and gut microbiota of offspring
title_sort effects of maternal echinococcus multilocularis infection on colitis susceptibility and gut microbiota of offspring
topic Echinococcus multilocularis
Colitis model
Foxp3
Gut microbiota
Maternal transmission
url https://doi.org/10.1186/s13071-025-06915-8
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