Bacteroides acidifaciens and its derived extracellular vesicles improve DSS-induced colitis

Cihua Zheng; Yuchun Zhong; Jian Xie; Zhuoya Wang; Wenming Zhang; Yiming Pi; Wenjun Zhang; Li Liu; Jun Luo; Wei Xu

doi:10.3389/fmicb.2023.1304232

Bacteroides acidifaciens and its derived extracellular vesicles improve DSS-induced colitis

Front Microbiol. 2023 Nov 30:14:1304232. doi: 10.3389/fmicb.2023.1304232. eCollection 2023.

Authors

Cihua Zheng^#^{1

2

3}, Yuchun Zhong^#¹, Jian Xie^#², Zhuoya Wang², Wenming Zhang¹, Yiming Pi², Wenjun Zhang², Li Liu⁴, Jun Luo^{2

3}, Wei Xu^{1

3}

Affiliations

¹ Department of General Surgery, The Second Affiliated Hospital of Nanchang University, Nanchang, Jiangxi, China.
² Department of Rehabilitation Medicine, The Second Affiliated Hospital of Nanchang University, Nanchang, Jiangxi, China.
³ The Institute of Translational Medicine, The Second Affiliated Hospital of Nanchang University, Nanchang University, Nanchang, Jiangxi, China.
⁴ Graduate School of Jiangxi University of Chinese Medicine, Nanchang, China.

^# Contributed equally.

Abstract

Introduction: "Probiotic therapy" to regulate gut microbiota and intervene in intestinal diseases such as inflammatory bowel disease (IBD) has become a research hotspot. Bacteroides acidifaciens, as a new generation of probiotics, has shown beneficial effects on various diseases.

Methods: In this study, we utilized a mouse colitis model induced by dextran sodium sulfate (DSS) to investigate how B. acidifaciens positively affects IBD. We evaluated the effects ofB. acidifaciens, fecal microbiota transplantation, and bacterial extracellular vesicles (EVs) on DSS-induced colitis in mice. We monitored the phenotype of mouse colitis, detected serum inflammatory factors using ELISA, evaluated intestinal mucosal barrier function using Western blotting and tissue staining, evaluated gut microbiota using 16S rRNA sequencing, and analyzed differences in EVs protein composition derived from B. acidifaciens using proteomics to explore how B. acidifaciens has a positive impact on mouse colitis.

Results: We confirmed that B. acidifaciens has a protective effect on colitis, including alleviating the colitis phenotype, reducing inflammatory response, and improving intestinal barrier function, accompanied by an increase in the relative abundance of B. acidifaciens and Ruminococcus callidus but a decrease in the relative abundance of B. fragilis. Further fecal bacterial transplantation or fecal filtrate transplantation confirmed the protective effect of eosinophil-regulated gut microbiota and metabolites on DSS-induced colitis. Finally, we validated that EVs derived from B. acidifaciens contain rich functional proteins that can contribute to the relief of colitis.

Conclusion: Therefore, B. acidifaciens and its derived EVs can alleviate DSS-induced colitis by reducing mucosal damage to colon tissue, reducing inflammatory response, promoting mucosal barrier repair, restoring gut microbiota diversity, and restoring gut microbiota balance in mice. The results of this study provide a theoretical basis for the preclinical application of the new generation of probiotics.

Keywords: Bacteroides acidifaciens; extracellular vesicles; gut microbiota; inflammatory bowel disease; intestinal mucosal barrier.

Grants and funding

The authors declare financial support was received for the research, authorship, and/or publication of this article. This study was supported by the National Natural Science Foundation of China grant 81860435 (WX), The Second Affiliated Hospital of Nanchang University Funding Program 2022efyA01 (WX), Jiangxi Provincial Department of Science and Technology Project 20224ABC03A02 (JL), and The Second Affiliated Hospital of Nanchang University Funding Program 2022efyB03 (JL).