Magnetic chitin beads (MCB) coated with Vibrio cholerae reveals transcriptome dynamics in adult mice with a complex gut microbiota

ABSTRACT

Vibrio cholerae adapts to the host environment by altering gene expression. Because of the complexity of the gut microbiome, current in vivo V. cholerae transcriptome studies have focused on microbiota-undeveloped conditions, neglecting the interaction between the host’s commensal gut microbiota and V. cholerae. In this study, we analyzed the transcriptome of fully colonized adult mice in vivo using V. cholerae coated-magnetic chitin beads (vcMCB). This provides a simple yet powerful method for obtaining high-quality RNA from V. cholerae during colonization in mice. The transcriptome of V. cholerae recovered from adult mice infected with vcMCB shows differential expression of several genes when compared to V. cholerae recovered from the infant mouse and infant rabbit model. Some of these genes were also observed to be differentially expressed in previous studies of V. cholerae recovered from human infection when compared to V. cholerae grown in vitro. In particular, we confirmed that V. cholerae resists the inhibitory effects of low pH and formic acid from gut microbiota, such as Anaerostipes caccae and Dorea formicigenerans, by downregulating vc1080. We propose that the vc1080 product may protect V. cholerae from formic acid stress through a novel acid tolerance response mechanism. Transcriptomic data obtained using the vcMCB system provide new perspectives on the interaction between V. cholerae and the gut microbiota, and this approach can also be applied to studies of other pathogenic bacteria.

GRAPHICAL ABSTRACT

KEYWORDS:

• In-situtranscriptome
• V. cholerae
• gut microbiota
• formic acid
• Anaerostipes caccae
• Dorea formicigenerans

Acknowledgments

This work was supported by the National Key R&D Program of China (2019YFA0905600) and National Natural Science Foundation of China (31770132 and 81873969). We are grateful to the mice for their contribution to this study. We thank the cell line support of Dr Chen-Hui Wang from Huazhong University of Science and Technology. We thank Dr. Fan Jin for plasmid support from the Shenzhen Institutes of Advanced Technology, Chinese Academy of Sciences. We thank the Research Core Facilities for Life Science (RCFLS) at Huazhong University of Science and Technology for their assistance with confocal microscopy.

Disclosure statement

No potential conflict of interest was reported by the author(s).

Contributions

ZXQ, JH and ZL designed and completed the study. ZXQ and XMY conducted bioinformatics analysis. ZXQ, WB, GZC, YM, XMY, CRY, and ML performed experiments. ZXQ, GZC, YM, XMY, and ML helped with the sample collection. ZXQ drew charts and wrote the manuscript. ZL supervised the project. All the authors approved the final version of the manuscript.

Data availability statement

All data relevant to the study are included in the article or uploaded as supplementary information. The datasets presented in this study can be found in the online repositories. The names of the repository/repositories and accession numbers (s) are PRJNA980451 and PRJNA980554 in the SRA database.

Provenance and peer review

Not commissioned; externally peer reviewed.

Supplementary material

Supplemental data for this article can be accessed online at https://doi.org/10.1080/19490976.2023.2274125

Correction Statement

This article has been corrected with minor changes. These changes do not impact the academic content of the article.

Additional information

Funding

The work was supported by the National Key Research and Development Program of China [2019YFA0905600]; National Natural Science Foundation of China [31770132 and 81873969].