Categorization of the effects of E. coliLF82 and mutants lacking the chuT and shuU genes on survival, the transcriptome, and metabolome in germ‐free honeybee

Author:

Feng Dongping12ORCID,Zhang Hujun3,Li Zhengpeng1,Li Yiyuan12,Yan Jingshuang1,Zhang Yan1,Yang Yunsheng12

Affiliation:

1. Microbiota Division, Department of Gastroenterology and Hepatology The First Medical Center, Chinese PLA General Hospital Beijing China

2. Medical School of Chinese PLA Beijing China

3. Institute of Genetics and Developmental Biology Chinese Academy of Sciences Beijing China

Abstract

The precise etiology of inflammatory bowel diseases (IBDs) remains elusive. The Escherichia coli strain LF82 (LF82) is known to be associated with IBD, and we hypothesized that this association may be related to the chuT and shuU genes. Here we constructed a germ‐free (GF) honeybee model to investigate the effects of LF82 chuT and shuU genes on the honeybee intestine and their mechanisms. The chuT and shuU gene deletion strains LF82∆chuT and LF82∆shuU were generated by CRISPR‐Cas9. These strains, together with nonpathogenic E. coli MG1655 (MG1655) and wildtype LF82, were allowed to colonize the guts of GF honeybees to establish single bacterial colonization models. Intestinal permeability was assessed following the administration of a sterile Brilliant Blue (FCF) solution. Comprehensive transcriptomic and metabolomic analyses of intestinal samples indicated that MG1655 had few disadvantageous effects on honeybees. Conversely, colonization with LF82 and its gene‐deletion mutants provoked pronounced activation of genes associated with innate immune pathways, stimulated defensive responses, and induced expression of genes associated with inflammation, oxidative stress, and glycosaminoglycan degradation. Crucially, the LF82∆chuT and LF82∆shuU strains perturbed host heme and iron regulation, as well as tryptophan metabolism. These findings suggest that the deletion of chuT and shuU genes in E. coli LF82 may alleviate intestinal inflammation by partially modulating tryptophan catabolism. Our study proposes that targeting iron uptake mechanisms could be a potential strategy to mitigate the virulence of IBD‐associated bacteria.

Publisher

Wiley

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