The natural symbiotic bacterium Enterococcus faecalis LX10 drives Bombyx mori refractoriness to Nosema bombycis infection via the secretion of enterococcin

Abstract Background The microsporidian Nosema bombycis is an obligate intracellular fungal-related parasites of the Bombyx mori, causing the epidemic disease Pebrine and extensive economic losses in the agricultural and sericulture industry. Enterococcus has emerged as one of the predominant gut mic...

Full description

Saved in:
Bibliographic Details
Main Authors: Xiancui Zhang, Liang Yang, Tong Cai, Haoran Liao, Peiwen Cai, Xinkuang Zhao, Nengjie Gu, Zihan Yue, Yanzhou Gu, Fan Zhang, Choufei Wu, Xingmeng Lu
Format: Article
Language:English
Published: BMC 2025-05-01
Series:BMC Microbiology
Subjects:
Online Access:https://doi.org/10.1186/s12866-025-03980-y
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1850132898679619584
author Xiancui Zhang
Liang Yang
Tong Cai
Haoran Liao
Peiwen Cai
Xinkuang Zhao
Nengjie Gu
Zihan Yue
Yanzhou Gu
Fan Zhang
Choufei Wu
Xingmeng Lu
author_facet Xiancui Zhang
Liang Yang
Tong Cai
Haoran Liao
Peiwen Cai
Xinkuang Zhao
Nengjie Gu
Zihan Yue
Yanzhou Gu
Fan Zhang
Choufei Wu
Xingmeng Lu
author_sort Xiancui Zhang
collection DOAJ
description Abstract Background The microsporidian Nosema bombycis is an obligate intracellular fungal-related parasites of the Bombyx mori, causing the epidemic disease Pebrine and extensive economic losses in the agricultural and sericulture industry. Enterococcus has emerged as one of the predominant gut microorganisms of the major model organism, Bombyx mori. However, the potential interactions mechanism between B. mori, N. bombycis and Enterococcus have not been well demonstrated. Methods To address this gap, we used an insect model, silkworm to examine the potential mechanism of the natural symbiotic bacterium Enterococcus faecalis LX10 drives B. mori refractoriness to N. bombycis infection. E. faecalis LX10 was isolated from the gut of healthy silkworms, and its inhibitory activity against N. bombycis was evaluated at both the cellular and individual levels using posttranslational modifications, gene and protein expression analysis, transfected cells, and in vitro immunofluorescence. Results We demonstrated that enterococcin (EntLX), the first antimicrobial protein family in gut commensal bacterium Enterococcus faecalis LX10 of B. mori, contributes to defending against N. bombycis infection resistance depends on the enzyme gelatinase (GelE), disulfide bond and disulfide bond formation proteinA (DsbA). The EntLX protein, abundantly expressed in transgenic BmN cells and gut organs(gut epithelium, peritrophic membrane and contents), can reduce the infection rate of cells and alleviate intestinal damage caused by N. bombycis infection. After simultaneous vaccination with E. faecalis LX10 and N. bombycis, the differentially key metabolites, physiological characteristics(larval mass), or economic traits(cocoon length, cocoon width, whole-cocoon weight, cocoon shell weight, pupation rate and adult emergence rate) showed a certain degrees of recovery and correction compared with those of single N. bombycis inoculation at the individual level. Conclusions This study advances the understanding of the anti-microsporidia activity of enterococci and paves the way for the expression of these molecules as antifungal agents via the genetic transformation of Enterococcus symbionts from disease-transmitting insects. Clinical trial number Not applicable.
format Article
id doaj-art-227d40e58d9b4e9ea17fc902af8cf7bb
institution OA Journals
issn 1471-2180
language English
publishDate 2025-05-01
publisher BMC
record_format Article
series BMC Microbiology
spelling doaj-art-227d40e58d9b4e9ea17fc902af8cf7bb2025-08-20T02:32:07ZengBMCBMC Microbiology1471-21802025-05-0125111610.1186/s12866-025-03980-yThe natural symbiotic bacterium Enterococcus faecalis LX10 drives Bombyx mori refractoriness to Nosema bombycis infection via the secretion of enterococcinXiancui Zhang0Liang Yang1Tong Cai2Haoran Liao3Peiwen Cai4Xinkuang Zhao5Nengjie Gu6Zihan Yue7Yanzhou Gu8Fan Zhang9Choufei Wu10Xingmeng Lu11School of Life Science, Huzhou UniversityInstitute of Sericulture, Huzhou Academy of Agricultural SciencesShandong Center for Disease Control and PreventionSchool of Life Science, Huzhou UniversitySchool of Life Science, Huzhou UniversitySchool of Life Science, Huzhou UniversitySchool of Life Science, Huzhou UniversitySchool of Life Science, Huzhou UniversitySchool of Life Science, Huzhou UniversityCollege of Life Science, Shandong Normal UniversitySchool of Life Science, Huzhou UniversityLaboratory of Invertebrate Pathology, College of Animal Sciences, Zhejiang UniversityAbstract Background The microsporidian Nosema bombycis is an obligate intracellular fungal-related parasites of the Bombyx mori, causing the epidemic disease Pebrine and extensive economic losses in the agricultural and sericulture industry. Enterococcus has emerged as one of the predominant gut microorganisms of the major model organism, Bombyx mori. However, the potential interactions mechanism between B. mori, N. bombycis and Enterococcus have not been well demonstrated. Methods To address this gap, we used an insect model, silkworm to examine the potential mechanism of the natural symbiotic bacterium Enterococcus faecalis LX10 drives B. mori refractoriness to N. bombycis infection. E. faecalis LX10 was isolated from the gut of healthy silkworms, and its inhibitory activity against N. bombycis was evaluated at both the cellular and individual levels using posttranslational modifications, gene and protein expression analysis, transfected cells, and in vitro immunofluorescence. Results We demonstrated that enterococcin (EntLX), the first antimicrobial protein family in gut commensal bacterium Enterococcus faecalis LX10 of B. mori, contributes to defending against N. bombycis infection resistance depends on the enzyme gelatinase (GelE), disulfide bond and disulfide bond formation proteinA (DsbA). The EntLX protein, abundantly expressed in transgenic BmN cells and gut organs(gut epithelium, peritrophic membrane and contents), can reduce the infection rate of cells and alleviate intestinal damage caused by N. bombycis infection. After simultaneous vaccination with E. faecalis LX10 and N. bombycis, the differentially key metabolites, physiological characteristics(larval mass), or economic traits(cocoon length, cocoon width, whole-cocoon weight, cocoon shell weight, pupation rate and adult emergence rate) showed a certain degrees of recovery and correction compared with those of single N. bombycis inoculation at the individual level. Conclusions This study advances the understanding of the anti-microsporidia activity of enterococci and paves the way for the expression of these molecules as antifungal agents via the genetic transformation of Enterococcus symbionts from disease-transmitting insects. Clinical trial number Not applicable.https://doi.org/10.1186/s12866-025-03980-yBombyx moriNosema bombycisEnterococcus faecalisEnterococcinSymbionts
spellingShingle Xiancui Zhang
Liang Yang
Tong Cai
Haoran Liao
Peiwen Cai
Xinkuang Zhao
Nengjie Gu
Zihan Yue
Yanzhou Gu
Fan Zhang
Choufei Wu
Xingmeng Lu
The natural symbiotic bacterium Enterococcus faecalis LX10 drives Bombyx mori refractoriness to Nosema bombycis infection via the secretion of enterococcin
BMC Microbiology
Bombyx mori
Nosema bombycis
Enterococcus faecalis
Enterococcin
Symbionts
title The natural symbiotic bacterium Enterococcus faecalis LX10 drives Bombyx mori refractoriness to Nosema bombycis infection via the secretion of enterococcin
title_full The natural symbiotic bacterium Enterococcus faecalis LX10 drives Bombyx mori refractoriness to Nosema bombycis infection via the secretion of enterococcin
title_fullStr The natural symbiotic bacterium Enterococcus faecalis LX10 drives Bombyx mori refractoriness to Nosema bombycis infection via the secretion of enterococcin
title_full_unstemmed The natural symbiotic bacterium Enterococcus faecalis LX10 drives Bombyx mori refractoriness to Nosema bombycis infection via the secretion of enterococcin
title_short The natural symbiotic bacterium Enterococcus faecalis LX10 drives Bombyx mori refractoriness to Nosema bombycis infection via the secretion of enterococcin
title_sort natural symbiotic bacterium enterococcus faecalis lx10 drives bombyx mori refractoriness to nosema bombycis infection via the secretion of enterococcin
topic Bombyx mori
Nosema bombycis
Enterococcus faecalis
Enterococcin
Symbionts
url https://doi.org/10.1186/s12866-025-03980-y
work_keys_str_mv AT xiancuizhang thenaturalsymbioticbacteriumenterococcusfaecalislx10drivesbombyxmorirefractorinesstonosemabombycisinfectionviathesecretionofenterococcin
AT liangyang thenaturalsymbioticbacteriumenterococcusfaecalislx10drivesbombyxmorirefractorinesstonosemabombycisinfectionviathesecretionofenterococcin
AT tongcai thenaturalsymbioticbacteriumenterococcusfaecalislx10drivesbombyxmorirefractorinesstonosemabombycisinfectionviathesecretionofenterococcin
AT haoranliao thenaturalsymbioticbacteriumenterococcusfaecalislx10drivesbombyxmorirefractorinesstonosemabombycisinfectionviathesecretionofenterococcin
AT peiwencai thenaturalsymbioticbacteriumenterococcusfaecalislx10drivesbombyxmorirefractorinesstonosemabombycisinfectionviathesecretionofenterococcin
AT xinkuangzhao thenaturalsymbioticbacteriumenterococcusfaecalislx10drivesbombyxmorirefractorinesstonosemabombycisinfectionviathesecretionofenterococcin
AT nengjiegu thenaturalsymbioticbacteriumenterococcusfaecalislx10drivesbombyxmorirefractorinesstonosemabombycisinfectionviathesecretionofenterococcin
AT zihanyue thenaturalsymbioticbacteriumenterococcusfaecalislx10drivesbombyxmorirefractorinesstonosemabombycisinfectionviathesecretionofenterococcin
AT yanzhougu thenaturalsymbioticbacteriumenterococcusfaecalislx10drivesbombyxmorirefractorinesstonosemabombycisinfectionviathesecretionofenterococcin
AT fanzhang thenaturalsymbioticbacteriumenterococcusfaecalislx10drivesbombyxmorirefractorinesstonosemabombycisinfectionviathesecretionofenterococcin
AT choufeiwu thenaturalsymbioticbacteriumenterococcusfaecalislx10drivesbombyxmorirefractorinesstonosemabombycisinfectionviathesecretionofenterococcin
AT xingmenglu thenaturalsymbioticbacteriumenterococcusfaecalislx10drivesbombyxmorirefractorinesstonosemabombycisinfectionviathesecretionofenterococcin
AT xiancuizhang naturalsymbioticbacteriumenterococcusfaecalislx10drivesbombyxmorirefractorinesstonosemabombycisinfectionviathesecretionofenterococcin
AT liangyang naturalsymbioticbacteriumenterococcusfaecalislx10drivesbombyxmorirefractorinesstonosemabombycisinfectionviathesecretionofenterococcin
AT tongcai naturalsymbioticbacteriumenterococcusfaecalislx10drivesbombyxmorirefractorinesstonosemabombycisinfectionviathesecretionofenterococcin
AT haoranliao naturalsymbioticbacteriumenterococcusfaecalislx10drivesbombyxmorirefractorinesstonosemabombycisinfectionviathesecretionofenterococcin
AT peiwencai naturalsymbioticbacteriumenterococcusfaecalislx10drivesbombyxmorirefractorinesstonosemabombycisinfectionviathesecretionofenterococcin
AT xinkuangzhao naturalsymbioticbacteriumenterococcusfaecalislx10drivesbombyxmorirefractorinesstonosemabombycisinfectionviathesecretionofenterococcin
AT nengjiegu naturalsymbioticbacteriumenterococcusfaecalislx10drivesbombyxmorirefractorinesstonosemabombycisinfectionviathesecretionofenterococcin
AT zihanyue naturalsymbioticbacteriumenterococcusfaecalislx10drivesbombyxmorirefractorinesstonosemabombycisinfectionviathesecretionofenterococcin
AT yanzhougu naturalsymbioticbacteriumenterococcusfaecalislx10drivesbombyxmorirefractorinesstonosemabombycisinfectionviathesecretionofenterococcin
AT fanzhang naturalsymbioticbacteriumenterococcusfaecalislx10drivesbombyxmorirefractorinesstonosemabombycisinfectionviathesecretionofenterococcin
AT choufeiwu naturalsymbioticbacteriumenterococcusfaecalislx10drivesbombyxmorirefractorinesstonosemabombycisinfectionviathesecretionofenterococcin
AT xingmenglu naturalsymbioticbacteriumenterococcusfaecalislx10drivesbombyxmorirefractorinesstonosemabombycisinfectionviathesecretionofenterococcin