Characterization of AI-2/LuxS quorum sensing system in biofilm formation, pathogenesis of Streptococcus equi subsp. zooepidemicus

Streptococcus equi subsp. zooepidemicus (SEZ) is an opportunistic pathogen of both humans and animals. Quorum sensing (QS) plays an important role in the regulation of bacterial group behaviors. The aim of this study was to characterize the LuxS in SEZ and evaluate its impact on biofilm formation, p...

Full description

Bibliographic Details
Main Authors: Honglin Xie, Riteng Zhang, Ruhai Guo, Yining Zhang, Jingya Zhang, Hui Li, Qiang Fu, Xinglong Wang
Format: Article
Language:English
Published: Frontiers Media S.A. 2024-02-01
Series:Frontiers in Cellular and Infection Microbiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fcimb.2024.1339131/full
_version_ 1797323702432432128
author Honglin Xie
Riteng Zhang
Ruhai Guo
Yining Zhang
Jingya Zhang
Hui Li
Qiang Fu
Xinglong Wang
author_facet Honglin Xie
Riteng Zhang
Ruhai Guo
Yining Zhang
Jingya Zhang
Hui Li
Qiang Fu
Xinglong Wang
author_sort Honglin Xie
collection DOAJ
description Streptococcus equi subsp. zooepidemicus (SEZ) is an opportunistic pathogen of both humans and animals. Quorum sensing (QS) plays an important role in the regulation of bacterial group behaviors. The aim of this study was to characterize the LuxS in SEZ and evaluate its impact on biofilm formation, pathogenesis and gene expression. The wild-type SEZ and its LuxS mutant (ΔluxS) were examined for growth, biofilm formation, virulence factors, and transcriptomic profiles. Our results showed that LuxS deficiency did not affect SEZ hemolytic activity, adhesion or capsule production. For biofilm assay demonstrated that mutation in the luxS gene significantly enhances biofilm formation, produced a denser biofilm and attached to a glass surface. RAW264.7 cell infection indicated that ΔluxS promoted macrophage apoptosis and pro-inflammatory responses. In mice infection, there was no significant difference in mortality between SEZ and ΔluxS. However, the bacterial load in the spleen of mice infected with ΔluxS was significantly higher than in those infected with SEZ. And the pathological analysis further indicated that spleen damage was more severe in the ΔluxS group. Moreover, transcriptomics analysis revealed significant alterations in carbon metabolism, RNA binding and stress response genes in ΔluxS. In summary, this study provides the first evidence of AI-2/LuxS QS system in SEZ and reveals its regulatory effects on biofilm formation, pathogenicity and gene expression.
first_indexed 2024-03-08T05:32:20Z
format Article
id doaj.art-bc3c4cd243e547178c11d979bebfa5d9
institution Directory Open Access Journal
issn 2235-2988
language English
last_indexed 2024-03-08T05:32:20Z
publishDate 2024-02-01
publisher Frontiers Media S.A.
record_format Article
series Frontiers in Cellular and Infection Microbiology
spelling doaj.art-bc3c4cd243e547178c11d979bebfa5d92024-02-06T04:37:14ZengFrontiers Media S.A.Frontiers in Cellular and Infection Microbiology2235-29882024-02-011410.3389/fcimb.2024.13391311339131Characterization of AI-2/LuxS quorum sensing system in biofilm formation, pathogenesis of Streptococcus equi subsp. zooepidemicusHonglin Xie0Riteng Zhang1Ruhai Guo2Yining Zhang3Jingya Zhang4Hui Li5Qiang Fu6Xinglong Wang7College of Veterinary Medicine, Northwest A&F University, Yangling, Shaanxi, ChinaCollege of Veterinary Medicine, Northwest A&F University, Yangling, Shaanxi, ChinaCollege of Veterinary Medicine, Northwest A&F University, Yangling, Shaanxi, ChinaCollege of Veterinary Medicine, Northwest A&F University, Yangling, Shaanxi, ChinaCollege of Veterinary Medicine, Northwest A&F University, Yangling, Shaanxi, ChinaCollege of Veterinary Medicine, Northwest A&F University, Yangling, Shaanxi, ChinaSchool of Life Science and Engineering, Foshan University, Foshan, ChinaCollege of Veterinary Medicine, Northwest A&F University, Yangling, Shaanxi, ChinaStreptococcus equi subsp. zooepidemicus (SEZ) is an opportunistic pathogen of both humans and animals. Quorum sensing (QS) plays an important role in the regulation of bacterial group behaviors. The aim of this study was to characterize the LuxS in SEZ and evaluate its impact on biofilm formation, pathogenesis and gene expression. The wild-type SEZ and its LuxS mutant (ΔluxS) were examined for growth, biofilm formation, virulence factors, and transcriptomic profiles. Our results showed that LuxS deficiency did not affect SEZ hemolytic activity, adhesion or capsule production. For biofilm assay demonstrated that mutation in the luxS gene significantly enhances biofilm formation, produced a denser biofilm and attached to a glass surface. RAW264.7 cell infection indicated that ΔluxS promoted macrophage apoptosis and pro-inflammatory responses. In mice infection, there was no significant difference in mortality between SEZ and ΔluxS. However, the bacterial load in the spleen of mice infected with ΔluxS was significantly higher than in those infected with SEZ. And the pathological analysis further indicated that spleen damage was more severe in the ΔluxS group. Moreover, transcriptomics analysis revealed significant alterations in carbon metabolism, RNA binding and stress response genes in ΔluxS. In summary, this study provides the first evidence of AI-2/LuxS QS system in SEZ and reveals its regulatory effects on biofilm formation, pathogenicity and gene expression.https://www.frontiersin.org/articles/10.3389/fcimb.2024.1339131/fullStreptococcus equi subsp. zooepidemicusLuxSbiofilmcapsular polysaccharidevirulenceinfection
spellingShingle Honglin Xie
Riteng Zhang
Ruhai Guo
Yining Zhang
Jingya Zhang
Hui Li
Qiang Fu
Xinglong Wang
Characterization of AI-2/LuxS quorum sensing system in biofilm formation, pathogenesis of Streptococcus equi subsp. zooepidemicus
Frontiers in Cellular and Infection Microbiology
Streptococcus equi subsp. zooepidemicus
LuxS
biofilm
capsular polysaccharide
virulence
infection
title Characterization of AI-2/LuxS quorum sensing system in biofilm formation, pathogenesis of Streptococcus equi subsp. zooepidemicus
title_full Characterization of AI-2/LuxS quorum sensing system in biofilm formation, pathogenesis of Streptococcus equi subsp. zooepidemicus
title_fullStr Characterization of AI-2/LuxS quorum sensing system in biofilm formation, pathogenesis of Streptococcus equi subsp. zooepidemicus
title_full_unstemmed Characterization of AI-2/LuxS quorum sensing system in biofilm formation, pathogenesis of Streptococcus equi subsp. zooepidemicus
title_short Characterization of AI-2/LuxS quorum sensing system in biofilm formation, pathogenesis of Streptococcus equi subsp. zooepidemicus
title_sort characterization of ai 2 luxs quorum sensing system in biofilm formation pathogenesis of streptococcus equi subsp zooepidemicus
topic Streptococcus equi subsp. zooepidemicus
LuxS
biofilm
capsular polysaccharide
virulence
infection
url https://www.frontiersin.org/articles/10.3389/fcimb.2024.1339131/full
work_keys_str_mv AT honglinxie characterizationofai2luxsquorumsensingsysteminbiofilmformationpathogenesisofstreptococcusequisubspzooepidemicus
AT ritengzhang characterizationofai2luxsquorumsensingsysteminbiofilmformationpathogenesisofstreptococcusequisubspzooepidemicus
AT ruhaiguo characterizationofai2luxsquorumsensingsysteminbiofilmformationpathogenesisofstreptococcusequisubspzooepidemicus
AT yiningzhang characterizationofai2luxsquorumsensingsysteminbiofilmformationpathogenesisofstreptococcusequisubspzooepidemicus
AT jingyazhang characterizationofai2luxsquorumsensingsysteminbiofilmformationpathogenesisofstreptococcusequisubspzooepidemicus
AT huili characterizationofai2luxsquorumsensingsysteminbiofilmformationpathogenesisofstreptococcusequisubspzooepidemicus
AT qiangfu characterizationofai2luxsquorumsensingsysteminbiofilmformationpathogenesisofstreptococcusequisubspzooepidemicus
AT xinglongwang characterizationofai2luxsquorumsensingsysteminbiofilmformationpathogenesisofstreptococcusequisubspzooepidemicus