Hemolysin function of Listeria is related to biofilm formation: transcriptomics analysis

Abstract Listeriolysin O (LLO) is the main virulence protein of Listeria monocytogenes (LM), that helps LM escape lysosomes. We previously found that the cellular immune response elicited by L.ivanovii (LI) is weaker than that elicited by LM. We speculated that this may be related to the function of...

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Main Authors: Ruidan Li, Qian Liang, Sicheng Tian, Yunwen Zhang, Sijing Liu, Qian Ou, Zhaobin Chen, Chuan Wang
Format: Article
Language:English
Published: BMC 2022-12-01
Series:Veterinary Research
Subjects:
Online Access:https://doi.org/10.1186/s13567-022-01124-y
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author Ruidan Li
Qian Liang
Sicheng Tian
Yunwen Zhang
Sijing Liu
Qian Ou
Zhaobin Chen
Chuan Wang
author_facet Ruidan Li
Qian Liang
Sicheng Tian
Yunwen Zhang
Sijing Liu
Qian Ou
Zhaobin Chen
Chuan Wang
author_sort Ruidan Li
collection DOAJ
description Abstract Listeriolysin O (LLO) is the main virulence protein of Listeria monocytogenes (LM), that helps LM escape lysosomes. We previously found that the cellular immune response elicited by L.ivanovii (LI) is weaker than that elicited by LM. We speculated that this may be related to the function of ivanolysin O (ILO). Here, we constructed hemolysin gene deletion strain, LIΔilo, and a modified strain, LIΔilo::hly, in which ilo was replaced by hly. Prokaryotic transcriptome sequencing was performed on LI, LIΔilo, and LIΔilo::hly. Transcriptome differences between the three strains were compared, and genes and pathways with significant differences between the three strains were analyzed. Prokaryotic transcriptome sequencing results revealed the relationship of ilo to the ribosome, quorum sensing, and phosphotransferase system (PTS) pathways, etc. LIΔilo exhibited attenuated biofilm formation ability compared to LI. Biofilm formation was significantly recovered or even increased after replenishing hly. After knocking out ilo, the relative expression levels of some virulence genes, including sigB, prfA, actA, smcL, and virR, were up-regulated compared to LI. After replenishing hly, these genes were down-regulated compared to LIΔilo. The trend and degree of such variation were not completely consistent when cultured in media containing only monosaccharides or disaccharides. The results confirmed that hemolysin is related to some important biological properties of Listeria, including biofilm formation and virulence gene expression levels. This is the first comprehensive study on ILO function at the transcriptomic level and the first evidence of a relationship between Listeria hemolysin and biofilm formation.
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spelling doaj.art-750081e8c25f4bba8d863b117ea285802023-01-01T12:25:13ZengBMCVeterinary Research1297-97162022-12-0153111510.1186/s13567-022-01124-yHemolysin function of Listeria is related to biofilm formation: transcriptomics analysisRuidan Li0Qian Liang1Sicheng Tian2Yunwen Zhang3Sijing Liu4Qian Ou5Zhaobin Chen6Chuan Wang7Department of Public Health Laboratory Sciences, West China School of Public Health and West China Fourth Hospital, Sichuan UniversityDepartment of Public Health Laboratory Sciences, West China School of Public Health and West China Fourth Hospital, Sichuan UniversityDepartment of Public Health Laboratory Sciences, West China School of Public Health and West China Fourth Hospital, Sichuan UniversityDepartment of Public Health Laboratory Sciences, West China School of Public Health and West China Fourth Hospital, Sichuan UniversityDepartment of Public Health Laboratory Sciences, West China School of Public Health and West China Fourth Hospital, Sichuan UniversityDepartment of Public Health Laboratory Sciences, West China School of Public Health and West China Fourth Hospital, Sichuan UniversityShen Zhen Biomed Alliance Biotech Group Co., LtdDepartment of Public Health Laboratory Sciences, West China School of Public Health and West China Fourth Hospital, Sichuan UniversityAbstract Listeriolysin O (LLO) is the main virulence protein of Listeria monocytogenes (LM), that helps LM escape lysosomes. We previously found that the cellular immune response elicited by L.ivanovii (LI) is weaker than that elicited by LM. We speculated that this may be related to the function of ivanolysin O (ILO). Here, we constructed hemolysin gene deletion strain, LIΔilo, and a modified strain, LIΔilo::hly, in which ilo was replaced by hly. Prokaryotic transcriptome sequencing was performed on LI, LIΔilo, and LIΔilo::hly. Transcriptome differences between the three strains were compared, and genes and pathways with significant differences between the three strains were analyzed. Prokaryotic transcriptome sequencing results revealed the relationship of ilo to the ribosome, quorum sensing, and phosphotransferase system (PTS) pathways, etc. LIΔilo exhibited attenuated biofilm formation ability compared to LI. Biofilm formation was significantly recovered or even increased after replenishing hly. After knocking out ilo, the relative expression levels of some virulence genes, including sigB, prfA, actA, smcL, and virR, were up-regulated compared to LI. After replenishing hly, these genes were down-regulated compared to LIΔilo. The trend and degree of such variation were not completely consistent when cultured in media containing only monosaccharides or disaccharides. The results confirmed that hemolysin is related to some important biological properties of Listeria, including biofilm formation and virulence gene expression levels. This is the first comprehensive study on ILO function at the transcriptomic level and the first evidence of a relationship between Listeria hemolysin and biofilm formation.https://doi.org/10.1186/s13567-022-01124-yTranscriptomicsListeria hemolysinbiofilmvirulence factors
spellingShingle Ruidan Li
Qian Liang
Sicheng Tian
Yunwen Zhang
Sijing Liu
Qian Ou
Zhaobin Chen
Chuan Wang
Hemolysin function of Listeria is related to biofilm formation: transcriptomics analysis
Veterinary Research
Transcriptomics
Listeria hemolysin
biofilm
virulence factors
title Hemolysin function of Listeria is related to biofilm formation: transcriptomics analysis
title_full Hemolysin function of Listeria is related to biofilm formation: transcriptomics analysis
title_fullStr Hemolysin function of Listeria is related to biofilm formation: transcriptomics analysis
title_full_unstemmed Hemolysin function of Listeria is related to biofilm formation: transcriptomics analysis
title_short Hemolysin function of Listeria is related to biofilm formation: transcriptomics analysis
title_sort hemolysin function of listeria is related to biofilm formation transcriptomics analysis
topic Transcriptomics
Listeria hemolysin
biofilm
virulence factors
url https://doi.org/10.1186/s13567-022-01124-y
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AT yunwenzhang hemolysinfunctionoflisteriaisrelatedtobiofilmformationtranscriptomicsanalysis
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