Mycobacterium tuberculosis Rv2617c is involved in stress response and phage infection resistance

Mycobacterium tuberculosis (M. tuberculosis) is the pathogen of human tuberculosis (TB). Resistance to numerous in vivo stresses, including oxidative stress, is determinant for M. tuberculosis intracellular survival, and understanding associated mechanisms is crucial for developing new therapeutic s...

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Main Authors: Liadrine Moukendza Koundi, Ulrich Aymard Ekomi Moure, Funmilayo Grâce Boni, Insaf Hamdi, Lin Fan, Jianping Xie
Format: Article
Language:English
Published: Elsevier 2024-03-01
Series:Heliyon
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S2405844024034315
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author Liadrine Moukendza Koundi
Ulrich Aymard Ekomi Moure
Funmilayo Grâce Boni
Insaf Hamdi
Lin Fan
Jianping Xie
author_facet Liadrine Moukendza Koundi
Ulrich Aymard Ekomi Moure
Funmilayo Grâce Boni
Insaf Hamdi
Lin Fan
Jianping Xie
author_sort Liadrine Moukendza Koundi
collection DOAJ
description Mycobacterium tuberculosis (M. tuberculosis) is the pathogen of human tuberculosis (TB). Resistance to numerous in vivo stresses, including oxidative stress, is determinant for M. tuberculosis intracellular survival, and understanding associated mechanisms is crucial for developing new therapeutic strategies. M. tuberculosis Rv2617c has been associated with oxidative stress response when interacting with other proteins in M. tuberculosis; however, its functional promiscuity and underlying molecular mechanisms remain elusive. In this study, we investigated the phenotypic changes of Mycobacterium smegmatis (M. smegmatis) expressing Rv2617c (Ms_Rv2617c) and its behavior in the presence of various in vitro stresses and phage infections. We found that Rv2617c conferred resistance to SDS and diamide while sensitizing M. smegmatis to oxidative stress (H2O2) and altered mycobacterial phenotypic properties (single-cell clone and motility), suggestive of reprogrammed mycobacterial cell wall lipid contents exemplified by increased cell wall permeability. Interestingly, we also found that Rv2617c promoted M. smegmatis resistance to infection by phages (SWU1, SWU2, D29, and TM4) and kept phage TM4 from destroying mycobacterial biofilms. Our findings provide new insights into the role of Rv2617c in resistance to oxide and acid stresses and report for the first time on its role in phage resistance in Mycobacterium.
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spelling doaj.art-685c7ec767c3498ca7bf2eb4ff3f4cb62024-03-17T07:58:04ZengElsevierHeliyon2405-84402024-03-01105e27400Mycobacterium tuberculosis Rv2617c is involved in stress response and phage infection resistanceLiadrine Moukendza Koundi0Ulrich Aymard Ekomi Moure1Funmilayo Grâce Boni2Insaf Hamdi3Lin Fan4Jianping Xie5Institute of Modern Biopharmaceuticals, State Key Laboratory Breeding Base of Eco-Environment and Bio-Resource of the Three Gorges Area, Key Laboratory of Eco-environments in Three Gorges Reservoir Region, Ministry of Education, School of Life Sciences, Southwest University, Chongqing, China; Corresponding author.The Ninth People's Hospital of Chongqing, Affiliated Hospital of Southwest University, Chongqing, China; Cancer Center, Medical Research Institute, Southwest University, 400716, Chongqing, ChinaInstitute of Modern Biopharmaceuticals, State Key Laboratory Breeding Base of Eco-Environment and Bio-Resource of the Three Gorges Area, Key Laboratory of Eco-environments in Three Gorges Reservoir Region, Ministry of Education, School of Life Sciences, Southwest University, Chongqing, ChinaInstitute of Modern Biopharmaceuticals, State Key Laboratory Breeding Base of Eco-Environment and Bio-Resource of the Three Gorges Area, Key Laboratory of Eco-environments in Three Gorges Reservoir Region, Ministry of Education, School of Life Sciences, Southwest University, Chongqing, ChinaShanghai Clinic and Research Center of Tuberculosis, Shanghai Pulmonary Hospital, Tongji University School of Medicine, Shanghai Key Laboratory of Tuberculosis, Shanghai, ChinaInstitute of Modern Biopharmaceuticals, State Key Laboratory Breeding Base of Eco-Environment and Bio-Resource of the Three Gorges Area, Key Laboratory of Eco-environments in Three Gorges Reservoir Region, Ministry of Education, School of Life Sciences, Southwest University, Chongqing, China; Corresponding author.Mycobacterium tuberculosis (M. tuberculosis) is the pathogen of human tuberculosis (TB). Resistance to numerous in vivo stresses, including oxidative stress, is determinant for M. tuberculosis intracellular survival, and understanding associated mechanisms is crucial for developing new therapeutic strategies. M. tuberculosis Rv2617c has been associated with oxidative stress response when interacting with other proteins in M. tuberculosis; however, its functional promiscuity and underlying molecular mechanisms remain elusive. In this study, we investigated the phenotypic changes of Mycobacterium smegmatis (M. smegmatis) expressing Rv2617c (Ms_Rv2617c) and its behavior in the presence of various in vitro stresses and phage infections. We found that Rv2617c conferred resistance to SDS and diamide while sensitizing M. smegmatis to oxidative stress (H2O2) and altered mycobacterial phenotypic properties (single-cell clone and motility), suggestive of reprogrammed mycobacterial cell wall lipid contents exemplified by increased cell wall permeability. Interestingly, we also found that Rv2617c promoted M. smegmatis resistance to infection by phages (SWU1, SWU2, D29, and TM4) and kept phage TM4 from destroying mycobacterial biofilms. Our findings provide new insights into the role of Rv2617c in resistance to oxide and acid stresses and report for the first time on its role in phage resistance in Mycobacterium.http://www.sciencedirect.com/science/article/pii/S2405844024034315Mycobacterium tuberculosisRv2617cDoxX domainStress responsesVirulenceMycobacteriophage resistance
spellingShingle Liadrine Moukendza Koundi
Ulrich Aymard Ekomi Moure
Funmilayo Grâce Boni
Insaf Hamdi
Lin Fan
Jianping Xie
Mycobacterium tuberculosis Rv2617c is involved in stress response and phage infection resistance
Heliyon
Mycobacterium tuberculosis
Rv2617c
DoxX domain
Stress responses
Virulence
Mycobacteriophage resistance
title Mycobacterium tuberculosis Rv2617c is involved in stress response and phage infection resistance
title_full Mycobacterium tuberculosis Rv2617c is involved in stress response and phage infection resistance
title_fullStr Mycobacterium tuberculosis Rv2617c is involved in stress response and phage infection resistance
title_full_unstemmed Mycobacterium tuberculosis Rv2617c is involved in stress response and phage infection resistance
title_short Mycobacterium tuberculosis Rv2617c is involved in stress response and phage infection resistance
title_sort mycobacterium tuberculosis rv2617c is involved in stress response and phage infection resistance
topic Mycobacterium tuberculosis
Rv2617c
DoxX domain
Stress responses
Virulence
Mycobacteriophage resistance
url http://www.sciencedirect.com/science/article/pii/S2405844024034315
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