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Title: Thiol reductive stress induces cellulose-anchored biofilm formation in Mycobacterium tuberculosis

Abstract

Mycobacterium tuberculosis (Mtb) forms biofilms harbouring antibiotic-tolerant bacilli in vitro, but the factors that induce biofilm formation and the nature of the extracellular material that holds the cells together are poorly understood. Here we show that intracellular thiol reductive stress (TRS) induces formation of Mtb biofilms in vitro, which harbour drug-tolerant but metabolically active bacteria with unchanged levels of ATP/ADP, NAD+/NADH and NADP+/NADPH. The development of these biofilms requires DNA, RNA and protein synthesis. Transcriptional analysis suggests that Mtb modulates only similar to 7% of its genes for survival in biofilms. In addition to proteins, lipids and DNA, the extracellular material in these biofilms is primarily composed of polysaccharides, with cellulose being a key component. Lastly, our results contribute to a better understanding of the mechanisms underlying Mtb biofilm formation, although the clinical relevance of Mtb biofilms in human tuberculosis remains unclear.

Authors:
 [1];  [1];  [1]; ORCiD logo [1]
  1. Inst. of Microbial Technology, Chandigarh (India). Council of Scientific and Industrial Research
Publication Date:
Research Org.:
Univ. of Georgia, Athens, GA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES). Chemical Sciences, Geosciences, and Biosciences Division; CSIR; DST, DBT India
OSTI Identifier:
1270967
Grant/Contract Number:  
FG02-93ER20097
Resource Type:
Journal Article: Accepted Manuscript
Journal Name:
Nature Communications
Additional Journal Information:
Journal Volume: 7; Journal ID: ISSN 2041-1723
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; gene-expression; pseudomonas-aeruginosa; escherichia-coli; bacterial biofilms; redox homeostasis; stationary-phase; growth; cell; dna; pathogenesis

Citation Formats

Trivedi, Abhishek, Mavi, Parminder Singh, Bhatt, Deepak, and Kumar, Ashwani. Thiol reductive stress induces cellulose-anchored biofilm formation in Mycobacterium tuberculosis. United States: N. p., 2016. Web. doi:10.1038/ncomms11392.
Trivedi, Abhishek, Mavi, Parminder Singh, Bhatt, Deepak, & Kumar, Ashwani. Thiol reductive stress induces cellulose-anchored biofilm formation in Mycobacterium tuberculosis. United States. https://doi.org/10.1038/ncomms11392
Trivedi, Abhishek, Mavi, Parminder Singh, Bhatt, Deepak, and Kumar, Ashwani. 2016. "Thiol reductive stress induces cellulose-anchored biofilm formation in Mycobacterium tuberculosis". United States. https://doi.org/10.1038/ncomms11392. https://www.osti.gov/servlets/purl/1270967.
@article{osti_1270967,
title = {Thiol reductive stress induces cellulose-anchored biofilm formation in Mycobacterium tuberculosis},
author = {Trivedi, Abhishek and Mavi, Parminder Singh and Bhatt, Deepak and Kumar, Ashwani},
abstractNote = {Mycobacterium tuberculosis (Mtb) forms biofilms harbouring antibiotic-tolerant bacilli in vitro, but the factors that induce biofilm formation and the nature of the extracellular material that holds the cells together are poorly understood. Here we show that intracellular thiol reductive stress (TRS) induces formation of Mtb biofilms in vitro, which harbour drug-tolerant but metabolically active bacteria with unchanged levels of ATP/ADP, NAD+/NADH and NADP+/NADPH. The development of these biofilms requires DNA, RNA and protein synthesis. Transcriptional analysis suggests that Mtb modulates only similar to 7% of its genes for survival in biofilms. In addition to proteins, lipids and DNA, the extracellular material in these biofilms is primarily composed of polysaccharides, with cellulose being a key component. Lastly, our results contribute to a better understanding of the mechanisms underlying Mtb biofilm formation, although the clinical relevance of Mtb biofilms in human tuberculosis remains unclear.},
doi = {10.1038/ncomms11392},
url = {https://www.osti.gov/biblio/1270967}, journal = {Nature Communications},
issn = {2041-1723},
number = ,
volume = 7,
place = {United States},
year = {Mon Apr 25 00:00:00 EDT 2016},
month = {Mon Apr 25 00:00:00 EDT 2016}
}

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Cited by: 91 works
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Works referenced in this record:

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The mechanism of redox sensing in Mycobacterium tuberculosis
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Moisture sorption by cellulose powders of varying crystallinity
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Mycobacterium tuberculosis gene expression during adaptation to stationary phase and low-oxygen dormancy
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Redox environment of the cell as viewed through the redox state of the glutathione disulfide/glutathione couple
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Differences in Metabolism between the Biofilm and Planktonic Response to Metal Stress
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Iron induces bimodal population development by Escherichia coli
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Self-organization of bacterial biofilms is facilitated by extracellular DNA
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Identification of a small molecule with activity against drug-resistant and persistent tuberculosis
journal, June 2013


Heme Oxygenase-1-derived Carbon Monoxide Induces the Mycobacterium tuberculosis Dormancy Regulon
journal, April 2008


Staphylococcus aureus golden pigment impairs neutrophil killing and promotes virulence through its antioxidant activity
journal, July 2005


Environmental Heme-Based Sensor Proteins: Implications for Understanding Bacterial Pathogenesis
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Paradoxical conservation of a set of three cellulose-targeting genes in Mycobacterium tuberculosis complex organisms
journal, May 2010


Growth of Mycobacterium tuberculosis biofilms containing free mycolic acids and harbouring drug-tolerant bacteria
journal, July 2008


Cell envelope stress response in Gram-positive bacteria
journal, January 2008


Pyocyanin Alters Redox Homeostasis and Carbon Flux through Central Metabolic Pathways in Pseudomonas aeruginosa PA14
journal, May 2007


A CsgD-Independent Pathway for Cellulose Production and Biofilm Formation in Escherichia coli
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journal, January 2007


Works referencing / citing this record:

Size-dependent antimycobacterial activity of titanium oxide nanoparticles against Mycobacterium tuberculosis
journal, January 2019


Reductive Stress in Inflammation-Associated Diseases and the Pro-Oxidant Effect of Antioxidant Agents
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Imaging the NADH:NAD+ Homeostasis for Understanding the Metabolic Response of Mycobacterium to Physiologically Relevant Stresses
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Biosynthesis of the redox cofactor mycofactocin comprises oligoglycosylation by MftF in Mycolicibacterium smegmatis
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Redox-guided small molecule antimycobacterials: REDOX-GUIDED SMALL MOLECULE ANTIMYCOBACTERIALS
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Genome-wide analysis of the transcriptional response to drought stress in root and leaf of common bean
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Bioenergetics of Mycobacterium: An Emerging Landscape for Drug Discovery
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Metabolic activity of mature biofilms of Mycobacterium tuberculosis and other non-tuberculous mycobacteria
journal, August 2017


Dual Acting Small-Molecule Inhibitors Targeting Mycobacterial DNA Replication
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Role of the Mycobacterium marinum ESX-1 Secretion System in Sliding Motility and Biofilm Formation
journal, May 2018


Reductive Stress in Inflammation-Associated Diseases and the Pro-Oxidant Effect of Antioxidant Agents
journal, October 2017


Bioenergetics of Mycobacterium: An Emerging Landscape for Drug Discovery
journal, February 2018