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

Trivedi, Abhishek; Mavi, Parminder Singh; Bhatt, Deepak; Kumar, Ashwani

doi:10.1038/ncomms11392

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

Journal Article · Mon Apr 25 00:00:00 EDT 2016 · Nature Communications

DOI:https://doi.org/10.1038/ncomms11392· OSTI ID:1270967

Trivedi, Abhishek ^[1]; Mavi, Parminder Singh ^[1]; Bhatt, Deepak ^[1];

^[1]

Inst. of Microbial Technology, Chandigarh (India). Council of Scientific and Industrial Research

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.

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Research Organization:: Univ. of Georgia, Athens, GA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES). Chemical Sciences, Geosciences, and Biosciences Division; CSIR; DST, DBT India

Grant/Contract Number:: FG02-93ER20097

OSTI ID:: 1270967

Journal Information:: Nature Communications, Vol. 7; ISSN 2041-1723

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 91 works

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References (53)

Extracellular M. tuberculosis DNA Targets Bacteria for Autophagy by Activating the Host DNA-Sensing Pathway Watson, Robert O.; Manzanillo, Paolo S.; Cox, Jeffery S. Cell, Vol. 150, Issue 4 https://doi.org/10.1016/j.cell.2012.06.040	journal	August 2012
Differences in Metabolism between the Biofilm and Planktonic Response to Metal Stress Booth, Sean C.; Workentine, Matthew L.; Wen, Jing Journal of Proteome Research, Vol. 10, Issue 7 https://doi.org/10.1021/pr2002353	journal	July 2011
A novel screening method based on menadione mediated rapid reduction of tetrazolium salt for testing of anti-mycobacterial agents Singh, Upasana; Akhtar, Shamim; Mishra, Abhishek Journal of Microbiological Methods, Vol. 84, Issue 2 https://doi.org/10.1016/j.mimet.2010.11.013	journal	February 2011
The role of iron in Mycobacterium smegmatis biofilm formation: the exochelin siderophore is essential in limiting iron conditions for biofilm formation but not for planktonic growth Ojha, Anil; Hatfull, Graham F. Molecular Microbiology, Vol. 66, Issue 2 https://doi.org/10.1111/j.1365-2958.2007.05935.x	journal	September 2007
Self-organization of bacterial biofilms is facilitated by extracellular DNA Gloag, E. S.; Turnbull, L.; Huang, A. Proceedings of the National Academy of Sciences, Vol. 110, Issue 28 https://doi.org/10.1073/pnas.1218898110	journal	June 2013
Mycobacterial Stationary Phase Induced by Low Oxygen Tension: Cell Wall Thickening and Localization of the 16-Kilodalton α-Crystallin Homolog Cunningham, Adam F.; Spreadbury, Claire L. Journal of Bacteriology, Vol. 180, Issue 4 https://doi.org/10.1128/JB.180.4.801-808.1998	journal	January 1998
Redox Biology of Tuberculosis Pathogenesis Trivedi, Abhishek; Singh, Nisha; Bhat, Shabir Ahmed Advances in Microbial Physiology https://doi.org/10.1016/b978-0-12-398264-3.00004-8	book	January 2012
Cell envelope stress response in Gram-positive bacteria Jordan, Sina; Hutchings, Matthew I.; Mascher, Thorsten FEMS Microbiology Reviews, Vol. 32, Issue 1 https://doi.org/10.1111/j.1574-6976.2007.00091.x	journal	January 2008
Growth of Mycobacterium tuberculosis biofilms containing free mycolic acids and harbouring drug-tolerant bacteria Ojha, Anil K.; Baughn, Anthony D.; Sambandan, Dhinakaran Molecular Microbiology, Vol. 69, Issue 1 https://doi.org/10.1111/j.1365-2958.2008.06274.x	journal	July 2008
Paradoxical conservation of a set of three cellulose-targeting genes in Mycobacterium tuberculosis complex organisms Mba Medie, Felix; Ben Salah, Iskandar; Drancourt, Michel Microbiology, Vol. 156, Issue 5 https://doi.org/10.1099/mic.0.037812-0	journal	May 2010
Mycobacterium tuberculosis Invasion of Macrophages: Linking Bacterial Gene Expression to Environmental Cues Rohde, Kyle H.; Abramovitch, Robert B.; Russell, David G. Cell Host & Microbe, Vol. 2, Issue 5 https://doi.org/10.1016/j.chom.2007.09.006	journal	November 2007
A CsgD-Independent Pathway for Cellulose Production and Biofilm Formation in Escherichia coli Da Re, Sandra; Ghigo, Jean-Marc Journal of Bacteriology, Vol. 188, Issue 8 https://doi.org/10.1128/jb.188.8.3073-3087.2006	journal	April 2006
Lessons from DNA microarray analysis: the gene expression profile of biofilms Lazazzera, Beth A. Current Opinion in Microbiology, Vol. 8, Issue 2 https://doi.org/10.1016/j.mib.2005.02.015	journal	April 2005
Impact of Mycobacterium ulcerans Biofilm on Transmissibility to Ecological Niches and Buruli Ulcer Pathogenesis Marsollier, Laurent; Brodin, Priscille; Jackson, Mary PLoS Pathogens, Vol. 3, Issue 5 https://doi.org/10.1371/journal.ppat.0030062	journal	January 2007
Identification of a small molecule with activity against drug-resistant and persistent tuberculosis Wang, F.; Sambandan, D.; Halder, R. Proceedings of the National Academy of Sciences, Vol. 110, Issue 27 https://doi.org/10.1073/pnas.1309171110	journal	June 2013
Detection and quantitation of cellulase by Congo red staining of substrates in a cup-plate diffusion assay Carder, John H. Analytical Biochemistry, Vol. 153, Issue 1 https://doi.org/10.1016/0003-2697(86)90063-1	journal	February 1986
TM4: A Free, Open-Source System for Microarray Data Management and Analysis Saeed, A. I.; Sharov, V.; White, J. BioTechniques, Vol. 34, Issue 2 https://doi.org/10.2144/03342mt01	journal	February 2003
The biofilm matrix Flemming, Hans-Curt; Wingender, Jost Nature Reviews Microbiology, Vol. 8, Issue 9 https://doi.org/10.1038/nrmicro2415	journal	August 2010
Staphylococcus aureus golden pigment impairs neutrophil killing and promotes virulence through its antioxidant activity Liu, George Y.; Essex, Anthony; Buchanan, John T. The Journal of Experimental Medicine, Vol. 202, Issue 2 https://doi.org/10.1084/jem.20050846	journal	July 2005
Pyocyanin Alters Redox Homeostasis and Carbon Flux through Central Metabolic Pathways in Pseudomonas aeruginosa PA14 Price-Whelan, Alexa; Dietrich, Lars E. P.; Newman, Dianne K. Journal of Bacteriology, Vol. 189, Issue 17 https://doi.org/10.1128/jb.00505-07	journal	May 2007
Finding gene-expression patterns in bacterial biofilms Beloin, Christophe; Ghigo, Jean-Marc Trends in Microbiology, Vol. 13, Issue 1 https://doi.org/10.1016/j.tim.2004.11.008	journal	January 2005
Metabolic Profiling of Lung Granuloma in Mycobacterium tuberculosis Infected Guinea Pigs: Ex vivo ¹ H Magic Angle Spinning NMR Studies Somashekar, B. S.; Amin, Anita G.; Rithner, Christopher D. Journal of Proteome Research, Vol. 10, Issue 9 https://doi.org/10.1021/pr2003352	journal	September 2011
Heme Oxygenase-1-derived Carbon Monoxide Induces the Mycobacterium tuberculosis Dormancy Regulon Kumar, Ashwani; Deshane, Jessy S.; Crossman, David K. Journal of Biological Chemistry, Vol. 283, Issue 26 https://doi.org/10.1074/jbc.m802274200	journal	April 2008
The glycosyltransferases of Mycobacterium tuberculosis—roles in the synthesis of arabinogalactan, lipoarabinomannan, and other glycoconjugates Berg, Stefan; Kaur, Devinder; Jackson, Mary Glycobiology, Vol. 17, Issue 6 https://doi.org/10.1093/glycob/cwm010	journal	January 2007
Expression of the multiple antibiotic resistance operon (mar) during growth of Escherichia coli as a biofilm Maira-Litran, T.; Allison, D. G.; Gilbert, P. Journal of Applied Microbiology, Vol. 88, Issue 2 https://doi.org/10.1046/j.1365-2672.2000.00963.x	journal	February 2000
Genomic Expression Programs in the Response of Yeast Cells to Environmental Changes Gasch, Audrey P.; Spellman, Paul T.; Kao, Camilla M. Molecular Biology of the Cell, Vol. 11, Issue 12 https://doi.org/10.1091/mbc.11.12.4241	journal	December 2000
The novel Pseudomonas aeruginosa two-component regulator BfmR controls bacteriophage-mediated lysis and DNA release during biofilm development through PhdA: BfmR and eDNA Petrova, Olga E.; Schurr, Jill R.; Schurr, Michael J. Molecular Microbiology, Vol. 81, Issue 3 https://doi.org/10.1111/j.1365-2958.2011.07733.x	journal	July 2011
Significance analysis of microarrays applied to the ionizing radiation response Tusher, V. G.; Tibshirani, R.; Chu, G. Proceedings of the National Academy of Sciences, Vol. 98, Issue 9, p. 5116-5121 https://doi.org/10.1073/pnas.091062498	journal	April 2001
Iron induces bimodal population development by Escherichia coli DePas, W. H.; Hufnagel, D. A.; Lee, J. S. Proceedings of the National Academy of Sciences, Vol. 110, Issue 7 https://doi.org/10.1073/pnas.1218703110	journal	January 2013
Dithiothreitol, a New Protective Reagent for SH Groups ^* Cleland, W. W. Biochemistry, Vol. 3, Issue 4 https://doi.org/10.1021/bi00892a002	journal	April 1964
Enhanced production of bacterial cellulose by using a biofilm reactor and its material property analysis Cheng, Kuan-Chen; Catchmark, Jeff M.; Demirci, Ali Journal of Biological Engineering, Vol. 3, Issue 1 https://doi.org/10.1186/1754-1611-3-12	journal	January 2009
Gene expression in Pseudomonas aeruginosa biofilms Whiteley, Marvin; Bangera, M. Gita; Bumgarner, Roger E. Nature, Vol. 413, Issue 6858 https://doi.org/10.1038/35101627	journal	October 2001
An Empirical Method for Estimating the Degree of Crystallinity of Native Cellulose Using the X-Ray Diffractometer Segal, L.; Creely, J. J.; Martin, A. E. Textile Research Journal, Vol. 29, Issue 10 https://doi.org/10.1177/004051755902901003	journal	October 1959
Redox environment of the cell as viewed through the redox state of the glutathione disulfide/glutathione couple Schafer, Freya Q.; Buettner, Garry R. Free Radical Biology and Medicine, Vol. 30, Issue 11 https://doi.org/10.1016/s0891-5849(01)00480-4	journal	June 2001
The mechanism of redox sensing in Mycobacterium tuberculosis Bhat, Shabir Ahmad; Singh, Nisha; Trivedi, Abhishek Free Radical Biology and Medicine, Vol. 53, Issue 8 https://doi.org/10.1016/j.freeradbiomed.2012.08.008	journal	October 2012
Microcolony formation: a novel biofilm model of Pseudomonas aeruginosa for the cystic fibrosis lung Sriramulu, Dinesh D.; Lünsdorf, Heinrich; Lam, Joseph S. Journal of Medical Microbiology, Vol. 54, Issue 7 https://doi.org/10.1099/jmm.0.45969-0	journal	July 2005
Biofilm formation at the air-liquid interface by the Pseudomonas fluorescens SBW25 wrinkly spreader requires an acetylated form of cellulose: Biofilm formation by P. fluorescens SBW25 Spiers, Andrew J.; Bohannon, John; Gehrig, Stefanie M. Molecular Microbiology, Vol. 50, Issue 1 https://doi.org/10.1046/j.1365-2958.2003.03670.x	journal	August 2003
MicroReview: Envelope stress responses and Gram-negative bacterial pathogenesis: Envelope stress responses and virulence Raivio, Tracy L. Molecular Microbiology, Vol. 56, Issue 5 https://doi.org/10.1111/j.1365-2958.2005.04625.x	journal	March 2005
Genetic analysis of Salmonella enteritidis biofilm formation: critical role of cellulose: S. enteritidis biofilm formation Solano, Cristina; García, Begoña; Valle, Jaione Molecular Microbiology, Vol. 43, Issue 3 https://doi.org/10.1046/j.1365-2958.2002.02802.x	journal	February 2002
Moisture sorption by cellulose powders of varying crystallinity Mihranyan, Albert; Llagostera, Assumpcio Piñas; Karmhag, Richard International Journal of Pharmaceutics, Vol. 269, Issue 2 https://doi.org/10.1016/j.ijpharm.2003.09.030	journal	January 2004
Mycobacterium tuberculosis gene expression during adaptation to stationary phase and low-oxygen dormancy Voskuil, M. I.; Visconti, K. C.; Schoolnik, G. K. Tuberculosis, Vol. 84, Issue 3-4 https://doi.org/10.1016/j.tube.2004.02.003	journal	January 2004
Environmental Heme-Based Sensor Proteins: Implications for Understanding Bacterial Pathogenesis Farhana, Aisha; Saini, Vikram; Kumar, Ashwani Antioxidants & Redox Signaling, Vol. 17, Issue 9 https://doi.org/10.1089/ars.2012.4613	journal	November 2012
Redox homeostasis in mycobacteria: the key to tuberculosis control? Kumar, Ashwani; Farhana, Aisha; Guidry, Loni Expert Reviews in Molecular Medicine, Vol. 13 https://doi.org/10.1017/S1462399411002079	journal	March 2011
Expression of antimicrobial drug tolerance by attached communities of Mycobacterium tuberculosis Ackart, David F.; Hascall-Dove, Laurel; Caceres, Silvia M. Pathogens and Disease, Vol. 70, Issue 3 https://doi.org/10.1111/2049-632X.12144	journal	February 2014
Reversal of Mycobacterium tuberculosis phenotypic drug resistance by 2-aminoimidazole-based small molecules Ackart, David F.; Lindsey, Erick A.; Podell, Brendan K. Pathogens and Disease, Vol. 70, Issue 3 https://doi.org/10.1111/2049-632X.12143	journal	February 2014
The Polyketide Pks1 Contributes to Biofilm Formation in Mycobacterium tuberculosis Pang, J. M.; Layre, E.; Sweet, L. Journal of Bacteriology, Vol. 194, Issue 3 https://doi.org/10.1128/JB.06304-11	journal	November 2011
Inhibition of Escherichia coli by thioglycerol. Jensen, K. K.; Javor, G. T. Antimicrobial Agents and Chemotherapy, Vol. 19, Issue 4 https://doi.org/10.1128/AAC.19.4.556	journal	April 1981
Functional and Genomic Analyses Reveal an Essential Coordination between the Unfolded Protein Response and ER-Associated Degradation Travers, Kevin J.; Patil, Christopher K.; Wodicka, Lisa Cell, Vol. 101, Issue 3 https://doi.org/10.1016/S0092-8674(00)80835-1	journal	April 2000
Optimizing a Candida Biofilm Microtiter Plate Model for Measurement of Antifungal Susceptibility by Tetrazolium Salt Assay Nett, J. E.; Cain, M. T.; Crawford, K. Journal of Clinical Microbiology, Vol. 49, Issue 4 https://doi.org/10.1128/JCM.02273-10	journal	January 2011
The Transcriptional Responses of Mycobacterium tuberculosis to Inhibitors of Metabolism: NOVEL INSIGHTS INTO DRUG MECHANISMS OF ACTION Boshoff, Helena I. M.; Myers, Timothy G.; Copp, Brent R. Journal of Biological Chemistry, Vol. 279, Issue 38 https://doi.org/10.1074/jbc.M406796200	journal	July 2004
Semimicro determination of cellulose inbiological materials Updegraff, David M. Analytical Biochemistry, Vol. 32, Issue 3 https://doi.org/10.1016/S0003-2697(69)80009-6	journal	December 1969
Role of Antibiotic Penetration Limitation in Klebsiella pneumoniae Biofilm Resistance to Ampicillin and Ciprofloxacin Anderl, J. N.; Franklin, M. J.; Stewart, P. S. Antimicrobial Agents and Chemotherapy, Vol. 44, Issue 7 https://doi.org/10.1128/AAC.44.7.1818-1824.2000	journal	July 2000
A Natural View of Microbial Biodiversity within Hot Spring Cyanobacterial Mat Communities Ward, David M.; Ferris, Michael J.; Nold, Stephen C. Microbiology and Molecular Biology Reviews, Vol. 62, Issue 4 https://doi.org/10.1128/mmbr.62.4.1353-1370.1998	journal	December 1998

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

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