Abstract
The genus Mycobacterium includes a wide range of species of both slow and rapid growth under major pathogens, opportunists, and saprophytes. The number and combination of sigma factors are extremely diversified among various species of Mycobacterium. The comparative genome analysis illustrates that SigC, SigD, SigG, SigH, SigK and SigI are dominant among the pathogens. Evolutionary analysis using Bayesian inference on 16S rRNA and MLST-based phylogeny using 14 housekeeping genes distinctly differentiate the slow-growing Mycobacterium from fast growers and segregate pathogens from opportunists and saprophytes. Based on the similarity coefficient upon the allotment of sigma factors in mycobacterial species through UPGMA dendrogram analysis, it is apparent that the pathogens are grouped separately following the similar trend observed from the evolutionary approach. Predominance of a set of sigma factors particularly the pathogenic Mycobacterium co-exists with the distribution of six well-known virulence factors of Mycobacterium (PhoP, PcaA, FbpA, Mce1B, KatG and PE_PGRS30). The pathogenicity responsible sigma factors elicit close resemblance with few notable characters of the known virulence factors. Thus the analysis renders that the distribution of sigma factors of different species of Mycobacterium can be a potential tool to predict their pathogenicity index.
Similar content being viewed by others
References
Ahmed N, Saini V, Raghuvanshi S, Khurana JP, Hasnain TAK, SE, (2007) Molecular analysis of a leprosy immunotherapeutic bacillus provides insights into Mycobacterium evolution. PLoS ONE 2:e968
Ahmed N, Dobrindt U, Hacker J, Hasnain SE (2008) Genomic fluidity and pathogenic bacteria: applications in diagnostics, epidemiology and intervention. Nat Rev Microbiol 6:387–394
Arnold C (2007) Molecular evolution of Mycobacterium tuberculosis. Clin Microbiol Infect 13:120–128
Bairoch A, Boeckmann B, Ferro S, Gasteiger E (2004) Protein sequence databases. Curr Opin Chem Biol 8:76–80. https://doi.org/10.1016/j.cbpa.2003.12.004
Besra GS, McNeil M, Minnikin DE, Portaels F, Ridell M, Brennan PJ (1991) Structural elucidation and antigenicity of a novel glycolipid antigen from Mycobacterium haemophilum. Biochemistry 30:7772–7777
Brosch R, Gordon SV, Marmiesse M, Bordin P, Buchrieser C et al (2002) A new evolutionary scenario for the Mycobacterium tuberculosis complex. Proc Natl Acad Sci USA 99:3684–3689
Cook JL (2010) Nontuberculous mycobacteria: opportunistic environmental pathogens for predisposed hosts. Br Med Bull 96:45–59
Gioffré A, Infante E, Aguilar D, Santangelo MP, Klepp L, Amadio A, Meikle V, Etchechoury I, Romano MI, Cataldi A, Hernández RP, Bigi F (2005) Mutation in mce operons attenuates Mycobacterium tuberculosis virulence. Microbes Infect 7:325–334
Glickman MS, Cox JS Jr, Jacobs WR (2000) A novel mycolic acid cyclopropane synthetase is required for cording, persistence, and virulence of Mycobacterium tuberculosis. Mol Cell 5:717–727
Grigorova IL, Phleger NJ, Mutalik VK, Gross CA (2006) Insights into transcriptional regulation and sigma competition from an equilibrium model of RNA polymerase binding to DNA. Proc Natl Acad Sci USA 103:5332–5337
Gruber TM, Gross CA (2003) Multiple sigma subunits and the partitioning of bacterial transcription space. Annu Rev Microbiol 57:441–466
Horsburgh CR (1991) Mycobacterium avium complex infection in the acquired immunodeficiency syndrome. N Engl J Med 324:1332–1338
Huelsenbeck JP, Ronquist F (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17:754–755
Hümpel A, Gebhard S, Cook GM, Berney M (2010) The SigF regulon in Mycobacterium smegmatis reveals roles in adaptation to stationary phase, heat, and oxidative stress. J Bacteriol 192:2491–2502
Iantomasi R, Sali M, Cascioferro A, Palucci I, Zumbo A, Soldini S, Rocca S, Greco E, Maulucci G, De Spirito M, Fraziano M, Fadda G, Manganelli R, Delogu G (2012) PE_PGRS30 is required for the full virulence of Mycobacterium tuberculosis. Cell Microbiol 14:356–367
Ikai AJ (1980) Thermostability and aliphatic index of globular proteins. J Biochem 88:1895–1898
Jaccard P (1908) Nouvelles recherches sur la distribution florale. Bull Soc Vaud Sci Nat 44:223–270
Kanehisa M, Goto S (2000) KEGG: Kyoto encyclopedia of genes and genomes. Nucleic Acids Res 28:27–30
Kanehisa M, Sato Y, Kawashima M, Furumichi M, Tanabe M (2016) KEGG as a reference resource for gene and protein annotation. Nucleic Acids Res 44:D457–D462
Kanehisa M, Furumichi M, Tanabe M, Sato Y, Morishima K (2017) KEGG: new perspectives on genomes, pathways, diseases and drugs. Nucleic Acids Res 45:D353–D361
Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, Buxton S, Cooper A, Markowitz S, Duran C, Thierer T, Ashton B, Mentjies P, Drummond A (2012) Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28:1647–1649
Khan AA, Kim SJ, Paine DD, Cerniglia CE (2002) Classification of a polycyclic aromatic hydrocarbon-metabolizing bacterium, Mycobacterium sp. strain PYR-1, as Mycobacterium vanbaalenii sp. nov. Int J Syst Evol Microbiol 52:1997–2002
Kim BJ, Math RK, Jeon CO, Yu HK, Park YG, Kook YH, Kim BJ (2013) Mycobacterium yongonense sp. Nov, a slow growing non-chromogenic species closely related to Mycobacterium intracellulare. Int J Syst Evol Microbiol 63:192–199
Kohli S, Singh Y, Sharma K, Mittal A, Ehtesham NZ, Hasnain SE (2012) Comparative genomic and proteomic analyses of PE/PPE multigene family of Mycobacterium tuberculosis H37Rv and H37Ra reveal novel and interesting differences with implications in virulence. Nucleic Acids Res 40:7113–7122
Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: Molecular Evolutionary Genetics Analysis across computing platforms. Mol Biol Evol 35:1547–1549
Kyte J, Doolittle RF (1982) A simple method for displaying the hydropathic character of a protein. J Mol Biol 157:105–132
Lowry CA, Hollis JH, de Vries A, Pan B, Brunet LR, Hunt JRF, Paton JFR, van Kampen E, Knight DM, Evans AK, Rook GAW, Lightman SL (2007) Identification of an immune-responsive mesolimbocortical serotonergic system: potential role in regulation of emotional behaviour. Neuroscience 146:756–772
Manganelli R, Dubnau E, Tyagi S, Kramer FR, Smith I (1999) Differential expression of 10 sigma factor genes in Mycobacterium tuberculosis. Mol Microbiol 31:715–724
Manganelli R, Provvedi R, Rodrigue S, Beaucher J, Gaudreau L, Smith I (2004) Sigma factors and global gene regulation in Mycobacterium tuberculosis. J Bacteriol 186:895–902
Mizuno T, Natori T, Kanazawa I, Eldesouky I, Fukunaga H, Ezaki T (2016) Core housekeeping proteins useful for identification and classification of mycobacteria. Microb Resour Syst 32:25–37
Murcia MI, Tortoli E, Menendez MC, Palenque E, Garcia MJ (2006) Mycobacterium colombiense sp. nov., a novel member of the Mycobacterium avium complex and description of MAC-X as a new ITS genetic variant. Int J Syst Evol Microbiol 56:2049–2054
Ng VH, Cox JS, Sousa AO, MacMicking JD, McKinney JD (2004) Role of KatG catalase-peroxidase in mycobacterial pathogenesis: countering the phagocyte oxidative burst. Mol Microbiol 52:1291–1302
Perez E, Samper S, Bordas Y, Guilhot C, Gicquel B, Martín C (2001) An essential role for phoP in Mycobacterium tuberculosis virulence. Mol Microbiol 41:179–187
Posada D (2008) jModelTest: phylogenetic model averaging. Mol Biol Evol 25:1253–1256
Prasanna AN, Mehra S (2013) Comparative phylogenomics of pathogenic and non-pathogenic Mycobacterium. PLoS ONE 8:e71248
Puech V, Guilhot C, Perez E, Tropis M, Armitige LY, Gicquel B, Daffé M (2002) Evidence for a partial redundancy of the fibronectin-binding proteins for the transfer of mycoloyl residues onto the cell wall arabinogalactan termini of Mycobacterium tuberculosis. Mol Microbiol 44:1109–1122
Ridell M (1983) Immunodiffusion analyses of Mycobacterium farcinogenes, Mycobacterium senegalense and some other mycobacteria. J Gen Microbiol 129:613–619
Rodrigue S, Provvedi R, Jacques PE, Gaudreau L, Manganelli R (2006) The sigma factors of Mycobacterium tuberculosis. FEMS Microbiol Rev 30(6):926–941
Ronning DR, Klabunde T, Besra GS, Vissa VD, Belisle JT, Sacchettini JC (2000) Crystal structure of the secreted form of antigen 85C reveals potential targets for mycobacterial drugs and vaccines. Nat Struct Biol 7:141–146
Saini V, Raghuvanshi S, Talwar GP, Ahmed N, Khurana JP, Hasnain SE, Tyagi AK, Tyagi AK (2009) Polyphasic taxonomic analysis establishes Mycobacterium indicus pranii as a distinct species. PLoS ONE 4:e6263
Schröder KH, Naumann L, Kroppenstedt RM, Reischl U (1997) Mycobacterium hassiacum sp. Nov., a new rapidly growing thermophilic Mycobacterium. Int J Syst Evol Microbiol 47:86–91
Smith I (2003) Mycobacterium tuberculosis pathogenesis and molecular determinants of virulence. Clin Microbiol Rev 16:463–496
Sneath PHA, Sokal RR (1973) Numerical taxonomy: the principles and practice of numerical classification. Freeman, San Francisco, p 573
Tortoli E, Kroppenstedt RM, Bartoloni A, Caroli G, Jan I, Pawlowski J, Emler S (1999) Mycobacterium tusciae sp. nov. Int J Syst Bact 49:1839–1844
van Ingen J, Boeree MJ, Kösters K, Wieland A, Tortoli E, Dekhuijzen PN, van Soolingen D (2009) Proposal to elevate Mycobacterium avium complex ITS sequevar MAC-Q to Mycobacterium vulneris sp. nov. Int J Syst Evol Microbiol 59:2277–2282
Wirth T, Hildebrand F, Allix-Béguec C, Wölbeling F, Kubica T, Kremer K, van Soolingen D et al (2008) Origin, spread and demography of the Mycobacterium tuberculosis complex. PLoS Pathog 4:e1000160
Yang J, Chen LH, Sun LL, Yu J, Jin Q (2008) VFDB 2008 release: an enhanced web-based resource for comparative pathogenomics. Nucleic Acids Res 36(Database issue):D539–D542
Acknowledgements
Fellowship of AMG and part of the research is supported by Grant no 548 (Sanc)/ST/P/S&T/9G-5/2015 funded by Department of Science and Technology, Govt. of West Bengal, India.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
Authors declared no potential conflict of interest.
Additional information
Communicated by Erko Stackebrandt.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Research highlights: the study confers the propagation of different sigma factors upon the diverged category of Mycobacterium species through a purely computational work with 40 different fully annotated whole-genome sequences of three different groups of mycobacterial species. The analysis renders that the distribution of sigma factors of different species of Mycobacterium can be a potential tool to predict their pathogenicity index.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Mallick Gupta, A., Mandal, S. Distribution of sigma factors delineates segregation of virulent and avirulent Mycobacterium. Arch Microbiol 203, 1627–1640 (2021). https://doi.org/10.1007/s00203-020-02172-8
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00203-020-02172-8