Lipidomics and genomics of Mycobacterium tuberculosis reveal lineage-specific trends in mycolic acid biosynthesis

MicrobiologyOpen

Volumn 3, Issue 6, 2014, Pages 823-835

  Portevin, Damien ^a,b,c   Sukumar, Sudarkodi ^d   Coscolla, Mireia ^b,c   Shui, Guanghou ^e   Li, Bowen ^d   Guan, Xue Li ^b,c,f   Bendt, Anne K ^d   Young, Douglas ^a   Gagneux, Sebastien ^b,c   Wenk, Markus R ^b,c,d,f  

^a NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

^b SWISS TROPICAL AND PUBLIC HEALTH INSTITUTE   (Switzerland)

^c UNIVERSITY OF BASEL   (Switzerland)

^d NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^e INSTITUTE OF GENETICS AND DEVELOPMENTAL BIOLOGY   (China)

^f NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

Author keywords

Genomics; Lipidomics; Mycolic acid; Phylogenetics; Tuberculosis

Indexed keywords

ETHIONAMIDE; ISONIAZID; MYCOLIC ACID;

ARTICLE; BACTERIAL MEMBRANE; BACTERIAL STRAIN; BACTERIUM CULTURE; BACTERIUM ISOLATION; CELL LINEAGE; CONTROLLED STUDY; ELECTROSPRAY; EPIGENETICS; FATTY ACID METABOLISM; FATTY ACID SYNTHESIS; GENE EXPRESSION PROFILING; GENE MAPPING; GENEALOGY; GENOMICS; IMMUNE RESPONSE; IMMUNOMODULATION; INNATE IMMUNITY; LIPIDOMICS; MASS SPECTROMETRY; MICROBIAL DIVERSITY; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PHYLOGENY; PRIORITY JOURNAL; SINGLE NUCLEOTIDE POLYMORPHISM; BACTERIAL GENOME; CHEMISTRY; CLASSIFICATION; GENETICS; HUMAN; METABOLISM; MICROBIOLOGY; SPECIES DIFFERENCE; TUBERCULOSIS;

MYCOBACTERIUM TUBERCULOSIS;

GENOME, BACTERIAL; GENOMICS; HUMANS; MASS SPECTROMETRY; MYCOBACTERIUM TUBERCULOSIS; MYCOLIC ACIDS; PHYLOGENY; SPECIES SPECIFICITY; TUBERCULOSIS;

EID: 84913605775     PISSN: None     EISSN: 20458827     Source Type: Journal    
DOI: 10.1002/mbo3.193     Document Type: Article

References (52)

1. Aguilar, D., M. Hanekom, D. Mata, N. C. van Gey Pittius, P. D. van Helden, R. M. Warren, et al. 2010. Mycobacterium tuberculosis strains with the Beijing genotype demonstrate variability in virulence associated with transmission. Tuberculosis (Edinb) 90:319-325.
2. Arnvig, K. B., I. Comas, N. R. Thomson, J. Houghton, H. I. Boshoff, N. J. Croucher, et al. 2011. Sequence-based analysis uncovers an abundance of non-coding RNA in the total transcriptome of Mycobacterium tuberculosis. PLoS Pathog. 7:e1002342.
3. Ausubel, F. M., R. Brent, R. E. Kingston, D. D. Moore, J. G. Seidman, J. A. Smith, et al. 1987. Current protocols in molecular biology. Greene Publishing Associates/Wiley Interscience, New York, NY.
4. Barkan, D., D. Hedhli, H.-G. Yan, K. Huygen, and M. S. Glickman . 2012. Mycobacterium tuberculosis lacking all mycolic acid cyclopropanation is viable but highly attenuated and hyperinflammatory in mice. Infect. Immun. 80:1958-1968.
5. Brosch, R., S. V. Gordon, M. Marmiesse, P. Brodin, C. Buchrieser, K. Eiglmeier, et al. 2002. A new evolutionary scenario for the Mycobacterium tuberculosis complex. Proc. Natl Acad. Sci. USA 99:3684-3689.
6. Caws, M., G. Thwaites, S. Dunstan, T. R. Hawn, N. T. N. Lan, N. T. T. Thuong, et al. 2008. The influence of host and bacterial genotype on the development of disseminated disease with Mycobacterium tuberculosis. PLoS Pathog. 4:e1000034.
7. Cole, S. T., R. Brosch, J. Parkhill, T. Garnier, C. Churcher, D. Harris, et al. 1998. Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence. Nature 393:537-544.
8. Comas, I., and S. Gagneux . 2011. A role for systems epidemiology in tuberculosis research. Trends Microbiol. 19:492-500.
9. Comas, I., S. Homolka, S. Niemann, and S. Gagneux . 2009. Genotyping of genetically monomorphic bacteria: DNA sequencing in Mycobacterium tuberculosis highlights the limitations of current methodologies. PLoS One 4:e7815.
10. Comas, I., J. Chakravartti, P. M. Small, J. Galagan, S. Niemann, K. Kremer, et al. 2010. Human T cell epitopes of Mycobacterium tuberculosis are evolutionarily hyperconserved. Nat. Genet. 42:498-503.
11. Comas, I., M. Coscolla, T. Luo, S. Borrell, K. E. Holt, M. Kato-Maeda, et al. 2013. Out-of-Africa migration and Neolithic coexpansion of Mycobacterium tuberculosis with modern humans. Nat. Genet. 45:1176-1182.
12. Coscolla, M., and S. Gagneux . 2010. Does M. tuberculosis genomic diversity explain disease diversity? Drug Discov. Today Dis. Mech. 7:e43-e59.
13. Dubnau, E., J. Chan, C. Raynaud, V. P. Mohan, M. A. Lanéelle, K. Yu, et al. 2000. Oxygenated mycolic acids are necessary for virulence of Mycobacterium tuberculosis in mice. Mol. Microbiol. 36:630-637.
14. Ford, C. B., R. R. Shah, M. K. Maeda, S. Gagneux, M. B. Murray, T. Cohen, et al. 2013. Mycobacterium tuberculosis mutation rate estimates from different lineages predict substantial differences in the emergence of drug-resistant tuberculosis. Nat. Genet. 45:784-790.
15. Gagneux, S., K. DeRiemer, T. Van, M. Kato-Maeda, B. C. Jong, S. Narayanan, et al. 2006. Variable host-pathogen compatibility in Mycobacterium tuberculosis. Proc. Natl Acad. Sci. USA 103:2869-2873.
16. Gao, Q., K. E. Kripke, A. J. Saldanha, W. Yan, S. Holmes, and P. M. Small . 2005. Gene expression diversity among Mycobacterium tuberculosis clinical isolates. Microbiology 151:5-14.
17. Gehre, F., J. Otu, K. DeRiemer, P. F. de Sessions, M. L. Hibberd, W. Mulders, et al. 2013. Deciphering the growth behaviour of Mycobacterium africanum. PLoS Negl. Trop. Dis. 7:e2220.
18. Glickman, M. S. 2003. The mmaA2 gene of Mycobacterium tuberculosis encodes the distal cyclopropane synthase of the alpha-mycolic acid. J. Biol. Chem. 278:7844-7849.
19. Guindon, S., J. F. Dufayard, V. Lefort, M. Anisimova, W. Hordijk, and O. Gascuel . 2010. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst. Biol. 59:307-321.
20. Hammer, Ø, D.A.T. Harper, and P. D. Ryan . 2001. PAST: Paleontological statistics software package for education and data analysis. http://palaeo-electronica.org/2001_1/past/issue1_01.htm.
21. Hanekom, M., N. C. Gey van Pittius, C. McEvoy, T. C. Victor, P. D. Van Helden, and R. M. Warren . 2011. Mycobacterium tuberculosis Beijing genotype: a template for success. Tuberculosis (Edinb) 91:510-523.
22. Hershberg, R., M. Lipatov, P. M. Small, H. Sheffer, S. Niemann, S. Homolka, et al. 2008. High functional diversity in Mycobacterium tuberculosis driven by genetic drift and human demography. PLoS Biol. 6:e311.
23. de Jong, B. C., P. C. Hill, A. Aiken, T. Awine, M. Antonio, I. M. Adetifa, et al. 2008. Progression to active tuberculosis, but not transmission, varies by Mycobacterium tuberculosis lineage in The Gambia. J. Infect. Dis. 198:1037-1043.
24. de Jong, B. C., M. Antonio, and S. Gagneux . 2010. Mycobacterium africanum-review of an important cause of human tuberculosis in West Africa. PLoS Negl. Trop. Dis. 4:e744.
25. Kastrinsky, D. B., N. S. McBride, K. M. Backus, J. J. LeBlanc, and C. E. Barry III. 2. Comprehensive Natural ProductsII. Elsevier.
26. Li, H., B. Handsaker, A. Wysoker, T. Fennell, J. Ruan, N. Homer, et al. 2009. The sequence alignment/map format and SAMtools. Bioinformatics 25:2078-2079.
27. Martinez, J. L., and F. Baquero . 2000. Mutation frequencies and antibiotic resistance. Antimicrob. Agents Chemother. 44:1771-1777.
28. Meena, L. S., P. Chopra, R. A. Vishwakarma, and Y. Singh . 2013. Biochemical characterization of an S-adenosyl-l-methionine-dependent methyltransferase (Rv0469) of Mycobacterium tuberculosis. Biol. Chem. 394:871-877.
29. Müller, B., S. Borrell, G. Rose, and S. Gagneux . 2013. The heterogeneous evolution of multidrug-resistant Mycobacterium tuberculosis. Trends Genet. 29:160-169.
30. Pepperell, C. S., A. M. Casto, A. Kitchen, J. M. Granka, O. E. Cornejo, E. C. Holmes, et al. 2013. The role of selection in shaping diversity of natural M. tuberculosis populations. PLoS Pathog. 9:e1003543.
31. Portevin, D., C. De Sousa-D'Auria, C. Houssin, C. Grimaldi, M. Chami, M. Daffé, et al. 2004. A polyketide synthase catalyzes the last condensation step of mycolic acid biosynthesis in mycobacteria and related organisms. Proc. Natl Acad. Sci. USA 101:314-319.
32. Portevin, D., S. Gagneux, I. Comas, and D. Young . 2011. Human macrophage responses to clinical isolates from the Mycobacterium tuberculosis complex discriminate between ancient and modern lineages. PLoS Pathog. 7:e1001307.
33. Rao, V., N. Fujiwara, S. A. Porcelli, and M. S. Glickman . 2005. Mycobacterium tuberculosis controls host innate immune activation through cyclopropane modification of a glycolipid effector molecule. J. Exp. Med. 201:535-543.
34. Reed, M. B., P. Domenech, C. Manca, H. Su, A. K. Barczak, B. N. Kreiswirth, et al. 2004. A glycolipid of hypervirulent tuberculosis strains that inhibits the innate immune response. Nature 431:84-87.
35. Reed, M. B., S. Gagneux, K. DeRiemer, P. M. Small, and C. E. Barry . 2007. The W-Beijing lineage of Mycobacterium tuberculosis overproduces triglycerides and has the DosR dormancy regulon constitutively upregulated. J. Bacteriol. 189:2583-2589.
36. Rose, G., T. Cortes, I. Comas, M. Coscolla, S. Gagneux, and D. B. Young . 2013. Mapping of genotype-phenotype diversity among clinical isolates of Mycobacterium tuberculosis by sequence-based transcriptional profiling. Genome Biol. Evol. 5:1849-1862.
37. Sambandan, D., D. N. Dao, B. C. Weinrick, C. Vilchèze, S. S. Gurcha, A. Ojha, et al. 2013. Keto-mycolic acid-dependent pellicle formation confers tolerance to drug-sensitive Mycobacterium tuberculosis. MBio 4:e00222.
38. Sequeira, P. C., R. H. Senaratne, and L. W. Riley . 2014. Inhibition of toll-like receptor 2 (TLR-2)-mediated response in human alveolar epithelial cells by mycolic acids and Mycobacterium tuberculosis mce1 operon mutant. Pathog. Dis. 70:132-140.
39. Shell, S. S., E. G. Prestwich, S.-H. Baek, R. R. Shah, C. M. Sassetti, P. C. Dedon, et al. 2013. DNA methylation impacts gene expression and ensures hypoxic survival of Mycobacterium tuberculosis. PLoS Pathog. 9:e1003419.
40. Shui, G., A. K. Bendt, I. A. Jappar, H. M. Lim, M. Laneelle, M. Hervé, et al. 2012. Mycolic acids as diagnostic markers for tuberculosis case detection in humans and drug efficacy in mice. EMBO Mol. Med. 4:27-37.
41. Sim, N.-L., P. Kumar, J. Hu, S. Henikoff, G. Schneider, and P. C. Ng . 2012. SIFT web server: predicting effects of amino acid substitutions on proteins. Nucleic Acids Res. 40:W452-W457.
42. Singh, A., R. Gupta, R. A. Vishwakarma, P. R. Narayanan, C. N. Paramasivan, V. D. Ramanathan, et al. 2005. Requirement of the mymA operon for appropriate cell wall ultrastructure and persistence of Mycobacterium tuberculosis in the spleens of guinea pigs. J. Bacteriol. 187:4173-4186.
43. Sreevatsan, S., X. Pan, K. E. Stockbauer, N. D. Connell, B. N. Kreiswirth, T. S. Whittam, et al. 1997. Restricted structural gene polymorphism in the Mycobacterium tuberculosis complex indicates evolutionarily recent global dissemination. Proc. Natl Acad. Sci. USA 94:9869-9874.
44. de Steenwinkel, J. E. M., M. T. ten Kate, G. J. de Knegt, K. Kremer, R. E. Aarnoutse, M. J. Boeree, et al. 2012. Drug susceptibility of Mycobacterium tuberculosis Beijing genotype and association with MDR TB. Emerg. Infect. Dis. 18:660-663.
45. Takayama, K., C. Wang, and G. S. Besra . 2005. Pathway to synthesis and processing of mycolic acids in Mycobacterium tuberculosis. Clin. Microbiol. Rev. 18:81-101.
46. Vander Beken, S., J. R. Al Dulayymi, T. Naessens, G. Koza, M. Maza-Iglesias, R. Rowles, et al. 2011. Molecular structure of the Mycobacterium tuberculosis virulence factor, mycolic acid, determines the elicited inflammatory pattern. Eur. J. Immunol. 41:450-460.
47. Veyron-Churlet, R., S. Bigot, O. Guerrini, S. Verdoux, W. Malaga, M. Daffé, et al. 2005. The biosynthesis of mycolic acids in Mycobacterium tuberculosis relies on multiple specialized elongation complexes interconnected by specific protein-protein interactions. J. Mol. Biol. 353:847-858.
48. Wang, C., P. Peyron, O. Mestre, G. Kaplan, D. van Soolingen, Q. Gao, et al. 2010. Innate immune response to Mycobacterium tuberculosis Beijing and other genotypes. PLoS One 5:e13594.
49. Watanabe, M., Y. Aoyagi, M. Ridell, and D. E. Minnikin . 2001. Separation and characterization of individual mycolic acids in representative mycobacteria. Microbiology 147:1825-1837.
50. Yang, C., T. Luo, G. Sun, K. Qiao, G. Sun, K. DeRiemer, et al. 2012. Mycobacterium tuberculosis Beijing strains favor transmission but not drug resistance in China. Clin. Infect. Dis. 55:1179-1187.
51. Yassin, A.-A. F. 2011. Detection and characterization of mycolic acids and their use in taxonomy and classification. Pp. 207-237 in Methods in microbiology. Elsevier. Available at: http://linkinghub.elsevier.com/retrieve/pii/B9780123877307000103 (accessed May 27, 2014).
52. Yuan, Y., R. E. Lee, G. S. Besra, J. T. Belisle, and C. E. Barry . 1995. Identification of a gene involved in the biosynthesis of cyclopropanated mycolic acids in Mycobacterium tuberculosis. Proc. Natl Acad. Sci. USA 92:6630-6634.