BMC Microbiology | |
Comparative genomics for mycobacterial peptidoglycan remodelling enzymes reveals extensive genetic multiplicity | |
Bavesh Davandra Kana1  Christopher Ealand1  Sibusiso Senzani1  Edith Erika Machowski1  | |
[1] DST/NRF Centre of Excellence for Biomedical TB Research, Faculty of Health Sciences, University of the Witwatersrand, National Health Laboratory Service, P.O. Box 1038, Johannesburg 2000, South Africa | |
关键词: Endopeptidases; Transpeptidases; D,D-carboxypeptidases; Amidases; Transglycosylases; Peptidoglycan; | |
Others : 1141548 DOI : 10.1186/1471-2180-14-75 |
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received in 2013-12-27, accepted in 2014-03-12, 发布年份 2014 | |
【 摘 要 】
Background
Mycobacteria comprise diverse species including non-pathogenic, environmental organisms, animal disease agents and human pathogens, notably Mycobacterium tuberculosis. Considering that the mycobacterial cell wall constitutes a significant barrier to drug penetration, the aim of this study was to conduct a comparative genomics analysis of the repertoire of enzymes involved in peptidoglycan (PG) remodelling to determine the potential of exploiting this area of bacterial metabolism for the discovery of new drug targets.
Results
We conducted an in silico analysis of 19 mycobacterial species/clinical strains for the presence of genes encoding resuscitation promoting factors (Rpfs), penicillin binding proteins, endopeptidases, L,D-transpeptidases and N-acetylmuramoyl-L-alanine amidases. Our analysis reveals extensive genetic multiplicity, allowing for classification of mycobacterial species into three main categories, primarily based on their rpf gene complement. These include the M. tuberculosis Complex (MTBC), other pathogenic mycobacteria and environmental species. The complement of these genes within the MTBC and other mycobacterial pathogens is highly conserved. In contrast, environmental strains display significant genetic expansion in most of these gene families. Mycobacterium leprae retains more than one functional gene from each enzyme family, underscoring the importance of genetic multiplicity for PG remodelling. Notably, the highest degree of conservation is observed for N-acetylmuramoyl-L-alanine amidases suggesting that these enzymes are essential for growth and survival.
Conclusion
PG remodelling enzymes in a range of mycobacterial species are associated with extensive genetic multiplicity, suggesting functional diversification within these families of enzymes to allow organisms to adapt.
【 授权许可】
2014 Machowski et al.; licensee BioMed Central Ltd.
【 预 览 】
Files | Size | Format | View |
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20150327075305952.pdf | 576KB | download | |
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Figure 1. | 65KB | Image | download |
【 图 表 】
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Figure 2.
【 参考文献 】
- [1]Nikaido H, Jarlier V: Permeability of the mycobacterial cell wall. Res Microbiol 1991, 142(4):437-443.
- [2]Chatterjee D: The mycobacterial cell wall: structure, biosynthesis and sites of drug action. Curr Opin Chem Biol 1997, 1(4):579-588.
- [3]Brennan PJ, Besra GS: Structure, function and biogenesis of the mycobacterial cell wall. Biochem Soc Trans 1997, 25(1):188-194.
- [4]Jarlier V, Nikaido H: Mycobacterial cell wall: structure and role in natural resistance to antibiotics. FEMS Microbiol Lett 1994, 123(1–2):11-18.
- [5]Barry CE 3rd, Mdluli K: Drug sensitivity and environmental adaptation of mycobacterial cell wall components. Trends Microbiol 1996, 4(7):275-281.
- [6]Favrot L, Ronning DR: Targeting the mycobacterial envelope for tuberculosis drug development. Expert Rev Anti Infect Ther 2012, 10(9):1023-1036.
- [7]Typas A, Banzhaf M, Gross CA, Vollmer W: From the regulation of peptidoglycan synthesis to bacterial growth and morphology. Nat Rev Microbiol 2012, 10(2):123-136.
- [8]Vollmer W, Blanot D, de Pedro MA: Peptidoglycan structure and architecture. FEMS Microbiol Rev 2008, 32(2):149-167.
- [9]Vollmer W, Joris B, Charlier P, Foster S: Bacterial peptidoglycan (murein) hydrolases. FEMS Microbiol Rev 2008, 32(2):259-286.
- [10]Boneca IG: The role of peptidoglycan in pathogenesis. Curr Opin Microbiol 2005, 8(1):46-53.
- [11]Kaur D, Guerin ME, Skovierova H, Brennan PJ, Jackson M: Chapter 2: Biogenesis of the cell wall and other glycoconjugates of Mycobacterium tuberculosis. Adv Appl Microbiol 2009, 69:23-78.
- [12]Besra GS, Brennan PJ: The mycobacterial cell wall: biosynthesis of arabinogalactan and lipoarabinomannan. Biochem Soc Trans 1997, 25(3):845-850.
- [13]Mahapatra S, Crick DC, McNeil MR, Brennan PJ: Unique structural features of the peptidoglycan of Mycobacterium leprae. J Bacteriol 2008, 190(2):655-661.
- [14]Raymond JB, Mahapatra S, Crick DC, Pavelka MS Jr: Identification of the namH gene, encoding the hydroxylase responsible for the N-glycolylation of the mycobacterial peptidoglycan. J Biol Chem 2005, 280(1):326-333.
- [15]Coulombe F, Divangahi M, Veyrier F, de Leseleuc L, Gleason JL, Yang Y, Kelliher MA, Pandey AK, Sassetti CM, Reed MB, Behr MA: Increased NOD2-mediated recognition of N-glycolyl muramyl dipeptide. J Exp Med 2009, 206(8):1709-1716.
- [16]Hansen JM, Golchin SA, Veyrier FJ, Domenech P, Boneca IG, Azad AK, Rajaram MV, Schlesinger LS, Divangahi M, Reed MB, Behr MA: N-Glycolylated Peptidoglycan Contributes to the Immunogenicity but Not Pathogenicity of Mycobacterium tuberculosis. J Infect Dis 2013, 209(7):1045-1054.
- [17]Desmarais SM, De Pedro MA, Cava F, Huang KC: Peptidoglycan at its peaks: how chromatographic analyses can reveal bacterial cell wall structure and assembly. Mol Microbiol 2013, 89(1):1-13.
- [18]Zumla A, Nahid P, Cole ST: Advances in the development of new tuberculosis drugs and treatment regimens. Nat Rev Drug Discov 2013, 12(5):388-404.
- [19]Boshoff HI, Barry CE 3rd: Is the mycobacterial cell wall a hopeless drug target for latent tuberculosis? Drug Discovery Today: Disease Mechanisms 2006, 3(2):237-245.
- [20]Sassetti CM, Boyd DH, Rubin EJ: Genes required for mycobacterial growth defined by high density mutagenesis. Mol Microbiol 2003, 48(1):77-84.
- [21]Griffin JE, Gawronski JD, Dejesus MA, Ioerger TR, Akerley BJ, Sassetti CM: High-resolution phenotypic profiling defines genes essential for mycobacterial growth and cholesterol catabolism. PLoS Pathog 2011, 7(9):e1002251.
- [22]Mukamolova GV, Kaprelyants AS, Young DI, Young M, Kell DB: A bacterial cytokine. Proc Natl Acad Sci U S A 1998, 95(15):8916-8921.
- [23]Mukamolova GV, Murzin AG, Salina EG, Demina GR, Kell DB, Kaprelyants AS, Young M: Muralytic activity of Micrococcus luteus Rpf and its relationship to physiological activity in promoting bacterial growth and resuscitation. Mol Microbiol 2006, 59(1):84-98.
- [24]Cole ST, Brosch R, Parkhill J, Garnier T, Churcher C, Harris D, Gordon SV, Eiglmeier K, Gas S, Barry CE 3rd, Tekaia F, Badcock K, Basham D, Brown D, Chillingworth T, Connor R, Davies R, Devlin K, Feltwell T, Gentles S, Hamlin N, Holroyd S, Hornsby T, Jagels K, Krogh A, McLean J, Moule S, Murphy L, Oliver K, Osborne J, et al.: Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence. Nature 1998, 393(6685):537-544.
- [25]Kana BD, Mizrahi V: Resuscitation-promoting factors as lytic enzymes for bacterial growth and signaling. FEMS Immunol Med Microbiol 2009, 58(1):39-50.
- [26]Mukamolova GV, Turapov OA, Young DI, Kaprelyants AS, Kell DB, Young M: A family of autocrine growth factors in Mycobacterium tuberculosis. Mol Microbiol 2002, 46(3):623-635.
- [27]Kana BD, Mizrahi V: Resuscitation promoting factors in bacterial population dynamics during TB infection. Drug Discovery Today: Disease Mechanisms 2010, 7:e13-e18.
- [28]Keep NH, Ward JM, Cohen-Gonsaud M, Henderson B: Wake up! Peptidoglycan lysis and bacterial non-growth states. Trends Microbiol 2006, 14(6):271-276.
- [29]Keep NH, Ward JM, Robertson G, Cohen-Gonsaud M, Henderson B: Bacterial resuscitation factors: revival of viable but non-culturable bacteria. Cell Mol Life Sci 2006, 63(22):2555-2559.
- [30]Kell DB, Young M: Bacterial dormancy and culturability: the role of autocrine growth factors. Curr Opin Microbiol 2000, 3(3):238-243.
- [31]Tufariello JM, Chan J, Flynn JL: Latent tuberculosis: mechanisms of host and bacillus that contribute to persistent infection. Lancet Infect Dis 2003, 3(9):578-590.
- [32]Downing KJ, Mischenko VV, Shleeva MO, Young DI, Young M, Kaprelyants AS, Apt AS, Mizrahi V: Mutants of Mycobacterium tuberculosis lacking three of the five rpf-like genes are defective for growth in vivo and for resuscitation in vitro. Infect Immun 2005, 73(5):3038-3043.
- [33]Kana BD, Gordhan BG, Downing KJ, Sung N, Vostroktunova G, Machowski EE, Tsenova L, Young M, Kaprelyants A, Kaplan G, Mizrahi V: The resuscitation-promoting factors of Mycobacterium tuberculosis are required for virulence and resuscitation from dormancy but are collectively dispensable for growth in vitro. Mol Microbiol 2008, 67(3):672-684.
- [34]Russell-Goldman E, Xu J, Wang X, Chan J, Tufariello JM: A Mycobacterium tuberculosis Rpf double-knockout strain exhibits profound defects in reactivation from chronic tuberculosis and innate immunity phenotypes. Infect Immun 2008, 76(9):4269-4281.
- [35]Tufariello JM, Mi K, Xu J, Manabe YC, Kesavan AK, Drumm J, Tanaka K, Jacobs WR Jr, Chan J: Deletion of the Mycobacterium tuberculosis resuscitation-promoting factor Rv1009 gene results in delayed reactivation from chronic tuberculosis. Infect Immun 2006, 74(5):2985-2995.
- [36]Gupta RK, Srivastava R: Resuscitation promoting factors: a family of microbial proteins in survival and resuscitation of dormant mycobacteria. Indian J Microbiol 2012, 52(2):114-121.
- [37]Haiser HJ, Yousef MR, Elliot MA: Cell wall hydrolases affect germination, vegetative growth, and sporulation in Streptomyces coelicolor. J Bacteriol 2009, 191(21):6501-6512.
- [38]Hett EC, Rubin EJ: Bacterial growth and cell division: a mycobacterial perspective. Microbiol Mol Biol Rev 2008, 72(1):126-156. table of contents
- [39]Cohen-Gonsaud M, Barthe P, Bagneris C, Henderson B, Ward J, Roumestand C, Keep NH: The structure of a resuscitation-promoting factor domain from Mycobacterium tuberculosis shows homology to lysozymes. Nat Struct Mol Biol 2005, 12(3):270-273.
- [40]Cohen-Gonsaud M, Keep NH, Davies AP, Ward J, Henderson B, Labesse G: Resuscitation-promoting factors possess a lysozyme-like domain. Trends Biochem Sci 2004, 29(1):7-10.
- [41]Ruggiero A, Tizzano B, Pedone E, Pedone C, Wilmanns M, Berisio R: Crystal structure of the resuscitation-promoting factor ΔDUFRpfB from M. tuberculosis. J Mol Biol 2009, 385(1):153-162.
- [42]Romano M, Aryan E, Korf H, Bruffaerts N, Franken CL, Ottenhoff TH, Huygen K: Potential of Mycobacterium tuberculosis resuscitation-promoting factors as antigens in novel tuberculosis sub-unit vaccines. Microbes Infect 2011, 14(1):86-95.
- [43]Riano F, Arroyo L, Paris S, Rojas M, Friggen AH, van Meijgaarden KE, Franken KL, Ottenhoff TH, Garcia LF, Barrera LF: T cell responses to DosR and Rpf proteins in actively and latently infected individuals from Colombia. Tuberculosis (Edinb) 2012, 92(2):148-159.
- [44]Kondratieva T, Rubakova E, Kana BD, Biketov S, Potapov V, Kaprelyants A, Apt A: Mycobacterium tuberculosis attenuated by multiple deletions of rpf genes effectively protects mice against TB infection. Tuberculosis (Edinb) 2011, 91(3):219-223.
- [45]Ravagnani A, Finan CL, Young M: A novel firmicute protein family related to the actinobacterial resuscitation-promoting factors by non-orthologous domain displacement. BMC Genomics 2005, 6(1):39. BioMed Central Full Text
- [46]Hett EC, Chao MC, Deng LL, Rubin EJ: A mycobacterial enzyme essential for cell division synergizes with resuscitation-promoting factor. PLoS Pathog 2008, 4(2):e1000001.
- [47]Mukamolova GV, Turapov O, Malkin J, Woltmann G, Barer MR: Resuscitation-promoting factors reveal an occult population of tubercle bacilli in sputum. Am J Respir Crit Care Med 2009, 181(2):174-180.
- [48]Goffin C, Ghuysen JM: Multimodular penicillin-binding proteins: an enigmatic family of orthologs and paralogs. Microbiol Mol Biol Rev 1998, 62(4):1079-1093.
- [49]Sauvage E, Kerff F, Terrak M, Ayala JA, Charlier P: The penicillin-binding proteins: structure and role in peptidoglycan biosynthesis. FEMS Microbiol Rev 2008, 32(2):234-258.
- [50]Billman-Jacobe H, Haites RE, Coppel RL: Characterization of a Mycobacterium smegmatis mutant lacking penicillin binding protein 1. Antimicrob Agents Chemother 1999, 43(12):3011-3013.
- [51]Patru MM, Pavelka MS Jr: A role for the class A penicillin-binding protein PonA2 in the survival of Mycobacterium smegmatis under conditions of nonreplication. J Bacteriol 2010, 192(12):3043-3054.
- [52]Dasgupta A, Datta P, Kundu M, Basu J: The serine/threonine kinase PknB of Mycobacterium tuberculosis phosphorylates PBPA, a penicillin-binding protein required for cell division. Microbiology 2006, 152(Pt 2):493-504.
- [53]Plocinski P, Ziolkiewicz M, Kiran M, Vadrevu SI, Nguyen HB, Hugonnet J, Veckerle C, Arthur M, Dziadek J, Cross TA, Madiraju M, Rajagopalan M: Characterization of CrgA, a new partner of the Mycobacterium tuberculosis peptidoglycan polymerization complexes. J Bacteriol 2011, 193(13):3246-3256.
- [54]Ghosh SS, Dakoji S, Tanaka Y, Cho YJ, Mobashery S: Properties of analogues of an intermediate in the process of mechanism-based inactivation of carboxypeptidase A. Bioorg Med Chem 1996, 4(9):1487-1492.
- [55]Bourai N, Jacobs WR Jr, Narayanan S: Deletion and overexpression studies on DacB2, a putative low molecular mass penicillin binding protein from Mycobacterium tuberculosis H37Rv. Microb Pathog 2012, 52(2):109-116.
- [56]Kumar P, Arora K, Lloyd JR, Lee IY, Nair V, Fischer E, Boshoff HI, Barry CE 3rd: Meropenem inhibits D, D-carboxypeptidase activity in Mycobacterium tuberculosis. Mol Microbiol 2012, 86(2):367-381.
- [57]Hett EC, Chao MC, Steyn AJ, Fortune SM, Deng LL, Rubin EJ: A partner for the resuscitation-promoting factors of Mycobacterium tuberculosis. Mol Microbiol 2007, 66(3):658-668.
- [58]Hett EC, Chao MC, Rubin EJ: Interaction and modulation of two antagonistic cell wall enzymes of mycobacteria. PLoS Pathog 2010, 6(7):e1001020.
- [59]Chao MC, Kieser KJ, Minami S, Mavrici D, Aldridge BB, Fortune SM, Alber T, Rubin EJ: Protein complexes and proteolytic activation of the cell wall hydrolase RipA regulate septal resolution in mycobacteria. PLoS Pathog 2013, 9(2):e1003197.
- [60]Both D, Schneider G, Schnell R: Peptidoglycan remodeling in Mycobacterium tuberculosis: comparison of structures and catalytic activities of RipA and RipB. J Mol Biol 2013, 413(1):247-260.
- [61]Ruggiero A, Marasco D, Squeglia F, Soldini S, Pedone E, Pedone C, Berisio R: Structure and functional regulation of RipA, a mycobacterial enzyme essential for daughter cell separation. Structure 2010, 18(9):1184-1190.
- [62]Gao LY, Pak M, Kish R, Kajihara K, Brown EJ: A mycobacterial operon essential for virulence in vivo and invasion and intracellular persistence in macrophages. Infect Immun 2006, 74(3):1757-1767.
- [63]Both D, Steiner EM, Izumi A, Schneider G, Schnell R: RipD (Rv1566c) from Mycobacterium tuberculosis: adaptation of an NlpC/p60 domain to a non-catalytic peptidoglycan-binding function. Biochem J 2013, 457(1):33-41.
- [64]Parthasarathy G, Lun S, Guo H, Ammerman NC, Geiman DE, Bishai WR: Rv2190c, an NlpC/P60 family protein, is required for full virulence of Mycobacterium tuberculosis. PLoS One 2012, 7(8):e43429.
- [65]Lavollay M, Fourgeaud M, Herrmann JL, Dubost L, Marie A, Gutmann L, Arthur M, Mainardi JL: The peptidoglycan of Mycobacterium abscessus is predominantly cross-linked by L, D-transpeptidases. J Bacteriol 2011, 193(3):778-782.
- [66]Lavollay M, Arthur M, Fourgeaud M, Dubost L, Marie A, Veziris N, Blanot D, Gutmann L, Mainardi JL: The peptidoglycan of stationary-phase Mycobacterium tuberculosis predominantly contains cross-links generated by L, D-transpeptidation. J Bacteriol 2008, 190(12):4360-4366.
- [67]Gupta R, Lavollay M, Mainardi JL, Arthur M, Bishai WR, Lamichhane G: The Mycobacterium tuberculosis protein LdtMt2 is a nonclassical transpeptidase required for virulence and resistance to amoxicillin. Nat Med 2010, 16(4):466-469.
- [68]Both D, Steiner EM, Stadler D, Lindqvist Y, Schnell R, Schneider G: Structure of LdtMt2, an L, D-transpeptidase from Mycobacterium tuberculosis. Acta Crystallogr D Biol Crystallogr 2013, 69(Pt 3):432-441.
- [69]Schoonmaker MK, Bishai WR, Lamichhane G: Non-classical transpeptidases of Mycobacterium tuberculosis alter cell size, morphology, cytosolic matrix, protein localization, virulence and resistance to beta-lactams. J Bacteriol 2014, 196(7):1394-1402.
- [70]Cordillot M, Dubee V, Triboulet S, Dubost L, Marie A, Hugonnet JE, Arthur M, Mainardi JL: In vitro cross-linking of peptidoglycan by Mycobacterium tuberculosis L,D-transpeptidases and inactivation of these enzymes by carbapenems. Antimicrob Agents Chemother 2013, 57(12):5940-5945.
- [71]Dubee V, Triboulet S, Mainardi JL, Etheve-Quelquejeu M, Gutmann L, Marie A, Dubost L, Hugonnet JE, Arthur M: Inactivation of Mycobacterium tuberculosis L, D-transpeptidase LdtMt1 by carbapenems and cephalosporins. Antimicrob Agents Chemother 2012, 56(8):4189-4195.
- [72]Heidrich C, Templin MF, Ursinus A, Merdanovic M, Berger J, Schwarz H, de Pedro MA, Holtje JV: Involvement of N-acetylmuramyl-L-alanine amidases in cell separation and antibiotic-induced autolysis of Escherichia coli. Mol Microbiol 2001, 41(1):167-178.
- [73]Korsak D, Liebscher S, Vollmer W: Susceptibility to antibiotics and beta-lactamase induction in murein hydrolase mutants of Escherichia coli. Antimicrob Agents Chemother 2005, 49(4):1404-1409.
- [74]Jacobs C, Joris B, Jamin M, Klarsov K, Van Beeumen J, Mengin-Lecreulx D, van Heijenoort J, Park JT, Normark S, Frere JM: AmpD, essential for both beta-lactamase regulation and cell wall recycling, is a novel cytosolic N-acetylmuramyl-L-alanine amidase. Mol Microbiol 1995, 15(3):553-559.
- [75]Popham DL, Helin J, Costello CE, Setlow P: Muramic lactam in peptidoglycan of Bacillus subtilis spores is required for spore outgrowth but not for spore dehydration or heat resistance. Proc Natl Acad Sci U S A 1996, 93(26):15405-15410.
- [76]Smith TJ, Blackman SA, Foster SJ: Autolysins of Bacillus subtilis: multiple enzymes with multiple functions. Microbiology 2000, 146(Pt 2):249-262.
- [77]Prigozhin DM, Mavrici D, Huizar JP, Vansell HJ, Alber T: Structural and Biochemical Analyses of Mycobacterium tuberculosis N-Acetylmuramyl-L-alanine Amidase Rv3717 Point to a Role in Peptidoglycan Fragment Recycling. J Biol Chem 2013, 288(44):31549-31555.
- [78]Cole ST, Eiglmeier K, Parkhill J, James KD, Thomson NR, Wheeler PR, Honoré N, Garnier T, Churcher C, Harris D, Mungall K, Basham D, Brown D, Chillingworth T, Connor R, Davies RM, Devlin K, Duthoy S, Feltwell T, Fraser A, Hamlin N, Holroyd S, Hornsby T, Jagels K, Lacroix C, Maclean J, Moule S, Murphy L, Oliver K, Quail MA, et al.: Massive gene decay in the leprosy bacillus. Nature 2001, 409(6823):1007-1011.
- [79]Kana D, Machowski E, Schechter N, Shin JT, Rubin H, Mizrahi V: Electron transport and respiration. In Mycobacterium: Genomics and Molecular Biology. Caister Academic Press: Norfolk, UK; 2009:35-64.
- [80]Williams MJ, Kana BD, Mizrahi V: Functional analysis of molybdopterin biosynthesis in mycobacteria identifies a fused molybdopterin synthase in Mycobacterium tuberculosis. J Bacteriol 2011, 193(1):98-106.
- [81]Bentley SD, Comas I, Bryant JM, Walker D, Smith NH, Harris SR, Thurston S, Gagneux S, Wood J, Antonio M, Quail MA, Gehre F, Adegbola RA, Parkhill J, de Jong BC: The genome of Mycobacterium africanum West African 2 reveals a lineage-specific locus and genome erosion common to the M. tuberculosis complex. PLoS Negl Trop Dis 2012, 6(2):e1552.
- [82]Brosch R, Gordon SV, Garnier T, Eiglmeier K, Frigui W, Valenti P, Dos Santos S, Duthoy S, Lacroix C, Garcia-Pelayo C, Inwald JK, Golby P, Garcia JN, Hewinson RG, Behr MA, Quail MA, Churcher C, Barrell BG, Parkhill J, Cole ST: Genome plasticity of BCG and impact on vaccine efficacy. Proc Natl Acad Sci U S A 2007, 104(13):5596-5601.
- [83]Fleischmann RD, Alland D, Eisen JA, Carpenter L, White O, Peterson J, DeBoy R, Dodson R, Gwinn M, Haft D, Hickey E, Kolonay JF, Nelson WC, Umayam LA, Ermolaeva M, Salzberg SL, Delcher A, Utterback T, Weidman J, Khouri H, Gill J, Mikula A, Bishai W, Jacobs Jr WR Jr, Venter JC, Fraser CM: Whole-genome comparison of Mycobacterium tuberculosis clinical and laboratory strains. J Bacteriol 2002, 184(19):5479-5490.
- [84]Garnier T, Eiglmeier K, Camus JC, Medina N, Mansoor H, Pryor M, Duthoy S, Grondin S, Lacroix C, Monsempe C, Simon S, Harris B, Atkin R, Doggett J, Mayes R, Keating L, Wheeler PR, Parkhill J, Barrell BG, Cole ST, Gordon SV, Hewinson RG: The complete genome sequence of Mycobacterium bovis. Proc Natl Acad Sci U S A 2003, 100(13):7877-7882.
- [85]Kim BJ, Choi BS, Lim JS, Choi IY, Lee JH, Chun J, Kook YH, Kim BJ: Complete genome sequence of Mycobacterium intracellulare strain ATCC 13950(T). J Bacteriol 2012, 194(10):2750.
- [86]Li L, Bannantine JP, Zhang Q, Amonsin A, May BJ, Alt D, Banerji N, Kanjilal S, Kapur V: The complete genome sequence of Mycobacterium avium subspecies paratuberculosis. Proc Natl Acad Sci U S A 2005, 102(35):12344-12349.
- [87]Shallom SJ, Gardina PJ, Myers TG, Sebastian Y, Conville P, Calhoun LB, Tettelin H, Olivier KN, Uzel G, Sampaio EP, Holland SM, Zelazny AM: New Rapid Scheme for Distinguishing the Subspecies of the Mycobacterium abscessus Group and Identifying Mycobacterium massiliense Isolates with Inducible Clarithromycin Resistance. J Clin Microbiol 2013, 51(9):2943-2949.
- [88]Stinear TP, Seemann T, Harrison PF, Jenkin GA, Davies JK, Johnson PD, Abdellah Z, Arrowsmith C, Chillingworth T, Churcher C, Clarke K, Cronin A, Davis P, Goodhead I, Holroyd N, Jagels K, Lord A, Moule S, Mungall K, Norbertczak H, Quail MA, Rabbinowitsch E, Walker D, White B, Whitehead S, Small PL, Brosch R, Ramakrishnan L, Fischbach MA, Parkhill J, Cole ST: Insights from the complete genome sequence of Mycobacterium marinum on the evolution of Mycobacterium tuberculosis. Genome Res 2008, 18(5):729-741.
- [89]Stinear TP, Seemann T, Pidot S, Frigui W, Reysset G, Garnier T, Meurice G, Simon D, Bouchier C, Ma L, Tichit M, Porter JL, Ryan J, Johnson PD, Davies JK, Jenkin GA, Small PL, Jones LM, Tekaia F, Laval F, Daffé M, Parkhill J, Cole ST: Reductive evolution and niche adaptation inferred from the genome of Mycobacterium ulcerans, the causative agent of Buruli ulcer. Genome Res 2007, 17(2):192-200.
- [90]Zheng H, Lu L, Wang B, Pu S, Zhang X, Zhu G, Shi W, Zhang L, Wang H, Wang S, Zhao G, Zhang Y: Genetic basis of virulence attenuation revealed by comparative genomic analysis of Mycobacterium tuberculosis strain H37Ra versus H37Rv. PLoS One 2008, 3(6):e2375.
- [91]Benson DA, Cavanaugh M, Clark K, Karsch-Mizrachi I, Lipman DJ, Ostell J, Sayers EW: GenBank. Nucleic Acids Res 2013, 41(Database issue):D36-D42.
- [92]Cole ST: Learning from the genome sequence of Mycobacterium tuberculosis H37Rv. FEBS Lett 1999, 452(1–2):7-10.
- [93]Lechat P, Hummel L, Rousseau S, Moszer I: GenoList: an integrated environment for comparative analysis of microbial genomes. Nucleic Acids Res 2008, 36(Database issue):D469-D474.
- [94]Reddy TB, Riley R, Wymore F, Montgomery P, DeCaprio D, Engels R, Gellesch M, Hubble J, Jen D, Jin H, Koehrsen M, Larson L, Mao M, Nitzberg M, Sisk P, Stolte C, Weiner B, White J, Zachariah ZK, Sherlock G, Galagan JE, Ball CA, Schoolnik GK, et al.: TB database: an integrated platform for tuberculosis research. Nucleic Acids Res 2009, 37(Database issue):D499-D508.
- [95]Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ: Basic local alignment search tool. J Mol Biol 1990, 215(3):403-410.
- [96]Kapopoulou A, Lew JM, Cole ST: The MycoBrowser portal: a comprehensive and manually annotated resource for mycobacterial genomes. Tuberculosis (Edinb) 2011, 91(1):8-13.
- [97]Carver TJ, Rutherford KM, Berriman M, Rajandream MA, Barrell BG, Parkhill J: ACT: the Artemis Comparison Tool. Bioinformatics 2005, 21(16):3422-3423.
- [98]Markowitz VM, Chen IM, Palaniappan K, Chu K, Szeto E, Grechkin Y, Ratner A, Jacob B, Huang J, Williams P, Huntemann M, Anderson I, Mavromatis K, Ivanova NN, Kyrpides NC: IMG: the Integrated Microbial Genomes database and comparative analysis system. Nucleic Acids Res 2012, 40(Database issue):D115-D122.
- [99]Sievers F, Wilm A, Dineen D, Gibson TJ, Karplus K, Li W, Lopez R, McWilliam H, Remmert M, Soding J, Thompson JD, Higgins DG: Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol Syst Biol 2011, 7:539.
- [100]Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG: Clustal W and Clustal X version 2.0. Bioinformatics 2007, 23(21):2947-2948.
- [101]Quevillon E, Silventoinen V, Pillai S, Harte N, Mulder N, Apweiler R, Lopez R: InterProScan: protein domains identifier. Nucleic Acids Res 2005, 33(Web Server issue):W116-W120.
- [102]Punta M, Coggill PC, Eberhardt RY, Mistry J, Tate J, Boursnell C, Pang N, Forslund K, Ceric G, Clements J, Heger A, Holm L, Sonnhammer EL, Eddy SR, Bateman A, Finn RD, et al.: The Pfam protein families database. Nucleic Acids Res 2012, 40(Database issue):D290-D301.
- [103]Petersen TN, Brunak S, von Heijne G, Nielsen H: SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat Methods 2011, 8(10):785-786.
- [104]Moller S, Croning MD, Apweiler R: Evaluation of methods for the prediction of membrane spanning regions. Bioinformatics 2001, 17(7):646-653.