The mycobacterial glycoside hydrolase LamH enables capsular arabinomannan release and stimulates growth.
Journal
Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555
Informations de publication
Date de publication:
09 Jul 2024
09 Jul 2024
Historique:
received:
06
12
2023
accepted:
26
06
2024
medline:
10
7
2024
pubmed:
10
7
2024
entrez:
9
7
2024
Statut:
epublish
Résumé
Mycobacterial glycolipids are important cell envelope structures that drive host-pathogen interactions. Arguably, the most important are lipoarabinomannan (LAM) and its precursor, lipomannan (LM), which are trafficked from the bacterium to the host via unknown mechanisms. Arabinomannan is thought to be a capsular derivative of these molecules, lacking a lipid anchor. However, the mechanism by which this material is generated has yet to be elucidated. Here, we describe the identification of a glycoside hydrolase family 76 enzyme that we term LamH (Rv0365c in Mycobacterium tuberculosis) which specifically cleaves α-1,6-mannoside linkages within LM and LAM, driving its export to the capsule releasing its phosphatidyl-myo-inositol mannoside lipid anchor. Unexpectedly, we found that the catalytic activity of this enzyme is important for efficient exit from stationary phase cultures, potentially implicating arabinomannan as a signal for growth phase transition. Finally, we demonstrate that LamH is important for M. tuberculosis survival in macrophages.
Identifiants
pubmed: 38982040
doi: 10.1038/s41467-024-50051-3
pii: 10.1038/s41467-024-50051-3
doi:
Substances chimiques
lipoarabinomannan
0
Lipopolysaccharides
0
Mannans
0
arabinomannan
53026-40-7
Glycoside Hydrolases
EC 3.2.1.-
Bacterial Proteins
0
lipomannan
0
phosphatidylinositol mannoside
0
Phosphatidylinositols
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
5740Subventions
Organisme : RCUK | Biotechnology and Biological Sciences Research Council (BBSRC)
ID : BB/S010122/1
Organisme : RCUK | Biotechnology and Biological Sciences Research Council (BBSRC)
ID : BB/X00841X/1
Organisme : RCUK | Biotechnology and Biological Sciences Research Council (BBSRC)
ID : BB/X016749/1
Organisme : RCUK | Biotechnology and Biological Sciences Research Council (BBSRC)
ID : BB/W01954X/1
Organisme : Wellcome Trust (Wellcome)
ID : 226644/Z/22/Z
Organisme : Wellcome Trust (Wellcome)
ID : 209437/Z/17/Z
Organisme : Wellcome Trust (Wellcome)
ID : 226644/Z/22/Z
Organisme : Wellcome Trust (Wellcome)
ID : 226644/Z/22/Z
Organisme : RCUK | Medical Research Council (MRC)
ID : MR/S000542/1
Organisme : Department of Education and Training | Australian Research Council (ARC)
ID : DP210100235
Organisme : Department of Education and Training | Australian Research Council (ARC)
ID : DP210100362
Organisme : U.S. Department of Health & Human Services | NIH | National Institute of General Medical Sciences (NIGMS)
ID : R01GM148075
Informations de copyright
© 2024. The Author(s).
Références
Dörr, T., Moynihan, P. J. & Mayer, C. Editorial: bacterial cell wall structure and dynamics. Front. Microbiol. 10, 2051 (2019).
pubmed: 31551985
pmcid: 6737391
doi: 10.3389/fmicb.2019.02051
Acharya, P. V. N. & Goldman, D. S. Chemical composition of the cell wall of the H37Ra strain of Mycobacterium tuberculosis. J. Bacteriol. 102, 733–739 (1970).
pubmed: 4988039
pmcid: 247620
doi: 10.1128/jb.102.3.733-739.1970
Lawn, S. D., Kerkhoff, A. D., Vogt, M. & Wood, R. Diagnostic accuracy of a low-cost, urine antigen, point-of-care screening assay for HIV-associated pulmonary tuberculosis before antiretroviral therapy: a descriptive study. Lancet Infect. Dis. 12, 201–209 (2012).
pubmed: 22015305
pmcid: 3315025
doi: 10.1016/S1473-3099(11)70251-1
Tailleux, L. et al. DC-SIGN is the major Mycobacterium tuberculosis receptor on human dendritic cells. J. Exp. Med. 197, 121–127 (2003).
pubmed: 12515819
pmcid: 2193794
doi: 10.1084/jem.20021468
Yonekawa, A. et al. Dectin-2 is a direct receptor for mannose-capped lipoarabinomannan of mycobacteria. Immunity 41, 402–413 (2014).
pubmed: 25176311
doi: 10.1016/j.immuni.2014.08.005
Chatterjee, D., Hunter, S. W., McNeil, M. & Brennan, P. J. Lipoarabinomannan. Multiglycosylated form of the mycobacterial mannosylphosphatidylinositols. J. Biol. Chem. 267, 6228–6233 (1992).
pubmed: 1556131
doi: 10.1016/S0021-9258(18)42685-3
Angala, S. K., Li, W., Boot, C. M., Jackson, M. & McNeil, M. R. Secondary extended mannan side chains and attachment of the arabinan in mycobacterial lipoarabinomannan. Commun. Chem. 3, 101 (2020).
pubmed: 34295997
pmcid: 8294699
doi: 10.1038/s42004-020-00356-3
Kaur, D. et al. A single arabinan chain is attached to the phosphatidylinositol mannosyl core of the major immunomodulatory mycobacterial cell envelope glycoconjugate, lipoarabinomannan*. J. Biol. Chem. 289, 30249–30256 (2014).
pubmed: 25231986
pmcid: 4215209
doi: 10.1074/jbc.M114.599415
Palčeková, Z. et al. Disruption of the SucT acyltransferase in Mycobacterium smegmatis abrogates succinylation of cell envelope polysaccharides. J. Biol. Chem. 294, 10325–10335 (2019).
pubmed: 31110045
pmcid: 6664188
doi: 10.1074/jbc.RA119.008585
Palčeková, Z. et al. Role of succinyl substituents in the mannose-capping of lipoarabinomannan and control of inflammation in Mycobacterium tuberculosis infection. PLOS Pathog. 19, e1011636 (2023).
pubmed: 37669276
pmcid: 10503756
doi: 10.1371/journal.ppat.1011636
Treumann, A. et al. 5-Methylthiopentose: a new substituent on lipoarabinomannan in Mycobacterium tuberculosis. J. Mol. Biol. 316, 89–100 (2002).
pubmed: 11829505
doi: 10.1006/jmbi.2001.5317
Turnbull, W. B., Shimizu, K. H., Chatterjee, D., Homans, S. W. & Treumann, A. Identification of the 5‐methylthiopentosyl substituent in Mycobacterium tuberculosis lipoarabinomannan. Angew. Chem. Int. Ed. 43, 3918–3922 (2004).
doi: 10.1002/anie.200454119
Joe, M. et al. The 5-Deoxy-5-Methylthio-Xylofuranose Residue in Mycobacterial Lipoarabinomannan. Absolute Stereochemistry, Linkage Position, Conformation, and Immunomodulatory Activity, Vol. 128 (American Chemical Society, 2006).
Chatterjee, D., Lowell, K., Rivoire, B., McNeil, M. R. & Brennan, P. J. Lipoarabinomannan of Mycobacterium tuberculosis. Capping with mannosyl residues in some strains. J. Biol. Chem. 267, 6234–6239 (1992).
pubmed: 1556132
doi: 10.1016/S0021-9258(18)42686-5
De, P. et al. Structural implications of lipoarabinomannan glycans from global clinical isolates in diagnosis of Mycobacterium tuberculosis infection. J. Biol. Chem. 297, 101265 (2021).
pubmed: 34600887
pmcid: 8531672
doi: 10.1016/j.jbc.2021.101265
Fukuda, T. et al. Critical roles for lipomannan and lipoarabinomannan in cell wall integrity of mycobacteria and pathogenesis of tuberculosis. Mbio 4, e00472–12 (2013).
pubmed: 23422411
pmcid: 3573661
doi: 10.1128/mBio.00472-12
Sparks, I. L. et al. Lipoarabinomannan mediates localized cell wall integrity during division in mycobacteria. Nat. Commun. 15, 2191 (2024).
pubmed: 38467648
pmcid: 10928101
doi: 10.1038/s41467-024-46565-5
Goodell, E. W. & Schwarz, U. Release of cell wall peptides into culture medium by exponentially growing Escherichia coli. J. Bacteriol. 162, 391–397 (1985).
pubmed: 2858468
pmcid: 219001
doi: 10.1128/jb.162.1.391-397.1985
Goldman, W. E., Klapper, D. G. & Baseman, J. B. Detection, isolation, and analysis of a released Bordetella pertussis product toxic to cultured tracheal cells. Infect. Immun. 36, 782–794 (1982).
pubmed: 6177637
pmcid: 351298
doi: 10.1128/iai.36.2.782-794.1982
Chan, J. M. & Dillard, J. P. Attention seeker: production, modification, and release of inflammatory peptidoglycan fragments in Neisseria species. J. Bacteriol. 199, 10–1128 (2017).
Al-Jourani, O. et al. Identification of d-arabinan-degrading enzymes in mycobacteria. Nat. Commun. 14, 2233 (2023).
pubmed: 37076525
pmcid: 10115798
doi: 10.1038/s41467-023-37839-5
Lemassu, A. & Daffé, M. Structural features of the exocellular polysaccharides of Mycobacterium tuberculosis. Biochem. J. 297, 351–357 (1994).
pubmed: 8297342
pmcid: 1137836
doi: 10.1042/bj2970351
Thompson, A. J. et al. Evidence for a boat conformation at the transition state of GH76 α‐1,6‐mannanases—key enzymes in bacterial and fungal mannoprotein metabolism. Angew. Chem. Int Ed. 54, 5378–5382 (2015).
doi: 10.1002/anie.201410502
Vogt, M. S., Schmitz, G. F., Silva, D. V., Mösch, H.-U. & Essen, L.-O. Structural base for the transfer of GPI-anchored glycoproteins into fungal cell walls. Proc. Natl. Acad. Sci. USA 117, 22061–22067 (2020).
pubmed: 32839341
pmcid: 7486726
doi: 10.1073/pnas.2010661117
Cuskin, F. et al. Human gut bacteroidetes can utilize yeast mannan through a selfish mechanism. Nature 517, 165–169 (2015).
pubmed: 25567280
pmcid: 4978465
doi: 10.1038/nature13995
Solanki, V. et al. Glycoside hydrolase from the GH76 family indicates that marine Salegentibacter sp. Hel_I_6 consumes alpha-mannan from fungi. ISME J. 16, 1818–1830 (2022).
pubmed: 35414716
pmcid: 9213526
doi: 10.1038/s41396-022-01223-w
Kempen, et al. Fast and accurate protein structure search with Foldseek. Nat. Biotechnol. https://doi.org/10.1038/s41587-023-01773-0 (2023).
Kabsch, W. A solution for the best rotation to relate two sets of vectors. Acta Crystallogr. Sect. Cryst. Phys. Diffr. Theor. Gen. Crystallogr. 32, 922–923 (1976).
doi: 10.1107/S0567739476001873
Souza, G. A. D., Leversen, N. A., Målen, H. & Wiker, H. G. Bacterial proteins with cleaved or uncleaved signal peptides of the general secretory pathway. J. Proteom. 75, 502–510 (2011).
doi: 10.1016/j.jprot.2011.08.016
Målen, H., Pathak, S., Søfteland, T., de Souza, G. A. & Wiker, H. G. Definition of novel cell envelope associated proteins in Triton X-114 extracts of Mycobacterium tuberculosis H37Rv. BMC Microbiol. 10, 132–132 (2010).
pubmed: 20429878
pmcid: 2874799
doi: 10.1186/1471-2180-10-132
Xiong, Y., Chalmers, M. J., Gao, F. P., Cross, T. A. & Marshall, A. G. Identification of Mycobacterium tuberculosis H37Rv integral membrane proteins by one-dimensional gel electrophoresis and liquid chromatography electrospray ionization tandem mass spectrometry. J. Proteome Res. 4, 855–861 (2005).
pubmed: 15952732
doi: 10.1021/pr0500049
Mawuenyega, K. G. et al. Mycobacterium tuberculosis functional network analysis by global subcellular protein profiling. Mol. Biol. Cell 16, 396–404 (2004).
pubmed: 15525680
doi: 10.1091/mbc.e04-04-0329
Hermann, C., Giddey, A. D., Nel, A. J. M., Soares, N. C. & Blackburn, J. M. Cell wall enrichment unveils proteomic changes in the cell wall during treatment of Mycobacterium smegmatis with sub-lethal concentrations of rifampicin. J. Proteom. 191, 166–179 (2019).
doi: 10.1016/j.jprot.2018.02.019
Perkowski, E. F. et al. The EXIT strategy: an approach for identifying bacterial proteins exported during host infection. Mbio 8, e00333–17 (2017).
pubmed: 28442606
pmcid: 5405230
Woude, A. D., Stoop, E., Stiess, M. & Wang, S. Analysis of SecA2‐dependent substrates in Mycobacterium marinum identifies protein kinase G (PknG) as a virulence effector. Cell. Microbiol. 16, 280–295 (2014).
Winden, V. J. C. van., Houben, E. N. G. & Braunstein, M. Protein export into and across the atypical diderm cell envelope of mycobacteria. Microbiol. Spectr. 7, 10–1128 (2019).
Lemoine, F. et al. NGPhylogeny.fr: new generation phylogenetic services for non-specialists. Nucleic Acids Res. 47, W260–W265 (2019).
pubmed: 31028399
pmcid: 6602494
doi: 10.1093/nar/gkz303
Altschul, S. F., Gish, W., Miller, W., Myers, E. W. & Lipman, D. J. Basic local alignment search tool. J. Mol. Biol. 215, 403–410 (1990).
pubmed: 2231712
doi: 10.1016/S0022-2836(05)80360-2
Chatterjee, D. et al. Structural definition of the non-reducing termini of mannose-capped LAM from Mycobacterium tuberculosis through selective enzymatic degradation and fast atom bombardment-mass spectrometry. Glycobiology 3, 497–506 (1993).
pubmed: 8286863
doi: 10.1093/glycob/3.5.497
Borgers, K. et al. Development of a counterselectable transposon to create markerless knockouts from an 18,432-clone ordered Mycobacterium bovis Bacillus Calmette-Guérin mutant resource. Msystems 5, e00180–20 (2020).
pubmed: 32788404
pmcid: 7426150
doi: 10.1128/mSystems.00180-20
Brosch, R. et al. A new evolutionary scenario for the Mycobacterium tuberculosis complex. Proc. Natl. Acad. Sci. USA 99, 3684–3689 (2002).
pubmed: 11891304
pmcid: 122584
doi: 10.1073/pnas.052548299
Lee, M. H., Pascopella, L., Jacobs, W. R. & Hatfull, G. F. Site-specific integration of mycobacteriophage L5: integration-proficient vectors for Mycobacterium smegmatis, Mycobacterium tuberculosis, and bacille Calmette-Guérin. Proc. Natl. Acad. Sci. USA 88, 3111–3115 (1991).
pubmed: 1901654
pmcid: 51395
doi: 10.1073/pnas.88.8.3111
Murphy, K. C. et al. ORBIT: a new paradigm for genetic engineering of mycobacterial chromosomes. Mbio 9, e01467–18 (2018).
pubmed: 30538179
pmcid: 6299477
doi: 10.1128/mBio.01467-18
Nguyen, P. P., Kado, T., Prithviraj, M., Siegrist, M. S. & Morita, Y. S. Inositol acylation of phosphatidylinositol mannosides: a rapid mass response to membrane fluidization in mycobacteria. J. Lipid Res. 63, 100262 (2022).
pubmed: 35952902
pmcid: 9490103
doi: 10.1016/j.jlr.2022.100262
Jankute, M. et al. Disruption of mycobacterial AftB results in complete loss of terminal β(1 → 2) arabinofuranose residues of lipoarabinomannan. ACS Chem. Biol. 12, 183–190 (2016).
pubmed: 28033704
pmcid: 5259755
doi: 10.1021/acschembio.6b00898
Birch, H. L. et al. Biosynthesis of mycobacterial arabinogalactan: identification of a novel α(1→3) arabinofuranosyltransferase. Mol. Microbiol. 69, 1191–1206 (2008).
pubmed: 18627460
pmcid: 2610374
doi: 10.1111/j.1365-2958.2008.06354.x
Škovierová, H. et al. AftD, a novel essential arabinofuranosyltransferase from mycobacteria. Glycobiology 19, 1235–1247 (2009).
pubmed: 19654261
pmcid: 2757576
doi: 10.1093/glycob/cwp116
Alderwick, L. J. et al. AftD functions as an α1→5 arabinofuranosyltransferase involved in the biosynthesis of the mycobacterial cell wall core. Cell Surf. 1, 2–14 (2018).
pubmed: 29998212
doi: 10.1016/j.tcsw.2017.10.001
Alderwick, L. J. et al. The C-terminal domain of the arabinosyltransferase Mycobacterium tuberculosis EmbC is a lectin-like carbohydrate binding module. PLoS Pathog. 7, e1001299 (2011).
pubmed: 21383969
pmcid: 3044687
doi: 10.1371/journal.ppat.1001299
Mishra, A. K. et al. Identification of an alpha(1->6) mannopyranosyltransferase (MptA), involved in Corynebacterium glutamicum lipomanann biosynthesis, and identification of its orthologue in Mycobacterium tuberculosis. Mol. Microbiol. 65, 1503–1517 (2007).
pubmed: 17714444
pmcid: 2157549
doi: 10.1111/j.1365-2958.2007.05884.x
Guerin, M. E. et al. Molecular recognition and interfacial catalysis by the essential phosphatidylinositol mannosyltransferase PimA from mycobacteria*. J. Biol. Chem. 282, 20705–20714 (2007).
pubmed: 17510062
doi: 10.1074/jbc.M702087200
Guerin, M. E., Korduláková, J., Alzari, P. M., Brennan, P. J. & Jackson, M. Molecular basis of phosphatidyl-myo-inositol mannoside biosynthesis and regulation in mycobacteria. J. Biol. Chem. 285, 33577–33583 (2010).
pubmed: 20801880
pmcid: 2962455
doi: 10.1074/jbc.R110.168328
Korduláková, J. et al. Definition of the first mannosylation step in phosphatidylinositol mannoside synthesis PimA is essential for growth of mycobacteria. J. Biol. Chem. 277, 31335–31344 (2002).
pubmed: 12068013
doi: 10.1074/jbc.M204060200
Tersa, M. et al. The molecular mechanism of substrate recognition and catalysis of the membrane acyltransferase PatA from mycobacteria. ACS Chem. Biol. 13, 131–140 (2018).
pubmed: 29185694
doi: 10.1021/acschembio.7b00578
Sparks, I. L., Kado, T., Prithviraj, M., Nijjer, J., Yan, J. & Morita, Y. S. Lipoarabinomannan mediates localized cell wall integrity during division in mycobacteria Nat Commun 15, 2191 (2024).
Lemassu, A. et al. Extracellular and surface-exposed polysaccharides of non-tuberculous mycobacteria. Microbiology 142, 1513–1520 (1996).
pubmed: 8704991
doi: 10.1099/13500872-142-6-1513
Rock, J. M. et al. Programmable transcriptional repression in mycobacteria using an orthogonal CRISPR interference platform. Nat. Microbiol. 2, 16274 (2017).
pubmed: 28165460
pmcid: 5302332
doi: 10.1038/nmicrobiol.2016.274
Yokoyama, K. & Ballou, C. E. Synthesis of alpha 1-6-mannooligosaccharides in Mycobacterium smegmatis. Function of beta-mannosylphosphoryldecaprenol as the mannosyl donor. J. Biol. Chem. 264, 21621–21628 (1989).
pubmed: 2480954
doi: 10.1016/S0021-9258(20)88230-1
Drula, E. et al. The carbohydrate-active enzyme database: functions and literature. Nucleic Acids Res. 50, D571–D577 (2021).
pmcid: 8728194
doi: 10.1093/nar/gkab1045
Khoo, K.-H., Dell, A., Morris, H. R., Breman, P. J. & Chatterjee, D. Structural definition of acylated phosphatidylinositol mannosides from Mycobacterium tuberculosis: definition of a common anchor for lipomannan and lipoarabinomannan. Glycobiology 5, 117–127 (1995).
pubmed: 7772860
doi: 10.1093/glycob/5.1.117
Kalscheuer, R., Weinrick, B., Veeraraghavan, U., Besra, G. S. & Jacobs, W. R. Trehalose-recycling ABC transporter LpqY-SugA-SugB-SugC is essential for virulence of Mycobacterium tuberculosis. Proc. Natl. Acad. Sci. USA 107, 21761–21766 (2010).
pubmed: 21118978
pmcid: 3003129
doi: 10.1073/pnas.1014642108
Pohane, A. A., Carr, C. R., Garhyan, J., Swarts, B. M. & Siegrist, M. S. Trehalose recycling promotes energy-efficient biosynthesis of the mycobacterial cell envelope. mBio 12, e02801–e02820 (2021).
pubmed: 33468692
pmcid: 7845637
doi: 10.1128/mBio.02801-20
Moynihan, P. J. et al. The hydrolase LpqI primes mycobacterial peptidoglycan recycling. Nat. Commun. 10, 2647 (2019).
pubmed: 31201321
pmcid: 6572805
doi: 10.1038/s41467-019-10586-2
Kumar, A.S. et al. Cloning and partial characterization of an endo-α-(1→6)-d-mannanase gene from Bacillus circulans. Int. J. Mol. Sci. 20, 6244 (2019).
doi: 10.3390/ijms20246244
Shukla, S. et al. Mycobacterium tuberculosis lipoprotein LprG binds lipoarabinomannan and determines its cell envelope localization to control phagolysosomal fusion. PLoS Pathog. 10, e1004471 (2014).
pubmed: 25356793
pmcid: 4214796
doi: 10.1371/journal.ppat.1004471
Alonso, H. et al. Protein O-mannosylation deficiency increases LprG-associated lipoarabinomannan release by Mycobacterium tuberculosis and enhances the TLR2-associated inflammatory response. Sci. Rep. 7, 7913 (2017).
pubmed: 28801649
pmcid: 5554173
doi: 10.1038/s41598-017-08489-7
Martinot, A. J. et al. Mycobacterial metabolic syndrome: LprG and Rv1410 regulate triacylglyceride levels, growth rate and virulence in Mycobacterium tuberculosis. PLoS Pathog. 12, e1005351 (2016).
pubmed: 26751071
pmcid: 4709180
doi: 10.1371/journal.ppat.1005351
Remm, S. et al. Structural basis for triacylglyceride extraction from mycobacterial inner membrane by MFS transporter Rv1410. Nat. Commun. 14, 6449 (2023).
pubmed: 37833269
pmcid: 10576003
doi: 10.1038/s41467-023-42073-0
Athman, J. J. et al. Bacterial membrane vesicles mediate the release of Mycobacterium tuberculosis lipoglycans and lipoproteins from infected macrophages. J. Immunol. 195, 1044–1053 (2015).
pubmed: 26109643
doi: 10.4049/jimmunol.1402894
Prados-Rosales, R. et al. Mycobacteria release active membrane vesicles that modulate immune responses in a TLR2-dependent manner in mice. J. Clin. Investig. 121, 1471–1483 (2011).
pubmed: 21364279
pmcid: 3069770
doi: 10.1172/JCI44261
Ortalo-Magné, A., Andersen, Å. B. & Daffé, M. The outermost capsular arabinomannans and other mannoconjugates of virulent and avirulent tubercle bacilli. Microbiology 142, 927–935 (1996).
pubmed: 8936319
doi: 10.1099/00221287-142-4-927
Chen, T. et al. Capsular glycan recognition provides antibody-mediated immunity against tuberculosis. J. Clin. Investig. 130, 1808–1822 (2020).
pubmed: 31935198
pmcid: 7108924
doi: 10.1172/JCI128459
Ishida, E. et al. Monoclonal antibodies from humans with Mycobacterium tuberculosis exposure or latent infection recognize distinct arabinomannan epitopes. Commun. Biol. 4, 1181 (2021).
pubmed: 34642445
pmcid: 8511196
doi: 10.1038/s42003-021-02714-w
Miller, B. H. & Shinnick, T. M. Identification of two Mycobacterium tuberculosis H37Rv ORFs involved in resistance to killing by human macrophages. BMC Microbiol. 1, 26 (2001).
pubmed: 11716786
pmcid: 59890
doi: 10.1186/1471-2180-1-26
Schirner, K., Marles‐Wright, J., Lewis, R. J. & Errington, J. Distinct and essential morphogenic functions for wall‐ and lipo‐teichoic acids in Bacillus subtilis. EMBO J. 28, 830–842 (2009).
pubmed: 19229300
pmcid: 2670855
doi: 10.1038/emboj.2009.25
Khatri, B. et al. High throughput phenotypic analysis of Mycobacterium tuberculosis and Mycobacterium bovis strains’ metabolism using biolog phenotype microarrays. PLoS ONE 8, e52673 (2013).
pubmed: 23326347
pmcid: 3542357
doi: 10.1371/journal.pone.0052673
Emsley, P., Lohkamp, B., Scott, W. G. & Cowtan, K. Features and development of Coot. Acta Crystallogr. Sect. D. Biol. Crystallogr. 66, 486–501 (2010).
doi: 10.1107/S0907444910007493
Meng, E. C. et al. UCSF ChimeraX: tools for structure building and analysis. Protein Sci. 32, e4792 (2023).
pubmed: 37774136
pmcid: 10588335
doi: 10.1002/pro.4792
Snapper, S. B., Melton, R. E., Mustafa, S., Kieser, T. & Jacobs, W. R. Jr. Isolation and characterization of efficient plasmid transformation mutants of Mycobacterium smegmatis. Mol. Microbiol. 4, 1911–1919 (1990).
pubmed: 2082148
doi: 10.1111/j.1365-2958.1990.tb02040.x
Driessen, N. N. et al. Role of phosphatidylinositol mannosides in the interaction between mycobacteria and DC-SIGN. Infect. Immun. 77, 4538–4547 (2009).
pubmed: 19651855
pmcid: 2747922
doi: 10.1128/IAI.01256-08
Ruhaak, L. R., Steenvoorden, E., Koeleman, C. A. M., Deelder, A. M. & Wuhrer, M. 2‐Picoline‐borane: a non‐toxic reducing agent for oligosaccharide labeling by reductive amination. PROTEOMICS 10, 2330–2336 (2010).
pubmed: 20391534
doi: 10.1002/pmic.200900804
Rappsilber, J., Mann, M. & Ishihama, Y. Protocol for micro-purification, enrichment, pre-fractionation and storage of peptides for proteomics using StageTips. Nat. Protoc. 2, 1896–1906 (2007).
pubmed: 17703201
doi: 10.1038/nprot.2007.261
Rappsilber, J., Ishihama, Y. & Mann, M. Stop and go extraction tips for matrix-assisted laser desorption/ionization, nanoelectrospray, and LC/MS sample pretreatment in proteomics. Anal. Chem. 75, 663–670 (2003).
pubmed: 12585499
doi: 10.1021/ac026117i
Teo, G. C., Polasky, D. A., Yu, F. & Nesvizhskii, A. I. Fast deisotoping algorithm and its implementation in the MSFragger search engine. J. Proteome Res. 20, 498–505 (2021).
pubmed: 33332123
doi: 10.1021/acs.jproteome.0c00544
Leprevost, F. et al. Philosopher: a versatile toolkit for shotgun proteomics data analysis. Nat. Methods 17, 869–870 (2020).
doi: 10.1038/s41592-020-0912-y
Geiszler, D. J. et al. PTM-Shepherd: analysis and summarization of post-translational and chemical modifications from open search results. Mol. Cell. Proteom. 20, 100018 (2021).
doi: 10.1074/mcp.TIR120.002216
Kong, A. T., Leprevost, F. V., Avtonomov, D. M., Mellacheruvu, D. & Nesvizhskii, A. I. MSFragger: ultrafast and comprehensive peptide identification in mass spectrometry-based proteomics. Nat. Methods 14, 513–520 (2017).
pubmed: 28394336
pmcid: 5409104
doi: 10.1038/nmeth.4256
Yu, F. et al. Identification of modified peptides using localization-aware open search. Nat. Commun. 11, 4065 (2020).
pubmed: 32792501
pmcid: 7426425
doi: 10.1038/s41467-020-17921-y
Tyanova, S. et al. The Perseus computational platform for comprehensive analysis of (prote)omics data. Nat. Methods 13, 731–740 (2016).
pubmed: 27348712
doi: 10.1038/nmeth.3901
Wattam, A. R. et al. PATRIC, the bacterial bioinformatics database and analysis resource. Nucleic Acids Res. 42, D581–D591 (2014).
pubmed: 24225323
doi: 10.1093/nar/gkt1099
Perez-Riverol, Y. et al. The PRIDE database resources in 2022: a hub for mass spectrometry-based proteomics evidences. Nucleic Acids Res. 50, D543–D552 (2021).
pmcid: 8728295
doi: 10.1093/nar/gkab1038