Illumination of growth, division and secretion by metabolic labeling of the bacterial cell surface

FEMS Microbiology Reviews

Volumn 39, Issue 2, 2015, Pages 184-202

  Siegrist, M Sloan ^a   Swarts, Benjamin M ^b   Fox, Douglas M ^a   Lim, Shion An ^a   Bertozzi, Carolyn R ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b CENTRAL MICHIGAN UNIVERSITY   (United States)

Author keywords

Bioorthogonal; Click chemistry; Glycolipid; Metabolic labeling; Peptidoglycan; Protein secretion

Indexed keywords

GLYCAN; LIPID;

BACTERIAL CELL; BACTERIAL GROWTH; BACTERIAL MEMBRANE; BACTERIAL SECRETION SYSTEM; CELL SURFACE; MACROMOLECULE; METABOLITE; NONHUMAN; REVIEW; BACTERIA; CELL MEMBRANE; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MICROBIOLOGICAL EXAMINATION; STAINING; TRENDS;

BACTERIA; BACTERIOLOGICAL TECHNIQUES; CELL MEMBRANE; STAINING AND LABELING;

EID: 84928211422     PISSN: 01686445     EISSN: 15746976     Source Type: Journal    
DOI: 10.1093/femsre/fuu012     Document Type: Review

References (184)

1. Abe R, Caaveiro JM, Kozuka-Hata H, et al. Mapping ultra-weak protein-protein interactions between heme transporters of Staphylococcus aureus. J Biol Chem 2012;287:16477-87.
2. Agard NJ, Prescher JA, Bertozzi CR. A strain-promoted [3 + 2] azide-alkyne cycloaddition for covalent modification of biomolecules in living systems. J Am Chem Soc 2004;126:15046-7.
3. Aldridge BB, Fernandez-Suarez M, Heller D, et al. Asymmetry and aging of mycobacterial cells lead to variable growth and antibiotic susceptibility. Science 2012;335:100-4.
4. Ali MM, Kang DK, Tsang K, et al. Cell-surface sensors: lighting the cellular environment. Wiley Interdiscip Rev Nanomed Nanobiotechnol 2012;4:547-61.
5. Alvarez L, Espaillat A, Hermoso JA, et al. Peptidoglycan remodeling by the coordinated action of multispecific enzymes. Microb Drug Resist 2014;20:190-8.
6. Antonczak AK, Simova Z, Tippmann EM. A critical examination of Escherichia coli esterase activity. J Biol Chem 2009;284:28795-800.
7. Backus KM, Boshoff HI, Barry CS, et al. Uptake of unnatural trehalose analogs as a reporter for Mycobacterium tuberculosis. Nat Chem Biol 2011;7:228-35.
8. Bansal-Mutalik R, Nikaido H. Mycobacterial outer membrane is a lipid bilayer and the inner membrane is unusually rich in diacyl phosphatidylinositol dimannosides. P Natl Acad Sci USA 2014;111:4958-63.
9. Bardou F, Quemard A, Dupont MA, et al. Effects of isoniazid on ultrastructure of Mycobacterium aurum and Mycobacterium tuberculosis and on production of secreted proteins. Antimicrob Agents Ch 1996;40:2459-67.
10. Barreteau H, Kovac A, Boniface A, et al. Cytoplasmic steps of peptidoglycan biosynthesis. FEMS Microbiol Rev 2008;32:168-207.
11. Barry CE, 3rd, Boshoff HI, Dartois V, et al. The spectrum of latent tuberculosis: rethinking the biology and intervention strategies. Nat Rev Microbiol 2009;7:845-55.
12. Baskin JM, Prescher JA, Laughlin ST, et al. Copper-free click chemistry for dynamic in vivo imaging. P Natl Acad Sci USA 2007;104:16793-7.
13. Beckwith J. The Sec-dependent pathway. Res Microbiol 2013;164:497-504.
14. Belisle JT, Vissa VD, Sievert T, et al. Role of the major antigen of Mycobacterium tuberculosis in cell wall biogenesis. Science 1997;276:1420-2.
15. Bensing BA, Yen YT, Seepersaud R, et al. A specific interaction between SecA2 and a region of the preprotein adjacent to the signal peptide occurs during transport via the accessory Sec system. J Biol Chem 2012;287:24438-47.
16. Besanceney-Webler C, Jiang H, Wang W, et al. Metabolic labeling of fucosylated glycoproteins in Bacteroidales species. Bioorg Med Chem Lett 2011;21:4989-92.
17. Birdsell DC, Cota-Robles EH. Production and ultrastructure of lysozyme and ethylenediaminetetraacetatelysozyme spheroplasts of Escherichia coli. J Bacteriol 1967;93:427-37.
18. Blackman ML, Royzen M, Fox JM. Tetrazine ligation: fast bioconjugation based on inverse-electron-demand Diels-Alder reactivity. J Am Chem Soc 2008;130:13518-9.
19. Boneca IG. The role of peptidoglycan in pathogenesis. Curr Opin Microbiol 2005;8:46-53.
20. Bouley DM, Ghori N, Mercer KL, et al. Dynamic nature of hostpathogen interactions in Mycobacterium marinum granulomas. Infect Immun 2001;69:7820-31.
21. Brown PJ, de Pedro MA, Kysela DT, et al. Polar growth in the Alphaproteobacterial order Rhizobiales. P Natl Acad Sci USA 2012;109:1697-701.
22. Bunschoten A, Welling MM, Termaat MF, et al. Development and prospects of dedicated tracers for the molecular imaging of bacterial infections. Bioconjugate Chem 2013;24:1971-89.
23. Burnaevskiy N, Fox TG, Plymire DA, et al. Proteolytic elimination of N-myristoylmodifications by the Shigella virulence factor IpaJ. Nature 2013;496:106-9.
24. Butland G, Peregrin-Alvarez JM, Li J, et al. Interaction network containing conserved and essential protein complexes in Escherichia coli. Nature 2005;433:531-7.
25. Cabeen MT, Jacobs-Wagner C. Bacterial cell shape. Nat Rev Microbiol 2005;3:601-10.
26. Cameron TA, Anderson-Furgeson J, Zupan JR, et al. Peptidoglycan synthesis machinery in Agrobacterium tumefaciens during unipolar growth and cell division. mBio 2014;5:e01219-14.
27. Caparros M, Pisabarro AG, de Pedro MA. Effect of D-amino acids on structure and synthesis of peptidoglycan in Escherichia coli. J Bacteriol 1992;174:5549-59.
28. Carel C, Nukdee K, Cantaloube S, et al. Mycobacterium tuberculosis proteins involved in mycolic acid synthesis and transport localize dynamically to the old growing pole and septum. PLoS One 2014;9:e97148.
29. Cava F, de Pedro MA, Lam H, et al. Distinct pathways for modification of the bacterial cell wall by non-canonical D-amino acids. EMBO J 2011;30:3442-53.
30. Cava F, Kuru E, Brun YV, et al. Modes of cell wall growth differentiation in rod-shaped bacteria. Curr Opin Microbiol 2013;16:731-7.
31. Cava F, Lam H, de Pedro MA, et al. Emerging knowledge of regulatory roles of D-amino acids in bacteria. Cell Mol Life Sci 2011;68:817-31.
32. Champasa K, Longwell SA, Eldridge AM, et al. Targeted identification of glycosylated proteins in the gastric pathogen Helicobacter pylori (Hp). Mol Cell Proteomics 2013;12:2568-86.
33. Chan J, Dodani SC, Chang CJ. Reaction-based small-molecule fluorescent probes for chemoselective bioimaging. Nat Chem 2012;4:973-84.
34. Chauhan A, Lofton H, Maloney E, et al. Interference of Mycobacterium tuberculosis cell division by Rv2719c, a cell wall hydrolase. Mol Microbiol 2006;62:132-47.
35. Check Hayden E. 'Killer application' for protein synthesis is retracted. Nature 2009;462:707.
36. Chopra I, Storey C, Falla TJ, et al. Antibiotics, peptidoglycan synthesis and genomics: the chlamydial anomaly revisited. Microbiology 1998;144(Pt 10):2673-8.
37. Crawford JM, Portmann C, Zhang X, et al. Smallmolecule perimeter defense in entomopathogenic bacteria. P Natl Acad Sci USA 2012;109:10821-6.
38. Crimmins GT, Isberg RR. Analyzingmicrobial disease at high resolution: following the fate of the bacterium during infection. Curr Opin Microbiol 2012;15:23-7.
39. Dahl JL. Electron microscopy analysis of Mycobacterium tuberculosis cell division. FEMS Microbiol Lett 2004;240:15-20.
40. Daniel RA, Errington J. Control of cell morphogenesis in bacteria: two distinct ways to make a rod-shaped cell. Cell 2003;113:767-76.
41. Das S, Oliver DB. Mapping of the SecA. SecY and SecA. SecG interfaces by site-directed in vivo photocross-linking. J Biol Chem 2011;286:12371-80.
42. de Pedro MA, Grunfelder CG, Schwarz H. Restricted mobility of cell surface proteins in the polar regions of Escherichia coli. J Bacteriol 2004;186:2594-602.
43. de Pedro MA, Quintela JC, Holtje JV, et al. Murein segregation in Escherichia coli. J Bacteriol 1997;179:2823-34.
44. Desmarais SM, De Pedro MA, Cava F, et al. Peptidoglycan at its peaks: how chromatographic analyses can reveal bacterial cell wall structure and assembly. Mol Microbiol 2013;89:1-13.
45. Dommerholt J, Schmidt S, Temming R, et al. Readily accessible bicyclononynes for bioorthogonal labeling and threedimensional imaging of living cells. Angew Chem Int Edit 2010;49:9422-5.
46. Dube DH, Champasa K, Wang B. Chemical tools to discover and target bacterial glycoproteins. Chem Commun (Camb) 2011;47:87-101.
47. Dumont A, Malleron A, Awwad M, et al. Click-mediated labeling of bacterial membranes through metabolic modification of the lipopolysaccharide inner core. Angew Chem Int Edit 2012;51:3143-6.
48. Egan AJ, Vollmer W. The physiology of bacterial cell division. Ann NY Acad Sci 2013;1277:8-28.
49. Eun YJ, Zhou M, Kiekebusch D, et al. Divin: a small molecule inhibitor of bacterial divisome assembly. J Am Chem Soc 2013;135:9768-76.
50. Feltcher ME, BraunsteinM. Emerging themes in SecA2-mediated protein export. Nat Rev Microbiol 2012;10:779-89.
51. Fenton AK, Gerdes K. Direct interaction of FtsZ and MreB is required for septum synthesis and cell division in Escherichia coli. EMBO J 2013;32:1953-65.
52. Fleurie A, Manuse S, Zhao C, et al. Interplay of the serine/threonine-kinase StkP and the paralogs DivIVA and GpsB in pneumococcal cell elongation and division. PLoS Genet 2014;10:e1004275.
53. Foss MH, Eun YJ, Weibel DB. Chemical-biological studies of subcellular organization in bacteria. Biochemistry 2011;50:7719-34.
54. Frirdich E, Gaynor EC. Peptidoglycan hydrolases, bacterial shape, and pathogenesis. Curr Opin Microbiol 2013;16:767-78.
55. Frobel J, Rose P, Muller M. Early contacts between substrate proteins and TatA translocase component in twin-arginine translocation. J Biol Chem 2011;286:43679-89.
56. Fura JM, Sabulski MJ, Pires MM. D-amino acid mediated recruitment of endogenous antibodies to bacterial surfaces. ACS Chem Biol 2014;9:1480-9.
57. Galan JE. Common themes in the design and function of bacterial effectors. Cell Host Microbe 2009;5:571-9.
58. Gautam S, Gniadek TJ, Kim T, et al. Exterior design: strategies for redecorating the bacterial surface with small molecules. Trends Biotechnol 2013;31:258-67.
59. Ghosh AS, Young KD. Helical disposition of proteins and lipopolysaccharide in the outer membrane of Escherichia coli. J Bacteriol 2005;187:1913-22.
60. Ghuysen JM, Goffin C. Lack of cell wall peptidoglycan versus penicillin sensitivity: new insights into the chlamydial anomaly. Antimicrob Agents Ch 1999;43:2339-44.
61. Gibbs KA, Isaac DD, Xu J, et al. Complex spatial distribution and dynamics of an abundant Escherichia coli outer membrane protein, LamB. Mol Microbiol 2004;53:1771-83.
62. Gill WP, Harik NS, Whiddon MR, et al. A replication clock for Mycobacterium tuberculosis. Nat Med 2009;15:211-4.
63. Goodman AL, McNulty NP, Zhao Y, et al. Identifying genetic determinants needed to establish a human gut symbiont in its habitat. Cell Host Microbe 2009;6:279-89.
64. Gouzy A, Larrouy-Maumus G, Wu TD, et al. Mycobacterium tuberculosis nitrogen assimilation and host colonization require aspartate. Nat Chem Biol 2013;9:674-6.
65. Grammel M, Hang HC. Chemical reporters for biological discovery. Nat Chem Biol 2013;9:475-84.
66. Grammel M, Luong P, Orth K, et al. A chemical reporter for protein AMPylation. J Am Chem Soc 2011;133:17103-5.
67. Hatzenpichler R, Scheller S, Tavormina PL, et al. In situ visualization of newly synthesized proteins in environmental microbes using amino acid tagging and click chemistry. Environ Microbiol 2014;16:2568-90.
68. Helaine S, Holden DW. Heterogeneity of intracellular replication of bacterial pathogens. Curr Opin Microbiol 2013;16:184-91.
69. Hett EC, Rubin EJ. Bacterial growth and cell division: a mycobacterial perspective. Microbiol Mol Biol Rev 2008;72:126-56.
70. Hicks SW, Charron G, Hang HC, et al. Subcellular targeting of Salmonella virulence proteins by host-mediated Spalmitoylation. Cell Host Microbe 2011;10:9-20.
71. Ho BT, Dong TG, Mekalanos JJ. A view to a kill: the bacterial type VI secretion system. Cell Host Microbe 2014;15:9-21.
72. Hocking J, Priyadarshini R, Takacs CN, et al. Osmolality-dependent relocation of penicillin-binding protein PBP2 to the division site in Caulobacter crescentus. J Bacteriol 2012;194:3116-27.
73. Hopf PS, Ford RS, Zebian N, et al. rotein glycosylation in Helicobacter pylori: beyond the flagellins? PLoS One 2011;6:e25722.
74. Hu P, Janga SC, Babu M, et al. Global functional atlas of Escherichia coli encompassing previously uncharacterized proteins. PLoS Biol 2009;7:e96.
75. Ieva R, Tian P, Peterson JH, et al. Sequential and spatially restricted interactions of assembly factors with an autotransporter beta domain. P Natl Acad Sci USA 2011;108:E383-391.
76. Indrigo J, Hunter RL, Jr, Actor JK. Cord factor trehalose 6,6'-dimycolate (TDM) mediates trafficking events during mycobacterial infection of murine macrophages. Microbiology 2003;149:2049-59.
77. Ivanov SS, Charron G, Hang HC, et al. Lipidation by the host prenyltransferase machinery facilitates membrane localization of Legionella pneumophila effector proteins. J Biol Chem 2010;285:34686-98.
78. Jacquier N, Frandi A, Pillonel T, et al. Cell wall precursors are required to organize the chlamydial division septum. Nat Commun 2014;5:3578.
79. Jewett JC, Sletten EM, Bertozzi CR. Rapid Cu-free click chemistry with readily synthesized biarylazacyclooctynones. J Am Chem Soc 2010;132:3688-90.
80. Jiang C, Brown PJ, Ducret A, et al. Sequential evolution of bacterial morphology by co-option of a developmental regulator. Nature 2014;506:489-93.
81. Joyce G, Williams KJ, Robb M, et al. Cell division site placement and asymmetric growth in mycobacteria. PLoS One 2012;7:e44582.
82. Justice SS, Hunstad DA, Cegelski L, et al. Morphological plasticity as a bacterial survival strategy. Nat Rev Microbiol 2008;6:162-8.
83. Kaewsapsak P, Esonu O, Dube DH. Recruiting the host's immune system to target Helicobacter pylori's surface glycans. Chembiochem 2013;14:721-6.
84. Kieser KJ, Rubin EJ. How sisters grow apart: mycobacterial growth and division. Nat Rev Microbiol 2014;12:550-62.
85. Koenigs MB, Richardson EA, Dube DH. Metabolic profiling of Helicobacter pylori glycosylation. Mol Biosyst 2009;5:909-12.
86. Kumar P, Arora K, Lloyd JR, et al. Meropenem inhibits D, Dcarboxypeptidase activity in Mycobacterium tuberculosis. Mol Microbiol 2012;86:367-81.
87. Kuru E, Hughes HV, Brown PJ, et al. In Situ probing of newly synthesized peptidoglycan in live bacteria with fluorescent Damino acids. Angew Chem Int Edit 2012;51:12519-23.
88. Kysela DT, Brown PJ, Huang KC, et al. Biological consequences and advantages of asymmetric bacterial growth. Annu Rev Microbiol 2013;67:417-35.
89. Lam H, Oh DC, Cava F, et al. D-amino acids govern stationary phase cellwall remodeling in bacteria. Science 2009;325:1552-5.
90. Lavollay M, Arthur M, Fourgeaud M, et al. The peptidoglycan of stationary-phase Mycobacterium tuberculosis predominantly contains cross-links generated by L, D-transpeptidation. J Bacteriol 2008;190:4360-6.
91. Lavollay M, Fourgeaud M, Herrmann JL, et al. The peptidoglycan of Mycobacterium abscessus is predominantly cross-linked by L, D-transpeptidases. J Bacteriol 2011;193:778-82.
92. Lebar MD, May JM, Meeske AJ, et al. Reconstitution of peptidoglycan cross-linking leads to improved fluorescent probes of cell wall synthesis. J Am Chem Soc 2014;136:10874-7.
93. Lederberg J, St Clair J. Protoplasts and L-type growth of Escherichia coli. J Bacteriol 1958;75:143-60.
94. Leyh-Bouille M, Bonaly R, Ghuysen JM, et al. LL-diaminopimelic acid containing peptidoglycans in walls of Streptomyces sp. and of Clostridium perfringens (type A). Biochemistry 1970;9:2944-52.
95. Li N, Overkleeft HS, Florea BI. Activity-based protein profiling: an enabling technology in chemical biology research. Curr Opin Chem Biol 2012;16:227-33.
96. Liechti GW, Kuru E, Hall E, et al. A new metabolic cell-wall labelling method reveals peptidoglycan in Chlamydia trachomatis. Nature 2013;506:507-10.
97. Lin S, Zhang Z, Xu H, et al. Site-specific incorporation of photocross-linker and bioorthogonal amino acids into enteric bacterial pathogens. J Am Chem Soc 2011;133:20581-7.
98. Link AJ, Tirrell DA. Cell surface labeling of Escherichia coli via copper(I)-catalyzed [3+2] cycloaddition. J Am Chem Soc 2003;125:11164-5.
99. Link AJ, Vink MK, Agard NJ, et al. Discovery of aminoacyl-tRNA synthetase activity through cell-surface display of noncanonical amino acids. P Natl Acad Sci USA 2006;103:10180-5.
100. Link AJ, Vink MK, Tirrell DA. Presentation and detection of azide functionality in bacterial cell surface proteins. J Am Chem Soc 2004;126:10598-602.
101. Liu F, Aubry AJ, Schoenhofen IC, et al. The engineering of bacteria bearing azido-pseudaminic acid-modified flagella. Chembiochem 2009;10:1317-20.
102. Luchansky SJ, Hang HC, Saxon E, et al. Constructing azidelabeled cell surfaces using polysaccharide biosynthetic pathways. Method Enzymol 2003;362:249-72.
103. Lupoli TJ, Tsukamoto H, Doud EH, et al. Transpeptidase-mediated incorporation of D-amino acids into bacterial peptidoglycan. J Am Chem Soc 2011;133:10748-51.
104. McCoy AJ, Maurelli AT. Building the invisible wall: updating the chlamydial peptidoglycan anomaly. Trends Microbiol 2006;14:70-7.
105. Mahdavi A, Szychowski J, Ngo JT, et al. Identification of secreted bacterial proteins by noncanonical amino acid tagging. P Natl Acad Sci USA 2014;111:433-8.
106. Makarov V, Manina G, Mikusova K, et al. Benzothiazinones kill Mycobacterium tuberculosis by blocking arabinan synthesis. Science 2009;324:801-4.
107. Mandon EC, Trueman SF, Gilmore R. Translocation of proteins through the Sec61 and SecYEG channels. Curr Opin Cell Biol 2009;21:501-7.
108. Manina G, McKinney JD. A single-cell perspective on nongrowing but metabolically active (NGMA) bacteria. Curr Top Microbiol Immunol 2013;374:135-61.
109. Mas Pons J, Dumont A, Sautejeau G, et al. Identification of living Legionella pneumophila using species-specific metabolic lipopolysaccharide labeling. Angew Chem Int Edit 2014;53:1275-8.
110. Memmel E, Homann A, Oelschlaeger TA, et al. Metabolic glycoengineering of Staphylococcus aureus reduces its adherence to human T24 bladder carcinoma cells. Chem Commun (Camb) 2013;49:7301-3.
111. Meniche X, Otten R, Siegrist MS, et al. Subpolar addition of new cell wall is directed by DivIVA in mycobacteria. P Natl Acad Sci USA 2014;111:E3243-51.
112. Meyer P, Gutierrez J, Pogliano K, et al. Cell wall synthesis is necessary for membrane dynamics during sporulation of Bacillus subtilis. Mol Microbiol 2010;76:956-70.
113. Mohammadi T, Breukink E. The chlamydial anomaly clarified? Chembiochem 2014;15:1391-2.
114. Mori H, Ito K. Differentmodes of SecY-SecA interactions revealed by site-directed in vivo photo-cross-linking. P Natl Acad Sci USA 2006;103:16159-64.
115. Moulder JW. Why is Chlamydia sensitive to penicillin in the absence of peptidoglycan? Infect Agent Dis 1993;2:87-99.
116. Muhlradt PF, Menzel J, Golecki JR, et al. Outer membrane of salmonella. Sites of export of newly synthesised lipopolysaccharide on the bacterial surface. Eur J Biochem 1973;35:471-81.
117. Nelson JW, Chamessian AG, McEnaney PJ, et al. A biosynthetic strategy for re-engineering the Staphylococcus aureus cell wall with non-native smallmolecules. ACS Chem Biol 2010;5:1147-55.
118. Ngo JT, Tirrell DA. Noncanonical amino acids in the interrogation of cellular protein synthesis. Accounts Chem Res 2011;44:677-85.
119. Nickerson NN, Mainprize IL, Hampton L, et al. Trapped translocation intermediates establish the route for export of capsular polysaccharides across Escherichia coli outer membranes. P Natl Acad Sci USA 2014;111:8203-8.
120. Ning X, Guo J, Wolfert MA, et al. Visualizing metabolically labeled glycoconjugates of living cells by copper-free and fast huisgen cycloadditions. Angew Chem Int Edit 2008;47:2253-5.
121. Okuda S, Freinkman E, Kahne D. Cytoplasmic ATP hydrolysis powers transport of lipopolysaccharide across the periplasm in E. coli. Science 2012;338:1214-7.
122. Okuda S, Tokuda H. Model of mouth-to-mouth transfer of bacterial lipoproteins through inner membrane Lol C, periplasmic Lol A, and outer membrane LolB. P Natl Acad Sci USA 2009;106:5877-82.
123. Olrichs NK, Aarsman ME, Verheul J, et al. A novel in vivo cell-wall labeling approach sheds new light on peptidoglycan synthesis in Escherichia coli. Chembiochem 2011;12:1124-33.
124. Park JT. Identification of a dedicated recycling pathway for anhydro-N-acetylmuramic acid and N-acetylglucosamine derived from Escherichia coli cell wall murein. J Bacteriol 2001;183:3842-7.
125. Patterson DM, Nazarova LA, Prescher JA. Finding the right (bioorthogonal) chemistry. ACS Chem Biol 2014;9:592-605.
126. Patterson DM, Nazarova LA, Xie B, et al. Functionalized cyclopropenes as bioorthogonal chemical reporters. J Am Chem Soc 2012;134:18638-43.
127. Pavlova O, Ieva R, Bernstein HD. Monitoring the assembly of a secreted bacterial virulence factor using site-specific crosslinking. J Vis Exp 2013;17:e51217.
128. Peltier J, Courtin P, El Meouche I, et al. Clostridium difficile has an original peptidoglycan structure with a high level of N-acetylglucosamine deacetylation and mainly 3-3 cross-links. J Biol Chem 2011;286:29053-62.
129. Pham ND, Parker RB, Kohler JJ. Photocrosslinking approaches to interactome mapping. Curr Opin Chem Biol 2013;17:90-101.
130. Philpott DJ, Sorbara MT, Robertson SJ, et al. NOD proteins: regulators of inflammation in health and disease. Nat Rev Immunol 2014;14:9-23.
131. Pilhofer M, Aistleitner K, Biboy J, et al. Discovery of chlamydial peptidoglycan reveals bacteria withmurein sacculi but without FtsZ. Nat Commun 2013;4:2856.
132. Pinho MG, Kjos M, Veening JW. Howto get (a)round: mechanisms controlling growth and division of coccoid bacteria. Nat Rev Microbiol 2013;11:601-14.
133. Preston GW, Wilson AJ. Photo-induced covalent cross-linking for the analysis of biomolecular interactions. Chem Soc Rev 2013;42:3289-301.
134. Rafelski SM, Theriot JA. Mechanism of polarization of Listeria monocytogenes surface protein ActA. Mol Microbiol 2006;59:1262-79.
135. Rangan KJ, Yang YY, Charron G, et al. Rapid visualization and large-scale profiling of bacterial lipoproteins with chemical reporters. J Am Chem Soc 2010;132:10628-9.
136. Ranjit DK, Young KD. The Rcs stress response and accessory envelope proteins are required for de novo generation of cell shape in Escherichia coli. J Bacteriol 2013;195:2452-62.
137. Rostovtsev VV, Green LG, Fokin VV, et al. A stepwise huisgen cycloaddition process: copper(I)-catalyzed regioselective 'ligation' of azides and terminal alkynes. Angew Chem Int Edit 2002;41:2596-9.
138. Russell AB, Peterson SB, Mougous JD. Type VI secretion system effectors: poisons with a purpose. Nat Rev Microbiol 2014;12:137-48.
139. Sachelaru I, Petriman NA, Kudva R, et al. YidC occupies the lateral gate of the SecYEG translocon and is sequentially displaced by a nascent membrane protein. J Biol Chem 2013;288:16295-307.
140. Santi I, Dhar N, Bousbaine D, et al. Single-cell dynamics of the chromosome replication and cell division cycles inmycobacteria. Nat Commun 2013;4:2470.
141. Sathyamoorthy N, Takayama K. Purification and characterization of a novelmycolic acid exchange enzyme from Mycobacterium smegmatis. J Biol Chem 1987;262:13417-23.
142. Saxon E, Bertozzi CR. Cell surface engineering by a modified Staudinger reaction. Science 2000;287:2007-10.
143. Schindler M, Osborn MJ, Koppel DE. Lateral diffusion of lipopolysaccharide in the outer membrane of Salmonella typhimurium. Nature 1980;285:261-3.
144. Schirm M, Soo EC, Aubry AJ, et al. Structural, genetic and functional characterization of the flagellin glycosylation process in Helicobacter pylori. Mol Microbiol 2003;48:1579-92.
145. Sham LT, Tsui HC, Land AD, et al. Recent advances in pneumococcal peptidoglycan biosynthesis suggest new vaccine and antimicrobial targets. Curr Opin Microbiol 2012;15:194-203.
146. Shieh P, Siegrist MS, Cullen AJ, et al. Imaging bacterial peptidoglycan with near-infrared fluorogenic azide probes. P Natl Acad Sci USA 2014;111:5456-61.
147. Siegrist MS, Whiteside S, Jewett JC, et al. (D)-amino acid chemical reporters reveal peptidoglycan dynamics of an intracellular pathogen. ACS Chem Biol 2013;8:500-5.
148. Singh B, Nitharwal RG, Ramesh M, et al. Asymmetric growth and division in Mycobacterium spp.: compensatory mechanisms for non-medial septa. Mol Microbiol 2013;88:64-76.
149. Sjollema KA, Schnell U, Kuipers J, et al. Correlated light microscopy and electron microscopy. Method Cell Biol 2012;111:157-73.
150. Solomon JM, Leung GS, Isberg RR. Intracellular replication of Mycobacterium marinum within Dictyostelium discoideum: efficient replication in the absence of host coronin. Infect Immun 2003;71:3578-86.
151. Spargo BJ, Crowe LM, Ioneda T, et al. Cord factor (alpha, alpha-trehalose 6,6'-dimycolate) inhibits fusion between phospholipid vesicles. P Natl Acad Sci USA 1991;88:737-40.
152. Swarts BM, Holsclaw CM, Jewett JC, et al. Probing themycobacterial trehalome with bioorthogonal chemistry. J Am Chem Soc 2012;134:16123-6.
153. Swulius MT, Jensen GJ. The helical MreB cytoskeleton in Escherichia coli MC1000/pLE7 is an artifact of the N-Terminal yellow fluorescent protein tag. J Bacteriol 2012;194:6382-6.
154. Takade A, Takeya K, Taniguchi H, et al. Electron microscopic observations of cell division in Mycobacterium vaccae V1. J Gen Microbiol 1983;129:2315-20.
155. Tan Q, Awano N, Inouye M. YeeV is an Escherichia coli toxin that inhibits cell division by targeting the cytoskeleton proteins, FtsZ and MreB. Mol Microbiol 2011;79:109-18.
156. Tanrikulu IC, Schmitt E, Mechulam Y, et al. Discovery of Escherichia coli methionyl-tRNA synthetase mutants for efficient labeling of proteins with azidonorleucine in vivo. P Natl Acad Sci USA 2009;106:15285-90.
157. Thanky NR, Young DB, Robertson BD. Unusual features of the cell cycle in mycobacteria: polar-restricted growth and the snapping-model of cell division. Tuberculosis (Edinb) 2007;87:231-6.
158. Thompson RJ, Bouwer HG, Portnoy DA, et al. Pathogenicity and immunogenicity of a Listeria monocytogenes strain that requires D-alanine for growth. Infect Immun 1998;66:3552-61.
159. Tiyanont K, Doan T, Lazarus MB, et al. Imaging peptidoglycan biosynthesis in Bacillus subtilis with fluorescent antibiotics. P Natl Acad Sci USA 2006;103:11033-8.
160. Tocheva EI, Lopez-Garrido J, Hughes HV, et al. Peptidoglycan transformations during Bacillus subtilis sporulation. Mol Microbiol 2013;88:673-86.
161. Tornoe CW, Christensen C, Meldal M. Peptidotriazoles on solid phase: [1,2,3]-triazoles by regiospecific copper(i)-catalyzed 1,3-dipolar cycloadditions of terminal alkynes to azides. J Org Chem 2002;67:3057-64.
162. Tra VN, Dube DH. Glycans in pathogenic bacteria-potential for targeted covalent therapeutics and imaging agents. Chem Commun (Camb) 2014;50:4659-73.
163. Tsuruoka T, Tamura A, Miyata A, et al. Penicillin-insensitive incorporation of D-amino acids into cell wall peptidoglycan influences the amount of bound lipoprotein in Escherichia coli. J Bacteriol 1984;160:889-94.
164. Typas A, Banzhaf M, Gross CA, et al. From the regulation of peptidoglycan synthesis to bacterial growth and morphology. Nat Rev Microbiol 2012;10:123-36.
165. Urbanek BL, Wing DC, Haislop KS, et al. Chemoenzymatic synthesis of trehalose analogues: rapid access to chemical probes for investigating mycobacteria. Chembiochem 2014;15:2066-70.
166. Ursell TS, Trepagnier EH, Huang KC, et al. Analysis of surface protein expression reveals the growth pattern of the gram-negative outer membrane. PLoS Comput Biol 2012;8: e1002680.
167. van Dam V, Olrichs N, Breukink E. Specific labeling of peptidoglycan precursors as a tool for bacterial cell wall studies. Chembiochem 2009;10:617-24.
168. Wakamoto Y, Dhar N, Chait R, et al. Dynamic persistence of antibiotic-stressed mycobacteria. Science 2013;339:91-5.
169. Watrous JD, Dorrestein PC. Imaging mass spectrometry in microbiology. Nat Rev Microbiol 2011;9:683-94.
170. Watrous JD, Phelan VV, Hsu CC, et al. Microbial metabolic exchange in 3D. ISME J 2013;7:770-80.
171. Wei L, Hu F, Shen Y, et al. Live-cell imaging of alkyne-tagged small biomolecules by stimulated Raman scattering. Nat Methods 2014;11:410-2.
172. Wietzerbin J, Das BC, Petit JF, et al. Occurrence of D-alanyl-(D)-meso-diaminopimelic acid and meso-diaminopimelylmeso-diaminopimelic acid interpeptide linkages in the peptidoglycan of Mycobacteria. Biochemistry 1974;13:3471-6.
173. Winther T, Xu L, Berg-Sorensen K, et al. Effect of energy metabolism on protein motility in the bacterial outer membrane. Biophys J 2009;97:1305-12.
174. Xu R, Hanson SR, Zhang Z, et al. Site-specific incorporation of the mucin-type N-acetylgalactosamine-alpha-O-threonine into protein in Escherichia coli. J Am Chem Soc 2004;126:15654-5.
175. Yang J, Seckute J, Cole CM, et al. Live-cell imaging of cyclopropene tags with fluorogenic tetrazine cycloadditions. Angew Chem Int Edit 2012;51:7476-9.
176. Yang M, Song Y, Zhang M, et al. Converting a solvatochromic fluorophore into a protein-based pH indicator for extreme acidity. Angew Chem Int Edit 2012;51:7674-9.
177. Yi W, Liu X, Li Y, et al. Remodeling bacterial polysaccharides by metabolic pathway engineering. P Natl Acad Sci USA 2009;106:4207-12.
178. Young KD. The selective value of bacterial shape. Microbiol Mol Biol Rev 2006;70:660-703.
179. Yu D, Wowor AJ, Cole JL, et al. Defining the Escherichia coli SecA dimer interface residues through in vivo site-specific photocross-linking. J Bacteriol 2013;195:2817-25.
180. Zhang M, Lin S, Song X, et al. A genetically incorporated crosslinker reveals chaperone cooperation in acid resistance. Nat Chem Biol 2011;7:671-7.
181. Zhang Z, Gildersleeve J, Yang YY, et al. A new strategy for the synthesis of glycoproteins. Science 2004;303:371-3.
182. Zhang Z, Smith BA, Wang L, et al. A new strategy for the site-specific modification of proteins in vivo. Biochemistry 2003;42:6735-46.
183. Zinder ND, Arndt WF. Production of protoplasts of Escherichia Coli by lysozyme treatment. P Natl Acad Sci USA 1956;42:586-90.
184. Zoufaly S, Frobel J, Rose P, et al. Mapping precursor-binding site on TatC subunit of twin arginine-specific protein translocase by site-specific photo cross-linking. J Biol Chem 2012;287:13430-41.