1932

Abstract

Complex carbohydrates are essential for many biological processes, from protein quality control to cell recognition, energy storage, and cell wall formation. Many of these processes are performed in topologically extracellular compartments or on the cell surface; hence, diverse secretion systems evolved to transport the hydrophilic molecules to their sites of action. Polyprenyl lipids serve as ubiquitous anchors and facilitators of these transport processes. Here, we summarize and compare bacterial biosynthesis pathways relying on the recognition and transport of lipid-linked complex carbohydrates. In particular, we compare transporters implicated in O antigen and capsular polysaccharide biosyntheses with those facilitating teichoic acid and -linked glycan transport. Further, we discuss recent insights into the generation, recognition, and recycling of polyprenyl lipids.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-biochem-011520-104707
2020-06-20
2024-06-18
Loading full text...

Full text loading...

/deliver/fulltext/biochem/89/1/annurev-biochem-011520-104707.html?itemId=/content/journals/10.1146/annurev-biochem-011520-104707&mimeType=html&fmt=ahah

Literature Cited

  1. 1. 
    Touzé T, Mengin-Lecreulx D. 2008. Undecaprenyl phosphate synthesis. EcoSal Plus 3: https://doi.org/10.1128/ecosalplus.4.7.1.7
    [Crossref] [Google Scholar]
  2. 2. 
    Manat G, Roure S, Auger R, Bouhss A, Barreteau H et al. 2014. Deciphering the metabolism of undecaprenyl-phosphate: the bacterial cell-wall unit carrier at the membrane frontier. Microb. Drug Resist. 20:199–214
    [Google Scholar]
  3. 3. 
    Eichler J, Guan Z. 2017. Lipid sugar carriers at the extremes: the phosphodolichols Archaea use in N-glycosylation. Biochim. Biophys. Acta Mol. Cell Biol. Lipids 1862:589–99
    [Google Scholar]
  4. 4. 
    Surmacz L, Swiezewska E. 2011. Polyisoprenoids—Secondary metabolites or physiologically important superlipids. Biochem. Biophys. Res. Commun. 407:627–32
    [Google Scholar]
  5. 5. 
    El Ghachi M, Howe N, Huang CY, Olieric V, Warshamanage R et al. 2018. Crystal structure of undecaprenyl-pyrophosphate phosphatase and its role in peptidoglycan biosynthesis. Nat. Commun. 9:1078
    [Google Scholar]
  6. 6. 
    Workman SD, Worrall LJ, Strynadka NCJ 2018. Crystal structure of an intramembranal phosphatase central to bacterial cell-wall peptidoglycan biosynthesis and lipid recycling. Nat. Commun. 9:1159
    [Google Scholar]
  7. 7. 
    Vergara-Jaque A, Fenollar-Ferrer C, Kaufmann D, Forrest LR 2015. Repeat-swap homology modeling of secondary active transporters: updated protocol and prediction of elevator-type mechanisms. Front. Pharmacol. 6:183
    [Google Scholar]
  8. 8. 
    El Ghachi M, Bouhss A, Blanot D, Mengin-Lecreulx D 2004. The bacA gene of Escherichia coli encodes an undecaprenyl pyrophosphate phosphatase activity. J. Biol. Chem. 279:30106–13
    [Google Scholar]
  9. 9. 
    El Ghachi M, Derbise A, Bouhss A, Mengin-Lecreulx D 2005. Identification of multiple genes encoding membrane proteins with undecaprenyl pyrophosphate phosphatase (UppP) activity in Escherichia coli. J. Biol. Chem 280:18689–95
    [Google Scholar]
  10. 10. 
    Fernandez F, Rush JS, Toke DA, Han GS, Quinn JE et al. 2001. The CWH8 gene encodes a dolichyl pyrophosphate phosphatase with a luminally oriented active site in the endoplasmic reticulum of Saccharomyces cerevisiae. J. Biol. Chem 276:41455–64
    [Google Scholar]
  11. 11. 
    Rush JS, Cho SK, Jiang S, Hofmann SL, Waechter CJ 2002. Identification and characterization of a cDNA encoding a dolichyl pyrophosphate phosphatase located in the endoplasmic reticulum of mammalian cells. J. Biol. Chem. 277:45226–34
    [Google Scholar]
  12. 12. 
    Ghachi ME, Howe N, Auger R, Lambion A, Guiseppi A et al. 2017. Crystal structure and biochemical characterization of the transmembrane PAP2 type phosphatidylglycerol phosphate phosphatase from Bacillus subtilis. Cell. Mol. Life Sci 74:2319–32
    [Google Scholar]
  13. 13. 
    Fan J, Jiang D, Zhao Y, Liu J, Zhang XC 2014. Crystal structure of lipid phosphatase Escherichia coli phosphatidylglycerophosphate phosphatase B. PNAS 111:7636–40
    [Google Scholar]
  14. 14. 
    Sigal YJ, McDermott MI, Morris AJ 2005. Integral membrane lipid phosphatases/phosphotransferases: common structure and diverse functions. Biochem. J. 387:281–93
    [Google Scholar]
  15. 15. 
    Hartley MD, Imperiali B. 2012. At the membrane frontier: a prospectus on the remarkable evolutionary conservation of polyprenols and polyprenyl-phosphates. Arch. Biochem. Biophys. 517:83–97
    [Google Scholar]
  16. 16. 
    ban Duijn G, Valtersson C, Chojnacki T, Verkleij AJ, Dallner G, de Kruijff B 1986. Dolichyl phosphate induces non-bilayer structures, vesicle fusion and transbilayer movement of lipids: a model membrane study. Biochim. Biophys. Acta Biomembr. 861:211–23
    [Google Scholar]
  17. 17. 
    Zhou GP, Troy FA II 2005. NMR study of the preferred membrane orientation of polyisoprenols (dolichol) and the impact of their complex with polyisoprenyl recognition sequence peptides on membrane structure. Glycobiology 15:347–59
    [Google Scholar]
  18. 18. 
    Wang X, Mansourian AR, Quinn PJ 2008. The effect of dolichol on the structure and phase behaviour of phospholipid model membranes. Mol. Membr. Biol. 25:547–56
    [Google Scholar]
  19. 19. 
    Yoo J, Mashalidis EH, Kuk ACY, Yamamoto K, Kaeser B et al. 2018. GlcNAc-1-P-transferase-tunicamycin complex structure reveals basis for inhibition of N-glycosylation. Nat. Struct. Mol. Biol. 25:217–24
    [Google Scholar]
  20. 20. 
    Hakulinen JK, Hering J, Branden G, Chen H, Snijder A et al. 2017. MraY-antibiotic complex reveals details of tunicamycin mode of action. Nat. Chem. Biol. 13:265–67
    [Google Scholar]
  21. 21. 
    Chung BC, Mashalidis EH, Tanino T, Kim M, Matsuda A et al. 2016. Structural insights into inhibition of lipid I production in bacterial cell wall synthesis. Nature 533:557–60
    [Google Scholar]
  22. 22. 
    Chung BC, Zhao J, Gillespie RA, Kwon DY, Guan Z et al. 2013. Crystal structure of MraY, an essential membrane enzyme for bacterial cell wall synthesis. Science 341:1012–16
    [Google Scholar]
  23. 23. 
    Kowarik M, Numao S, Feldman MF, Schulz BL, Callewaert N et al. 2006. N-linked glycosylation of folded proteins by the bacterial oligosaccharyltransferase. Science 314:1148–50
    [Google Scholar]
  24. 24. 
    Perez C, Gerber S, Boilevin J, Bucher M, Darbre T et al. 2015. Structure and mechanism of an active lipid-linked oligosaccharide flippase. Nature 524:433–38
    [Google Scholar]
  25. 25. 
    Perez C, Mehdipour AR, Hummer G, Locher KP 2019. Structure of outward-facing PglK and molecular dynamics of lipid-linked oligosaccharide recognition and translocation. Structure 27:669–78.e5
    [Google Scholar]
  26. 26. 
    Raetz CRH, Reynolds CM, Trent MS, Bishop RE 2007. Lipid A modification systems in gram-negative bacteria. Annu. Rev. Biochem. 76:295–329
    [Google Scholar]
  27. 27. 
    Needham BD, Trent MS. 2013. Fortifying the barrier: the impact of lipid A remodelling on bacterial pathogenesis. Nat. Rev. Microbiol. 11:467–81
    [Google Scholar]
  28. 28. 
    Petrou VI, Herrera CM, Schultz KM, Clarke OB, Vendome J et al. 2016. Structures of aminoarabinose transferase ArnT suggest a molecular basis for lipid A glycosylation. Science 351:608–12
    [Google Scholar]
  29. 29. 
    Napiorkowska M, Boilevin J, Sovdat T, Darbre T, Reymond JL et al. 2017. Molecular basis of lipid-linked oligosaccharide recognition and processing by bacterial oligosaccharyltransferase. Nat. Struct. Mol. Biol. 24:1100–6
    [Google Scholar]
  30. 30. 
    Lizak C, Gerber S, Numao S, Aebi M, Locher KP 2011. X-ray structure of a bacterial oligosaccharyltransferase. Nature 474:350–55
    [Google Scholar]
  31. 31. 
    Caffalette CA, Corey RA, Sansom MSP, Stansfeld PJ, Zimmer J 2019. A lipid gating mechanism for the channel-forming O antigen ABC transporter. Nat. Commun. 10:824
    [Google Scholar]
  32. 32. 
    Reeves P. 1995. Role of O-antigen variation in the immune response. Trends Microbiol 3:381–86
    [Google Scholar]
  33. 33. 
    Whitfield C, Trent MS. 2014. Biosynthesis and export of bacterial lipopolysaccharides. Annu. Rev. Biochem. 83:99–128
    [Google Scholar]
  34. 34. 
    Liston SD, Mann E, Whitfield C 2017. Glycolipid substrates for ABC transporters required for the assembly of bacterial cell-envelope and cell-surface glycoconjugates. Biochim. Biophys. Acta Mol. Cell Biol. Lipids 1862:1394–403
    [Google Scholar]
  35. 35. 
    Raetz CRH, Whitfield C. 2002. Lipopolysaccharide endotoxins. Annu. Rev. Biochem. 71:635–700
    [Google Scholar]
  36. 36. 
    Lam JS, Taylor VL, Islam ST, Hao Y, Kocincova D 2011. Genetic and functional diversity of Pseudomonas aeruginosa lipopolysaccharide. Front. Microbiol. 2:118
    [Google Scholar]
  37. 37. 
    Whitfield C. 2006. Biosynthesis and assembly of capsular polysaccharides in Escherichia coli. Annu. Rev. Biochem 75:39–68
    [Google Scholar]
  38. 38. 
    Wang L, Liu D, Reeves PR 1996. C-terminal half of Salmonella enterica WbaP (RfbP) is the galactosyl-1-phosphate transferase domain catalyzing the first step of O-antigen synthesis. J. Bacteriol. 178:2598–604
    [Google Scholar]
  39. 39. 
    Lehrer J, Vigeant KA, Tatar LD, Valvano MA 2007. Functional characterization and membrane topology of Escherichia coli WecA, a sugar-phosphate transferase initiating the biosynthesis of enterobacterial common antigen and O-antigen lipopolysaccharide. J. Bacteriol. 189:2618–28
    [Google Scholar]
  40. 40. 
    Rocchetta HL, Burrows LL, Pacan JC, Lam JS 1998. Three rhamnosyltransferases responsible for assembly of the A-band D-rhamnan polysaccharide in Pseudomonas aeruginosa: a fourth transferase, WbpL, is required for the initiation of both A-band and B-band lipopolysaccharide synthesis. Mol. Microbiol. 28:1103–19
    [Google Scholar]
  41. 41. 
    Rush JS, Rick PD, Waechter CJ 1997. Polyisoprenyl phosphate specificity of UDP-GlcNAc:undecaprenyl phosphate N-acetylglucosaminyl 1-P transferase from E. coli. Glycobiology 7:315–22
    [Google Scholar]
  42. 42. 
    Al-Dabbagh B, Mengin-Lecreulx D, Bouhss A 2008. Purification and characterization of the bacterial UDP-GlcNAc:undecaprenyl-phosphate GlcNAc-1-phosphate transferase WecA. J. Bacteriol. 190:7141–46
    [Google Scholar]
  43. 43. 
    Al-Dabbagh B, Henry X, El Ghachi M, Auger G, Blanot D et al. 2008. Active site mapping of MraY, a member of the polyprenyl-phosphate N-acetylhexosamine 1-phosphate transferase superfamily, catalyzing the first membrane step of peptidoglycan biosynthesis. Biochemistry 47:8919–28
    [Google Scholar]
  44. 44. 
    Al-Dabbagh B, Olatunji S, Crouvoisier M, El Ghachi M, Blanot D et al. 2016. Catalytic mechanism of MraY and WecA, two paralogues of the polyprenyl-phosphate N-acetylhexosamine 1-phosphate transferase superfamily. Biochimie 127:249–57
    [Google Scholar]
  45. 45. 
    Liu Y, Rodrigues JP, Bonvin AM, Zaal EA, Berkers CR et al. 2016. New insight into the catalytic mechanism of bacterial MraY from enzyme kinetics and docking studies. J. Biol. Chem. 291:15057–68
    [Google Scholar]
  46. 46. 
    Hong Y, Liu MA, Reeves PR 2018. Progress in our understanding of Wzx flippase for translocation of bacterial membrane lipid-linked oligosaccharide. J. Bacteriol. 200:e00154–17
    [Google Scholar]
  47. 47. 
    Paulsen IT, Beness AM, Saier MH Jr 1997. Computer-based analyses of the protein constituents of transport systems catalysing export of complex carbohydrates in bacteria. Microbiology 143:Part 82685–99
    [Google Scholar]
  48. 48. 
    Feldman MF, Marolda CL, Monteiro MA, Perry MB, Parodi AJ, Valvano MA 1999. The activity of a putative polyisoprenol-linked sugar translocase (Wzx) involved in Escherichia coli O antigen assembly is independent of the chemical structure of the O repeat. J. Biol. Chem. 274:35129–38
    [Google Scholar]
  49. 49. 
    Marolda CL, Tatar LD, Alaimo C, Aebi M, Valvano MA 2006. Interplay of the Wzx translocase and the corresponding polymerase and chain length regulator proteins in the translocation and periplasmic assembly of lipopolysaccharide O antigen. J. Bacteriol. 188:5124–35
    [Google Scholar]
  50. 50. 
    Marolda CL, Vicarioli J, Valvano MA 2004. Wzx proteins involved in biosynthesis of O antigen function in association with the first sugar of the O-specific lipopolysaccharide subunit. Microbiology 150:4095–105
    [Google Scholar]
  51. 51. 
    Islam ST, Lam JS. 2014. Synthesis of bacterial polysaccharides via the Wzx/Wzy-dependent pathway. Can. J. Microbiol. 60:697–716
    [Google Scholar]
  52. 52. 
    Liu MA, Morris P, Reeves PR 2019. Wzx flippases exhibiting complex O-unit preferences require a new model for Wzx-substrate interactions. Microbiology 8:e00655
    [Google Scholar]
  53. 53. 
    Islam ST, Fieldhouse RJ, Anderson EM, Taylor VL, Keates RA et al. 2012. A cationic lumen in the Wzx flippase mediates anionic O-antigen subunit translocation in Pseudomonas aeruginosa PAO1. Mol. Microbiol. 84:1165–76
    [Google Scholar]
  54. 54. 
    Islam ST, Eckford PD, Jones ML, Nugent T, Bear CE et al. 2013. Proton-dependent gating and proton uptake by Wzx support O-antigen-subunit antiport across the bacterial inner membrane. mBio 4:e00678–13
    [Google Scholar]
  55. 55. 
    Kuk AC, Mashalidis EH, Lee SY 2017. Crystal structure of the MOP flippase MurJ in an inward-facing conformation. Nat. Struct. Mol. Biol. 24:171–76
    [Google Scholar]
  56. 56. 
    Kuk ACY, Hao A, Guan Z, Lee SY 2019. Visualizing conformation transitions of the Lipid II flippase MurJ. Nat. Commun. 10:1736
    [Google Scholar]
  57. 57. 
    Whitfield C. 1995. Biosynthesis of lipopolysaccharide O antigens. Trends Microbiol 3:178–85
    [Google Scholar]
  58. 58. 
    Kim TH, Sebastian S, Pinkham JT, Ross RA, Blalock LT, Kasper DL 2010. Characterization of the O-antigen polymerase (Wzy) of Francisella tularensis. J. Biol. Chem 285:27839–49
    [Google Scholar]
  59. 59. 
    Islam ST, Taylor VL, Qi M, Lam JS 2010. Membrane topology mapping of the O-antigen flippase (Wzx), polymerase (Wzy), and ligase (WaaL) from Pseudomonas aeruginosa PAO1 reveals novel domain architectures. mBio 1:e00189–10
    [Google Scholar]
  60. 60. 
    Woodward R, Yi W, Li L, Zhao G, Eguchi H et al. 2010. In vitro bacterial polysaccharide biosynthesis: defining the functions of Wzy and Wzz. Nat. Chem. Biol. 6:418–23
    [Google Scholar]
  61. 61. 
    Cuthbertson L, Mainprize IL, Naismith JH, Whitfield C 2009. Pivotal roles of the outer membrane polysaccharide export and polysaccharide copolymerase protein families in export of extracellular polysaccharides in gram-negative bacteria. Microbiol. Mol. Biol. Rev. 73:155–77
    [Google Scholar]
  62. 62. 
    Collins RF, Kargas V, Clarke BR, Siebert CA, Clare DK et al. 2017. Full-length, oligomeric structure of Wzz determined by cryoelectron microscopy reveals insights into membrane-bound states. Structure 25:806–15.e3
    [Google Scholar]
  63. 63. 
    Tocilj A, Munger C, Proteau A, Morona R, Purins L et al. 2008. Bacterial polysaccharide co-polymerases share a common framework for control of polymer length. Nat. Struct. Mol. Biol. 15:130–38
    [Google Scholar]
  64. 64. 
    Larue K, Kimber MS, Ford R, Whitfield C 2009. Biochemical and structural analysis of bacterial O-antigen chain length regulator proteins reveals a conserved quaternary structure. J. Biol. Chem. 284:7395–403
    [Google Scholar]
  65. 65. 
    Kalynych S, Cherney M, Bostina M, Rouiller I, Cygler M 2015. Quaternary structure of WzzB and WzzE polysaccharide copolymerases. Protein Sci 24:58–69
    [Google Scholar]
  66. 66. 
    Kalynych S, Yao D, Magee J, Cygler M 2012. Structural characterization of closely related O-antigen lipopolysaccharide (LPS) chain length regulators. J. Biol. Chem. 287:15696–705
    [Google Scholar]
  67. 67. 
    Papadopoulos M, Morona R. 2010. Mutagenesis and chemical cross-linking suggest that Wzz dimer stability and oligomerization affect lipopolysaccharide O-antigen modal chain length control. J. Bacteriol. 192:3385–93
    [Google Scholar]
  68. 68. 
    Huszczynski SM, Coumoundouros C, Pham P, Lam JS, Khursigara CM 2019. Unique regions of the polysaccharide copolymerase Wzz2 from Pseudomonas aeruginosa are essential for O-specific antigen chain length control. J. Bacteriol. 201:e00165–19
    [Google Scholar]
  69. 69. 
    Clarke BR, Cuthbertson L, Whitfield C 2004. Nonreducing terminal modifications determine the chain length of polymannose O antigens of Escherichia coli and couple chain termination to polymer export via an ATP-binding cassette transporter. J. Biol. Chem. 279:35709–18
    [Google Scholar]
  70. 70. 
    Kos V, Cuthbertson L, Whitfield C 2009. The Klebsiella pneumoniae O2a antigen defines a second mechanism for O antigen ATP-binding cassette transporters. J. Biol. Chem. 284:2947–56
    [Google Scholar]
  71. 71. 
    Cuthbertson L, Kimber MS, Whitfield C 2007. Substrate binding by a bacterial ABC transporter involved in polysaccharide export. PNAS 104:19529–34
    [Google Scholar]
  72. 72. 
    Kos V, Whitfield C. 2010. A membrane-located glycosyltransferase complex required for biosynthesis of the d-galactan I lipopolysaccharide O antigen in Klebsiella pneumoniae. J. Biol. Chem 285:19668–87
    [Google Scholar]
  73. 73. 
    Clarke BR, Greenfield LK, Bouwman C, Whitfield C 2009. Coordination of polymerization, chain termination, and export in assembly of the Escherichia coli lipopolysaccharide O9a antigen in an ATP-binding cassette transporter-dependent pathway. J. Biol. Chem. 284:30662–72
    [Google Scholar]
  74. 74. 
    Kido N, Torgov VI, Sugiyama T, Uchiya K, Sugihara H et al. 1995. Expression of the O9 polysaccharide of Escherichia coli: sequencing of the E. coli O9 rfb gene cluster, characterization of mannosyl transferases, and evidence for an ATP-binding cassette transport system. J. Bacteriol. 177:2178–87
    [Google Scholar]
  75. 75. 
    Greenfield LK, Richards MR, Li J, Wakarchuk WW, Lowary TL, Whitfield C 2012. Biosynthesis of the polymannose lipopolysaccharide O-antigens from Escherichia coli serotypes O8 and O9a requires a unique combination of single- and multiple-active site mannosyltransferases. J. Biol. Chem. 287:35078–91
    [Google Scholar]
  76. 76. 
    Clarke BR, Ovchinnikova OG, Sweeney RP, Kamski-Hennekam ER, Gitalis R et al. 2020. A bifunctional O-antigen polymerase structure reveals a new glycosyltransferase family. Nat. Chem. Biol. 16:450–57
    [Google Scholar]
  77. 77. 
    Guan S, Clarke AJ, Whitfield C 2001. Functional analysis of the galactosyltransferases required for biosynthesis of d-galactan I, a component of the lipopolysaccharide O1 antigen of Klebsiella pneumoniae. J. Bacteriol 183:3318–27
    [Google Scholar]
  78. 78. 
    Kido N, Sugiyama T, Yokochi T, Kobayashi H, Okawa Y 1998. Synthesis of Escherichia coli O9a polysaccharide requires the participation of two domains of WbdA, a mannosyltransferase encoded within the wb* gene cluster. Mol. Microbiol. 27:1213–21
    [Google Scholar]
  79. 79. 
    Greenfield LK, Richards MR, Vinogradov E, Wakarchuk WW, Lowary TL, Whitfield C 2012. Domain organization of the polymerizing mannosyltransferases involved in synthesis of the Escherichia coli O8 and O9a lipopolysaccharide O-antigens. J. Biol. Chem. 287:38135–49
    [Google Scholar]
  80. 80. 
    Liston SD, Clarke BR, Greenfield LK, Richards MR, Lowary TL, Whitfield C 2015. Domain interactions control complex formation and polymerase specificity in the biosynthesis of the Escherichia coli O9a antigen. J. Biol. Chem. 290:1075–85
    [Google Scholar]
  81. 81. 
    Hagelueken G, Huang H, Clarke BR, Lebl T, Whitfield C, Naismith JH 2012. Structure of WbdD: a bifunctional kinase and methyltransferase that regulates the chain length of the O antigen in Escherichia coli O9a. Mol. Microbiol. 86:730–42
    [Google Scholar]
  82. 82. 
    Hagelueken G, Clarke BR, Huang H, Tuukkanen A, Danciu I et al. 2015. A coiled-coil domain acts as a molecular ruler to regulate O-antigen chain length in lipopolysaccharide. Nat. Struct. Mol. Biol. 22:50–56
    [Google Scholar]
  83. 83. 
    Greenfield LK, Whitfield C. 2012. Synthesis of lipopolysaccharide O-antigens by ABC transporter-dependent pathways. Carbohydr. Res. 356:12–24
    [Google Scholar]
  84. 84. 
    Bi Y, Mann E, Whitfield C, Zimmer J 2018. Architecture of a channel-forming O-antigen polysaccharide ABC transporter. Nature 553:7688361–65
    [Google Scholar]
  85. 85. 
    Mann E, Mallette E, Clarke BR, Kimber MS, Whitfield C 2016. The Klebsiella pneumoniae O12 ATP-binding cassette (ABC) transporter recognizes the terminal residue of its O-antigen polysaccharide substrate. J. Biol. Chem. 291:9748–61
    [Google Scholar]
  86. 86. 
    Hashimoto H. 2006. Recent structural studies of carbohydrate-binding modules. Cell. Mol. Life Sci. 63:2954–67
    [Google Scholar]
  87. 87. 
    Brown S, Santa Maria JP Jr., Walker S 2013. Wall teichoic acids of gram-positive bacteria. Annu. Rev. Microbiol. 67:313–36
    [Google Scholar]
  88. 88. 
    Morgan JLW, Strumillo J, Zimmer J 2012. Crystallographic snapshot of cellulose synthesis and membrane translocation. Nature 493:181–86
    [Google Scholar]
  89. 89. 
    Whitfield C, Amor PA, Köplin R 1997. Modulation of the surface architecture of Gram‐negative bacteria by the action of surface polymer:lipid A–core ligase and by determinants of polymer chain length. Mol. Microbiol. 23:629–38
    [Google Scholar]
  90. 90. 
    Abeyrathne PD, Lam JS. 2007. WaaL of Pseudomonas aeruginosa utilizes ATP in in vitro ligation of O antigen onto lipid A-core. Mol. Microbiol. 65:1345–59
    [Google Scholar]
  91. 91. 
    Ruan X, Monjarás Feria J, Hamad M, Valvano MA 2018. Escherichia coli and Pseudomonas aeruginosa lipopolysaccharide O-antigen ligases share similar membrane topology and biochemical properties. Mol. Microbiol. 110:95–113
    [Google Scholar]
  92. 92. 
    Pérez JM, McGarry MA, Marolda CL, Valvano MA 2008. Functional analysis of the large periplasmic loop of the Escherichia coli K-12 WaaL O-antigen ligase. Mol. Microbiol. 70:1424–40
    [Google Scholar]
  93. 93. 
    Schild S, Lamprecht A-K, Reidl J 2005. Molecular and functional characterization of O antigen transfer in Vibrio cholerae. J. Biol. Chem 280:25936–47
    [Google Scholar]
  94. 94. 
    Lairson LL, Henrissat B, Davies GJ, Withers SG 2008. Glycosyltransferases: structures, functions, and mechanisms. Annu. Rev. Biochem. 77:521–55
    [Google Scholar]
  95. 95. 
    Reichmann NT, Grundling A. 2011. Location, synthesis and function of glycolipids and polyglycerolphosphate lipoteichoic acid in Gram-positive bacteria of the phylum Firmicutes. FEMS Microbiol. Lett 319:97–105
    [Google Scholar]
  96. 96. 
    Lovering AL, Lin LY-C, Sewell EW, Spreter T, Brown ED, Strynadka NCJ 2010. Structure of the bacterial teichoic acid polymerase TagF provides insights into membrane association and catalysis. Nature 17:582–89
    [Google Scholar]
  97. 97. 
    Schertzer JW, Brown ED. 2008. Use of CDP-glycerol as an alternate acceptor for the teichoic acid polymerase reveals that membrane association regulates polymer length. J. Bacteriol. 190:6940–47
    [Google Scholar]
  98. 98. 
    Schirner K, Marles-Wright J, Lewis RJ, Errington J 2009. Distinct and essential morphogenic functions for wall- and lipo-teichoic acids in Bacillus subtilis. EMBO J 28:830–42
    [Google Scholar]
  99. 99. 
    Lu D, Wormann ME, Zhang X, Schneewind O, Grundling A, Freemont PS 2009. Structure-based mechanism of lipoteichoic acid synthesis by Staphylococcus aureus LtaS. PNAS 106:1584–89
    [Google Scholar]
  100. 100. 
    Cabacungan E, Pieringer RA. 1981. Mode of elongation of the glycerol phosphate polymer of membrane lipoteichoic acid of Streptococcus faecium ATCC 9790. J. Bacteriol. 147:75–79
    [Google Scholar]
  101. 101. 
    Schirner K, Stone LK, Walker S 2011. ABC transporters required for export of wall teichoic acids do not discriminate between different main chain polymers. ACS Chem. Biol. 6:407–12
    [Google Scholar]
  102. 102. 
    Gerlach D, Guo Y, De Castro C, Kim SH, Schlatterer K et al. 2018. Methicillin-resistant Staphylococcus aureus alters cell wall glycosylation to evade immunity. Nature 563:705–9
    [Google Scholar]
  103. 103. 
    Sobhanifar S, Worrall LJ, Gruninger RJ, Wasney GA, Blaukopf M et al. 2015. Structure and mechanism of Staphylococcus aureus TarM, the wall teichoic acid α-glycosyltransferase. PNAS 112:E576–85
    [Google Scholar]
  104. 104. 
    Koc C, Gerlach D, Beck S, Peschel A, Xia G, Stehle T 2015. Structural and enzymatic analysis of TarM glycosyltransferase from Staphylococcus aureus reveals an oligomeric protein specific for the glycosylation of wall teichoic acid. J. Biol. Chem. 290:9874–85
    [Google Scholar]
  105. 105. 
    Sobhanifar S, Worrall LJ, King DT, Wasney GA, Baumann L et al. 2016. Structure and mechanism of Staphylococcus aureus TarS, the wall teichoic acid β-glycosyltransferase involved in methicillin resistance. PLOS Pathog 12:e1006067
    [Google Scholar]
  106. 106. 
    Reichmann NT, Cassona CP, Grundling A 2013. Revised mechanism of d-alanine incorporation into cell wall polymers in Gram-positive bacteria. Microbiology 159:1868–77
    [Google Scholar]
  107. 107. 
    Whitfield GB, Marmont LS, Howell PL 2015. Enzymatic modifications of exopolysaccharides enhance bacterial persistence. Front. Microbiol. 6:471
    [Google Scholar]
  108. 108. 
    Perego M, Glaser P, Minutello A, Strauch MA, Leopold K, Fischer W 1995. Incorporation of d-alanine into lipoteichoic acid and wall teichoic acid in Bacillus subtilis. Identification of genes and regulation. J. Biol. Chem. 270:15598–606
    [Google Scholar]
  109. 109. 
    Ma D, Wang Z, Merrikh CN, Lang KS, Lu P et al. 2018. Crystal structure of a membrane-bound O-acyltransferase. Nature 562:286–90
    [Google Scholar]
  110. 110. 
    Wacker M, Linton D, Hitchen PG, Nita-Lazar M, Haslam SM et al. 2002. N-linked glycosylation in Campylobacter jejuni and its functional transfer into E. coli. Science 298:1790–93
    [Google Scholar]
  111. 111. 
    Breitling J, Aebi M. 2013. N-linked protein glycosylation in the endoplasmic reticulum. Cold Spring Harb. Perspect. Biol. 5:a013359
    [Google Scholar]
  112. 112. 
    Jarrell KF, Ding Y, Meyer BH, Albers SV, Kaminski L, Eichler J 2014. N-linked glycosylation in Archaea: a structural, functional, and genetic analysis. Microbiol. Mol. Biol. Rev. 78:304–41
    [Google Scholar]
  113. 113. 
    Nothaft H, Szymanski CM. 2010. Protein glycosylation in bacteria: sweeter than ever. Nat. Rev. Microbiol. 8:765–78
    [Google Scholar]
  114. 114. 
    Horwitz MA, Silverstein SC. 1980. Influence of the Escherichia coli capsule on complement fixation and on phagocytosis and killing by human phagocytes. J. Clin. Invest. 65:82–94
    [Google Scholar]
  115. 115. 
    Cress BF, Englaender JA, He W, Kasper D, Linhardt RJ, Koffas MAG 2014. Masquerading microbial pathogens: Capsular polysaccharides mimic host-tissue molecules. Microbiol. Rev. 38:660–97
    [Google Scholar]
  116. 116. 
    Sachdeva S, Palur RV, Sudhakar KU, Rathinavelan T 2017. E. coli group 1 capsular polysaccharide exportation nanomachinary as a plausible antivirulence target in the perspective of emerging antimicrobial resistance. Front. Microbiol. 8:70
    [Google Scholar]
  117. 117. 
    Taylor CM, Roberts IS. 2005. Capsular polysaccharides and their role in virulence. Contrib. Microbiol. 12:55–66
    [Google Scholar]
  118. 118. 
    Hyams C, Camberlein E, Cohen JM, Bax K, Brown JS 2010. The Streptococcus pneumoniae capsule inhibits complement activity and neutrophil phagocytosis by multiple mechanisms. Infect. Immun. 78:704–15
    [Google Scholar]
  119. 119. 
    Whitfield C. 2010. Glycan chain-length control. Nat. Chem. Biol. 6:403–4
    [Google Scholar]
  120. 120. 
    Wugeditsch T, Paiment A, Hocking J, Drummelsmith J, Forrester C, Whitfield C 2001. Phosphorylation of Wzc, a tyrosine autokinase, is essential for assembly of group 1 capsular polysaccharides in Escherichia coli. J. Biol. Chem 267:2361–71
    [Google Scholar]
  121. 121. 
    Collins RF, Beis K, Dong C, Botting CH, McDonnell C et al. 2007. The 3D structure of a periplasm-spanning platform required for assembly of group 1 capsular polysaccharides in Escherichia coli. PNAS 104:2390–95
    [Google Scholar]
  122. 122. 
    Bechet E, Gruszczyk J, Terreux R, Gueguen-Chaignon V, Vigouroux A et al. 2010. Identification of structural and molecular determinants of the tyrosine-kinase Wzc and implications in capsular polysaccharide export. Mol. Microbiol. 77:1315–25
    [Google Scholar]
  123. 123. 
    Drummelsmith J. 2000. Translocation of group 1 capsular polysaccharide to the surface of Escherichia coli requires a multimeric complex in the outer membrane. EMBO J 19:57–66
    [Google Scholar]
  124. 124. 
    Dong C, Beis K, Nesper J, Brunkan-LaMontagne AL, Clarke BR et al. 2006. Wza the translocon for E. coli capsular polysaccharides defines a new class of membrane protein. Nature 444:226–29
    [Google Scholar]
  125. 125. 
    Nickerson NN, Mainprize IL, Hampton L, Jones ML, Naismith JH, Whitfield C 2014. Trapped translocation intermediates establish the route for export of capsular polysaccharides across Escherichia coli outer membranes. PNAS 111:8203–8
    [Google Scholar]
  126. 126. 
    Jann K, Jann B. 1992. Capsules of Escherichia coli, expression and biological significance. Can. J. Microbiol. 38:705–10
    [Google Scholar]
  127. 127. 
    Willis LM, Stupak J, Richards MR, Lowary TL, Li J, Whitfield C 2013. Conserved glycolipid termini in capsular polysaccharides synthesized by ATP-binding cassette transporter-dependent pathways in Gram-negative pathogens. PNAS 110:7868–73
    [Google Scholar]
  128. 128. 
    Willis LM, Whitfield C. 2013. KpsC and KpsS are retaining 3-deoxy-d-manno-oct-2-ulosonic acid (Kdo) transferases involved in synthesis of bacterial capsules. PNAS 110:20753–58
    [Google Scholar]
  129. 129. 
    Kohlbrenner WE, Fesik SW. 1985. Determination of the anomeric specificity of the Escherichia coli CTP:CMP-3-deoxy-d-manno-octulosonate cytidyltransferase by 13C NMR spectroscopy. J. Biol. Chem. 260:14695–700
    [Google Scholar]
  130. 130. 
    Satola SW, Schirmer PL, Farley MM 2003. Complete sequence of the cap locus of Haemophilus influenzae serotype b and nonencapsulated b capsule-negative variants. Infect. Immun. 71:3639–44
    [Google Scholar]
  131. 131. 
    Frosch M, Müller A. 1993. Phospholipid substitution of capsular polysaccharides and mechanisms of capsule formation in Neisseria meningitidis. Mol. Microbiol 8:483–93
    [Google Scholar]
  132. 132. 
    Jelakovic S, Jann K, Schulz GE 1996. The three-dimensional structure of capsule-specific CMP: 2-keto-3-deoxy-manno-octonic acid synthetase from Escherichia coli. FEBS Lett 391:157–61
    [Google Scholar]
  133. 133. 
    Doyle L, Ovchinnikova OG, Myler K, Mallette E, Huang BS et al. 2019. Biosynthesis of a conserved glycolipid anchor for Gram-negative bacterial capsules. Nat. Chem. Biol. 15:632–40
    [Google Scholar]
  134. 134. 
    Liston SD, Ovchinnikova OG, Whitfield C 2016. Unique lipid anchor attaches Vi antigen capsule to the surface of Salmonella enterica serovar Typhi. PNAS 113:6719–24
    [Google Scholar]
  135. 135. 
    Hu X, Chen Z, Xiong K, Wang J, Rao X, Cong Y 2017. Vi capsular polysaccharide: synthesis, virulence, and application. Crit. Rev. Microbiol. 43:440–52
    [Google Scholar]
  136. 136. 
    DeAngelis PL, White CL. 2002. Identification and molecular cloning of a heparosan synthase from Pasteurella multocida Type D. J. Biol. Chem. 277:7209–13
    [Google Scholar]
  137. 137. 
    Jing W, De Angelis PL 2000. Dissection of the two transferase activities of the Pasteurella multocida hyaluronan synthase: Two active sites exist in one polypeptide. Glycobiology 10:883–89
    [Google Scholar]
  138. 138. 
    Osawa T, Sugiura N, Shimada H, Hirooka R, Tsuji A et al. 2009. Crystal structure of chondroitin polymerase from Escherichia coli K4. Biochem. Biophys. Res. Comm. 378:10–14
    [Google Scholar]
  139. 139. 
    Wasteson Å 1971. A method for the determination of the molecular weight and molecular-weight distribution of chondroitin sulphate. J. Chromatogr. A 59:87–97
    [Google Scholar]
  140. 140. 
    Sugiura N, Tawada A, Sugimoto K, Watanabe H 2002. Molecular cloning and characterization of chondroitin polymerase from Escherichia coli strain K4. J. Biol. Chem. 227:21567–75
    [Google Scholar]
  141. 141. 
    Jing W, DeAngelis PL. 2003. Analysis of the two active sites of the hyaluronan synthase and the chondroitin synthase of Pasteurella multocida. Glycobiology 13:661–71
    [Google Scholar]
  142. 142. 
    Mandawe J, Infanzon B, Eisele A, Zaun H, Kuballa J et al. 2018. Directed evolution of hyaluronic acid synthase from Pasteurella multocida towards high-molecular-weight hyaluronic acid. ChemBioChem 19:1414–23
    [Google Scholar]
  143. 143. 
    Otto NJ, Green DE, Masuko S, Mayer A, Tanner ME et al. 2012. Structure/function analysis of Pasteurella multocida heparosan synthases: toward defining enzyme specificity and engineering novel catalysts. J. Biol. Chem. 287:7203–12
    [Google Scholar]
  144. 144. 
    Sugiura N, Baba Y, Kawaguchi Y, Iwatani T, Suzuki K et al. 2010. Glucuronyltransferase activity of KfiC from Escherichia coli strain K5 requires association of KfiA: KfiC and KfiA are essential enzymes for production of K5 polysaccharide, N-acetylheparosan. J. Biol. Chem. 285:1597–606
    [Google Scholar]
  145. 145. 
    Liu J, Yang A, Liu J, Ding X, Liu L, Shi Z 2014. KfoE encodes a fructosyltransferase involved in capsular polysaccharide biosynthesis in Escherichia coli K4. Biotechnol. Lett. 36:1469–77
    [Google Scholar]
  146. 146. 
    Neuberger A, Du D, Luisi BF 2018. Structure and mechanism of bacterial tripartite efflux pumps. Res. Microbiol. 169:401–13
    [Google Scholar]
  147. 147. 
    Nsahlai CJ, Silver RP. 2003. Purification and characterization of KpsT, the ATP-binding component of the ABC-capsule exporter of Escherichia coli K1. FEMS Microbiol. Lett. 224:113–18
    [Google Scholar]
  148. 148. 
    Pavelka MS, Hayes SF, Silver RP 1994. Characterization of KpsT, the ATP-binding component of the ABC-transporter involved with the export of capsular polysialic acid in Escherichia coli K1. J. Biol. Chem. 269:20149–58
    [Google Scholar]
  149. 149. 
    Lo RYC, McKerral LJ, Hills TL, Kostrzynska M 2001. Analysis of the capsule biosynthetic locus of Mannheimia (Pasteurella) haemolytica A1 and proposal of a nomenclature system. Infect. Immun. 69:4458–64
    [Google Scholar]
  150. 150. 
    Liston SD, McMahon SA, Le Bas A, Suits MDL, Naismith JH, Whitfield C 2018. Periplasmic depolymerase provides insight into ABC transporter-dependent secretion of bacterial capsular polysaccharides. PNAS 115:E4870–79
    [Google Scholar]
/content/journals/10.1146/annurev-biochem-011520-104707
Loading
/content/journals/10.1146/annurev-biochem-011520-104707
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error