1932

Abstract

Polysaccharides are dominant features of most bacterial surfaces and are displayed in different formats. Many bacteria produce abundant long-chain capsular polysaccharides, which can maintain a strong association and form a capsule structure enveloping the cell and/or take the form of exopolysaccharides that are mostly secreted into the immediate environment. These polymers afford the producing bacteria protection from a wide range of physical, chemical, and biological stresses, support biofilms, and play critical roles in interactions between bacteria and their immediate environments. Their biological and physical properties also drive a variety of industrial and biomedical applications. Despite the immense variation in capsular polysaccharide and exopolysaccharide structures, patterns are evident in strategies used for their assembly and export. This review describes recent advances in understanding those strategies, based on a wealth of biochemical investigations of select prototypes, supported by complementary insight from expanding structural biology initiatives. This provides a framework to identify and distinguish new systems emanating from genomic studies.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-micro-011420-075607
2020-09-08
2024-06-23
Loading full text...

Full text loading...

/deliver/fulltext/micro/74/1/annurev-micro-011420-075607.html?itemId=/content/journals/10.1146/annurev-micro-011420-075607&mimeType=html&fmt=ahah

Literature Cited

  1. 1. 
    Acheson JF, Derewenda ZS, Zimmer J 2019. Architecture of the cellulose synthase outer membrane channel and its association with the periplasmic TPR domain. Structure 27:1855–61
    [Google Scholar]
  2. 2. 
    Allen KN, Imperiali B. 2019. Structural and mechanistic themes in glycoconjugate biosynthesis at membrane interfaces. Curr. Opin. Struct. Biol. 59:81–90
    [Google Scholar]
  3. 3. 
    Aslam SN, Newman M-A, Erbs G, Morrissey KL, Chinchilla D et al. 2008. Bacterial polysaccharides suppress induced innate immunity by calcium chelation. Curr. Biol. 18:141078–83
    [Google Scholar]
  4. 4. 
    Baker P, Ricer T, Moynihan PJ, Kitova EN, Walvoort MTC et al. 2014. P. aeruginosa SGNH hydrolase-like proteins AlgJ and AlgX have similar topology but separate and distinct roles in alginate acetylation. PLOS Pathog 10:8e1004334
    [Google Scholar]
  5. 5. 
    Bechet E, Gruszczyk J, Terreux REL, 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. 77:51315–25
    [Google Scholar]
  6. 6. 
    Bi Y, Mann E, Whitfield C, Zimmer J 2018. Architecture of a channel-forming O-antigen polysaccharide ABC transporter. Nature 553:361–65
    [Google Scholar]
  7. 7. 
    Bowen WH, Koo H. 2011. Biology of Streptococcus mutans-derived glucosyltransferases: role in extracellular matrix formation of cariogenic biofilms. Caries Res 45:169–86
    [Google Scholar]
  8. 8. 
    Brown RMJ, Willison JHM, Richardson CL 1976. Cellulose biosynthesis in Acetobacter xylinum: visualization of the site of synthesis and direct measurement of the in vivo process. PNAS 73:124565–69
    [Google Scholar]
  9. 9. 
    Bundalovic-Torma C, Whitfield GB, Marmont LS, Howell PL, Parkinson J 2019. A systematic pipeline for classifying bacterial operons reveals the evolutionary landscape of biofilm machineries. bioRxiv 769745
  10. 10. 
    Bushell SR, Mainprize IL, Wear MA, Lou H, Whitfield C, Naismith JH 2013. Wzi is an outer membrane lectin that underpins group 1 capsule assembly in Escherichia coli. . Structure 21:5844–53
    [Google Scholar]
  11. 11. 
    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. 10:1824
    [Google Scholar]
  12. 12. 
    Chan YGY, Frankel MB, Dengler V, Schneewind O, Missiakas D 2013. Staphylococcus aureus mutants lacking the LytR-CpsA-Psr family of enzymes release cell wall teichoic acids into the extracellular medium. J. Bacteriol. 195:204650–59
    [Google Scholar]
  13. 13. 
    Chan YG-Y, Kim HK, Schneewind O, Missiakas D 2014. The capsular polysaccharide of Staphylococcus aureus is attached to peptidoglycan by the LytR-CpsA-Psr (LCP) family of enzymes. J. Biol. Chem. 289:2215680–90
    [Google Scholar]
  14. 14. 
    Collins RF, Beis K, Clarke BR, Ford RC, Hulley M et al. 2006. Periplasmic protein-protein contacts in the inner membrane protein Wzc form a tetrameric complex required for the assembly of Escherichia coli group 1 capsules. J. Biol. Chem. 281:42144–50
    [Google Scholar]
  15. 15. 
    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 104:72390–95
    [Google Scholar]
  16. 16. 
    Cress BF, Englaender JA, He W, Kasper D, Linhardt RJ, Koffas MAG 2014. Masquerading microbial pathogens: capsular polysaccharides mimic host-tissue molecules. FEMS Microbiol. Rev. 38:4660–97
    [Google Scholar]
  17. 17. 
    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. 73:1155–77
    [Google Scholar]
  18. 18. 
    DeAngelis PL, Liu J, Linhardt RJ 2013. Chemoenzymatic synthesis of glycosaminoglycans: re-creating, re-modeling and re-designing nature's longest or most complex carbohydrate chains. Glycobiology 23:7764–77
    [Google Scholar]
  19. 19. 
    D'Haeze W, Holsters M. 2004. Surface polysaccharides enable bacteria to evade plant immunity. Trend Microbiol 12:12555–61
    [Google Scholar]
  20. 20. 
    Diao J, Bouwman C, Yan D, Kang J, Katakam AK et al. 2017. Peptidoglycan association of murein lipoprotein is required for KpsD-dependent group 2 capsular polysaccharide expression and serum resistance in a uropathogenic Escherichia coli isolate. mBio 8:3e00603–17
    [Google Scholar]
  21. 21. 
    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 444:7116226–29
    [Google Scholar]
  22. 22. 
    Doyle L, Ovchinnikova OG, Myler K, Mallette E, Huang B-S et al. 2019. Biosynthesis of a conserved glycolipid anchor for Gram-negative bacterial capsules. Nat. Chem. Biol. 15:6632–40
    [Google Scholar]
  23. 23. 
    Du J, Vepachedu V, Cho SH, Kumar M, Nixon BT 2016. Structure of the cellulose synthase complex of Gluconacetobacter hansenii at 23.4 Å resolution. PLOS ONE 11:5e0155886
    [Google Scholar]
  24. 24. 
    Eberhardt A, Hoyland CN, Vollmer D, Bisle S, Cleverley RM et al. 2012. Attachment of capsular polysaccharide to the cell wall in Streptococcus pneumoniae. Microb. . Drug Resist 18:3240–55
    [Google Scholar]
  25. 25. 
    Feldman MF, Bridwell AEM, Scott NE, Vinogradov E, McKee SR et al. 2019. A promising bioconjugate vaccine against hypervirulent Klebsiella pneumoniae. . PNAS 116:3718655–63
    [Google Scholar]
  26. 26. 
    Fresno S, Jiménez N, Izquierdo L, Merino S, Corsaro MM et al. 2006. The ionic interaction of Klebsiella pneumoniae K2 capsule and core lipopolysaccharide. Microbiology 152:1807–18
    [Google Scholar]
  27. 27. 
    Gale RT, Li FKK, Sun T, Strynadka NCJ, Brown ED 2017. B. subtilis LytR-CpsA-Psr enzymes transfer wall teichoic acids from authentic lipid-linked substrates to mature peptidoglycan in vitro. Cell Chem. Biol. 24:121537–46.e4
    [Google Scholar]
  28. 28. 
    Gangoiti J, Pijning T, Dijkhuizen L 2018. Biotechnological potential of novel glycoside hydrolase family 70 enzymes synthesizing α-glucans from starch and sucrose. Biotechnol. Adv. 36:1196–207
    [Google Scholar]
  29. 29. 
    Hagelueken G, Huang H, Mainprize IL, Whitfield C, Naismith JH 2009. Crystal structures of Wzb of Escherichia coli and CpsB of Streptococcus pneumoniae, representatives of two families of tyrosine phosphatases that regulate capsule assembly. J. Mol. Biol. 392:3678–88
    [Google Scholar]
  30. 30. 
    Harding CM, Feldman MF. 2019. Glycoengineering bioconjugate vaccines, therapeutics, and diagnostics in E. coli. . Glycobiology 29:519–29
    [Google Scholar]
  31. 31. 
    Harding CM, Nasr MA, Scott NE, Goyette-Desjardins G, Nothaft H et al. 2019. A platform for glycoengineering a polyvalent pneumococcal bioconjugate vaccine using E. coli as a host. Nat. Commun. 10:1891
    [Google Scholar]
  32. 32. 
    Hasdemir DE, Kasper DL. 2018. Finding a needle in a haystack: Bacteroides fragilis polysaccharide A as the archetypical symbiosis factor. Ann. N. Y. Acad. Sci. 1417:1116–29
    [Google Scholar]
  33. 33. 
    Hernández-Rocamora VM, Otten CF, Radkov A, Simorre J-P, Breukink E et al. 2018. Coupling of polymerase and carrier lipid phosphatase prevents product inhibition in peptidoglycan synthesis. Cell Surface 2:1–13
    [Google Scholar]
  34. 34. 
    Hinchliffe P, Symmons MF, Hughes C, Koronakis V 2013. Structure and operation of bacterial tripartite pumps. Ann. Rev. Biochem. 67:221–42
    [Google Scholar]
  35. 35. 
    Hong Y, Liu MA, Reeves PR 2017. Progress in our understanding of Wzx flippase for translocation of bacterial membrane lipid-linked oligosaccharide. J. Bacteriol. 200:1e00154–17
    [Google Scholar]
  36. 36. 
    Islam ST, Lam JS. 2014. Synthesis of bacterial polysaccharides via the Wzx/Wzy-dependent pathway. Can. J. Microbiol. 60:11697–716
    [Google Scholar]
  37. 37. 
    Jiménez N, Senchenkova SN, Knirel YA, Pieretti G, Corsaro MM et al. 2012. Effects of lipopolysaccharide biosynthesis mutations on K1 polysaccharide association with the Escherichia coli cell surface. J. Bacteriol. 194:133356–67
    [Google Scholar]
  38. 38. 
    Jorgenson MA, Kannan S, Laubacher ME, Young KD 2016. Dead-end intermediates in the enterobacterial common antigen pathway induce morphological defects in Escherichia coli by competing for undecaprenyl phosphate. Mol. Microbiol. 100:1–14
    [Google Scholar]
  39. 39. 
    Kawai Y, Marles-Wright J, Cleverley RM, Emmins R, Ishikawa S et al. 2011. A widespread family of bacterial cell wall assembly proteins. EMBO J 30:244931–41
    [Google Scholar]
  40. 40. 
    Kawakami N, Fujisaki S. 2017. Undecaprenyl phosphate metabolism in Gram-negative and Gram-positive bacteria. Biosci. Biotechnol. Biochem. 82:6940–46
    [Google Scholar]
  41. 41. 
    Keiski C-L, Harwich M, Jain S, Neculai AM, Yip P et al. 2010. AlgK is a TPR-containing protein and the periplasmic component of a novel exopolysaccharide secretin. Structure 18:2265–73
    [Google Scholar]
  42. 42. 
    Krasteva PV, Bernal-Bayard J, Travier L, Martin FA, Kaminski P-A et al. 2017. Insights into the structure and assembly of a bacterial cellulose secretion system. Nat. Commun. 8:12065
    [Google Scholar]
  43. 43. 
    Kuk ACY, Hao A, Guan Z, Lee S-Y 2019. Visualizing conformation transitions of the lipid II flippase MurJ. Nat. Commun. 10:11012
    [Google Scholar]
  44. 44. 
    Kumar A, Rao KM, Han SS 2018. Application of xanthan gum as polysaccharide in tissue engineering: a review. Carbohydr. Polym. 180:128–44
    [Google Scholar]
  45. 45. 
    Lairson LL, Henrissat B, Davies GJ, Withers SG 2008. Glycosyltransferases: structures, functions, and mechanisms. Annu. Rev. Biochem. 77:521–55
    [Google Scholar]
  46. 46. 
    Larson TR, Yother J. 2017. Streptococcus pneumoniae capsular polysaccharide is linked to peptidoglycan via a direct glycosidic bond to β-d-N-acetylglucosamine. PNAS 114:225695–700
    [Google Scholar]
  47. 47. 
    Larue K, Ford RC, Willis LM, Whitfield C 2011. Functional and structural characterization of polysaccharide co-polymerase proteins required for polymer export in ATP-binding cassette transporter-dependent capsule biosynthesis pathways. J. Biol. Chem. 286:1916658–68
    [Google Scholar]
  48. 48. 
    Le Quéré B, Ghigo J-M 2009. BcsQ is an essential component of the Escherichia coli cellulose biosynthesis apparatus that localizes at the bacterial cell pole. Mol. Microbiol. 72:3724–40
    [Google Scholar]
  49. 49. 
    Lebeer S, Verhoeven TLA, Francius G, Schoofs G, Lambrichts I et al. 2009. Identification of a gene cluster for the biosynthesis of a long, galactose-rich exopolysaccharide in Lactobacillus rhamnosus GG and functional analysis of the priming glycosyltransferase. Appl. Env. Microbiol. 75:113554–63
    [Google Scholar]
  50. 50. 
    Limoli DH, Jones CJ, Wozniak DJ 2015. Bacterial extracellular polysaccharides in biofilm formation and function. Microbiol. Spectr. 3:3 https://doi.org/10.1128/microbiolspec.MB-0011-2014
    [Crossref] [Google Scholar]
  51. 51. 
    Lin MH, Hsu TL, Lin SY, Pan YJ, Jan JT, Wang JT, Kooh KH, Wu SH 2009. Phosphoproteomics of Klebsiella pneumoniae NTUH-K2044 reveals a tight link between tyrosine phosphorylation and virulence. Mol. Cell. Proteomics. 8:122613–23
    [Google Scholar]
  52. 52. 
    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 1862:111394–403
    [Google Scholar]
  53. 53. 
    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 115:21E4870–79
    [Google Scholar]
  54. 54. 
    Liston SD, Ovchinnikova OG, Whitfield C 2016. Unique lipid anchor attaches Vi antigen capsule to the surface of Salmonella enterica serovar Typhi. PNAS 113:246719–24
    [Google Scholar]
  55. 55. 
    Litschko C, Oldrini D, Budde I, Berger M, Meens J et al. 2018. A new family of capsule polymerases generates teichoic acid-like capsule polymers in Gram-negative pathogens. mBio 9:3e00641–18
    [Google Scholar]
  56. 56. 
    Little DJ, Bamford NC, Pokrovskaya V, Robinson H, Nitz M, Howell PL 2014. Structural basis for the de-N-acetylation of poly-β-1,6-N-acetyl-d-glucosamine in Gram-positive bacteria. J. Biol. Chem. 289:5235907–17
    [Google Scholar]
  57. 57. 
    Little DJ, Li G, Ing C, DiFrancesco BR, Bamford NC et al. 2014. Modification and periplasmic translocation of the biofilm exopolysaccharide poly-β-1,6-N-acetyl-d-glucosamine. PNAS 111:3011013–18
    [Google Scholar]
  58. 58. 
    Little DJ, Pfoh R, Le Mauff F, Bamford NC, Notte C et al. 2018. PgaB orthologues contain a glycoside hydrolase domain that cleaves deacetylated poly-β(1,6)-N-acetylglucosamine and can disrupt bacterial biofilms. PLOS Pathog 14:4e1006998
    [Google Scholar]
  59. 59. 
    Low KE, Howell PL. 2018. Gram-negative synthase-dependent exopolysaccharide biosynthetic machines. Curr. Opin. Struct. Biol. 53:32–44
    [Google Scholar]
  60. 60. 
    Mann E, Whitfield C. 2016. A widespread three-component mechanism for the periplasmic modification of bacterial glycoconjugates. Can. J. Chem. 94:11883–93
    [Google Scholar]
  61. 61. 
    Marczak M, Mazur A, Koper P, Żebracki K, Skorupska A 2017. Synthesis of rhizobial exopolysaccharides and their importance for symbiosis with legume plants. Genes 8:12360
    [Google Scholar]
  62. 62. 
    Marmont LS, Whitfield GB, Rich JD, Yip P, Giesbrecht LB et al. 2017. PelA and PelB proteins form a modification and secretion complex essential for Pel polysaccharide-dependent biofilm formation in Pseudomonas aeruginosa. J. Biol. . Chem 292:4719411–22
    [Google Scholar]
  63. 63. 
    McNamara JT, Morgan JLW, Zimmer J 2015. A molecular description of cellulose biosynthesis. Annu. Rev. Biochem. 84:895–921
    [Google Scholar]
  64. 64. 
    McNulty C, Thompson J, Barrett B, Lord L, Andersen C, Roberts IS 2006. The cell surface expression of group 2 capsular polysaccharides in Escherichia coli: the role of KpsD, RhsA and a multi-protein complex at the pole of the cell. Mol. Microbiol. 59:3907–22
    [Google Scholar]
  65. 65. 
    Mendis HC, Madzima TF, Queiroux C, Jones KM 2016. Function of succinoglycan polysaccharide in Sinorhizobium meliloti host plant invasion depends on succinylation, not molecular weight. mBio 7:3619
    [Google Scholar]
  66. 66. 
    Micoli F, Costantino P, Adamo R 2018. Potential targets for next generation antimicrobial glycoconjugate vaccines. FEMS Microbiol. Rev. 42:3388–423
    [Google Scholar]
  67. 67. 
    Mijakovic I, Grangeasse C, Turgay K 2016. Exploring the diversity of protein modifications: special bacterial phosphorylation systems. FEMS Microbiol. Rev. 40:3398–417
    [Google Scholar]
  68. 68. 
    Morgan JLW, McNamara JT, Fischer M, Rich J, Chen H-M et al. 2016. Observing cellulose biosynthesis and membrane translocation in crystallo. . Nature 531:7594329–34
    [Google Scholar]
  69. 69. 
    Morgan JLW, Strumillo J, Zimmer J 2013. Crystallographic snapshot of cellulose synthesis and membrane translocation. Nature 493:7431181–86
    [Google Scholar]
  70. 70. 
    Mostowy RJ, Holt KE. 2018. Diversity-generating machines: genetics of bacterial sugar-coating. Trends Microbiol 26:121008–21
    [Google Scholar]
  71. 71. 
    Napiórkowska M, Boilevin J, Sovdat T, Darbre T, Reymond J-L et al. 2017. Molecular basis of lipid-linked oligosaccharide recognition and processing by bacterial oligosaccharyltransferase. Nat. Struct. Mol. Biol. 24:121100–6
    [Google Scholar]
  72. 72. 
    Nesper J, Hill CMD, Paiment A, Harauz G, Beis K et al. 2003. Translocation of group 1 capsular polysaccharide in Escherichia coli serotype K30: structural and functional analysis of the outer membrane lipoprotein Wza. J. Biol. Chem. 278:5049763–72
    [Google Scholar]
  73. 73. 
    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 111:228203–8
    [Google Scholar]
  74. 74. 
    Nojima S, Fujishima A, Kato K, Ohuchi K, Shimizu N et al. 2017. Crystal structure of the flexible tandem repeat domain of bacterial cellulose synthesis subunit C. Sci. Rep. 7:19
    [Google Scholar]
  75. 75. 
    Nourikyan J, Kjos M, Mercy C, Cluzel C, Morlot C et al. 2015. Autophosphorylation of the bacterial tyrosine-kinase CpsD connects capsule synthesis with the cell cycle in Streptococcus pneumoniae. . PLOS Genet 11:9e1005518
    [Google Scholar]
  76. 76. 
    Olivares-Illana V, Meyer P, Bechet E, Gueguen-Chaignon V, Soulat D et al. 2008. Structural basis for the regulation mechanism of the tyrosine kinase CapB from Staphylococcus aureus. . PLOS Biol 6:6e143
    [Google Scholar]
  77. 77. 
    Ostapska H, Howell PL, Sheppard DC 2018. Deacetylated microbial biofilm exopolysaccharides: It pays to be positive. PLOS Pathog 14:12e1007411
    [Google Scholar]
  78. 78. 
    Paton JC, Trappetti C. 2019. Streptococcus pneumoniae capsular polysaccharide. Microbiol. Spectr. 7:2 https://doi.org/10.1128/microbiolspec.GPP3-0019-2018
    [Crossref] [Google Scholar]
  79. 79. 
    Pavelka MS, Hayes SF, Silver RP 1994. Characterization of KpsT, the ATP-binding component of the BAC transporter involved in the export of capsular polysialic acid in Escherichia coli K1. J Biol Chem 269:3120149–58
    [Google Scholar]
  80. 80. 
    Phanphak S, Georgiades P, Li R, King J, Roberts IS, Waigh TA 2019. Super-resolution fluorescence microscopy study of the production of K1 capsules by Escherichia coli: evidence for the differential distribution of the capsule at the poles and the equator of the cell. Langmuir 35:165635–46
    [Google Scholar]
  81. 81. 
    Raetz CRH, Whitfield C. 2002. Lipopolysaccharide endotoxins. Annu. Rev. Biochem. 71:635–700
    [Google Scholar]
  82. 82. 
    Rausch M, Deisinger JP, Ulm H, Müller A, Li W et al. 2019. Coordination of capsule assembly and cell wall biosynthesis in Staphylococcus aureus. Nat. . Commun 10:11404
    [Google Scholar]
  83. 83. 
    Ray LC, Das D, Entova S, Lukose V, Lynch AJ et al. 2018. Membrane association of monotopic phosphoglycosyl transferase underpins function. Nat. Chem. Biol. 14:6538–41
    [Google Scholar]
  84. 84. 
    Rehman ZU, Wang Y, Moradali MF, Hay ID, Rehm BHA 2013. Insights into the assembly of the alginate biosynthesis machinery in Pseudomonas aeruginosa. Appl. Env. . Microbiol 79:103264–72
    [Google Scholar]
  85. 85. 
    Römling U, Galperin MY. 2015. Bacterial cellulose biosynthesis: diversity of operons, subunits, products, and functions. Trends Microbiol 23:9545–57
    [Google Scholar]
  86. 86. 
    Ruiz N. 2016. Filling holes in peptidoglycan biogenesis of Escherichia coli. Curr. Opin. Microbiol 34:1–6
    [Google Scholar]
  87. 87. 
    Sande C, Bouwman C, Kell E, Nickerson NN, Kapadia SB, Whitfield C 2019. Structural and functional variation in outer membrane polysaccharide export (OPX) proteins from the two major capsule assembly pathways present in Escherichia coli. J. Bacteriol 201:14e00213–19
    [Google Scholar]
  88. 88. 
    Schaefer K, Matano LM, Qiao Y, Kahne D, Walker S 2017. In vitro reconstitution demonstrates the cell wall ligase activity of LCP proteins. Nat. Chem. Biol. 13:4396–401
    [Google Scholar]
  89. 89. 
    Schmid J, Sieber V, Rehm B 2015. Bacterial exopolysaccharides: biosynthesis pathways and engineering strategies. Front. Microbiol. 6:496
    [Google Scholar]
  90. 90. 
    Schmidt H, Hansen G, Singh S, Hanuszkiewicz A, Lindner B et al. 2012. Structural and mechanistic analysis of the membrane-embedded glycosyltransferase WaaA required for lipopolysaccharide synthesis. PNAS 109:166253–58
    [Google Scholar]
  91. 91. 
    Schulz BL, Jen FEC, Power PM, Jones CE, Fox KL et al. 2013. Identification of bacterial protein O-oligosaccharyltransferases and their glycoprotein substrates. PLOS ONE 8:5e62768
    [Google Scholar]
  92. 92. 
    Sham L-T, Zheng S, Yakhnina AA, Kruse AC, Bernhardt TG 2018. Loss of specificity variants of WzxC suggest that substrate recognition is coupled with transporter opening in MOP‐family flippases. Mol. Microbiol. 109:5633–41
    [Google Scholar]
  93. 93. 
    Spiers AJ, Bohannon J, Gehrig SM, Rainey PB 2003. Biofilm formation at the air-liquid interface by the Pseudomonas fluorescens SBW25 wrinkly spreader requires an acetylated form of cellulose. Mol. Microbiol. 50:115–27
    [Google Scholar]
  94. 94. 
    Sun L, Vella P, Schnell R, Polyakova A, Bourenkov G et al. 2018. Structural and functional characterization of the BcsG subunit of the cellulose synthase in Salmonella typhimurium. J. Mol. . Biol 430:183170–89
    [Google Scholar]
  95. 95. 
    Sutherland IW. 1998. Novel and established applications of microbial polysaccharides. Trends Biotechnol 16:141–46
    [Google Scholar]
  96. 96. 
    Tan J, Rouse SL, Li D, Pye VE, Vogeley L et al. 2014. A conformational landscape for alginate secretion across the outer membrane of Pseudomonas aeruginosa. Acta Crystallogr. D 70:82054–68
    [Google Scholar]
  97. 97. 
    Temel DB, Dutta K, Alphonse SEB, Nourikyan J, Grangeasse C, Ghose R 2013. Regulatory interactions between a bacterial tyrosine kinase and its cognate phosphatase. J. Biol. Chem. 288:2115212–28
    [Google Scholar]
  98. 98. 
    Thongsomboon W, Serra DO, Possling A, Hadjineophytou C, Hengge R, Cegelski L 2018. Phosphoethanolamine cellulose: a naturally produced chemically modified cellulose. Science 359:6373334–38
    [Google Scholar]
  99. 99. 
    Tocilj A, Munger C, Proteau A, Morona R, Purins L et al. 2009. Bacterial polysaccharide co-polymerases share a common framework for control of polymer length. Nat. Struct. Mol. Biol. 15:130–38
    [Google Scholar]
  100. 100. 
    Toniolo C, Balducci E, Romano MR, Proietti D, Ferlenghi I et al. 2015. Streptococcus agalactiae capsule polymer length and attachment is determined by the proteins CpsABCD. J. Biol. Chem. 290:159521–32
    [Google Scholar]
  101. 101. 
    Toukach PV, Egorova KS. 2016. Carbohydrate structure database merged from bacterial, archaeal, plant and fungal parts. Nucl Acids Res 44:D1D1229–36
    [Google Scholar]
  102. 102. 
    Valentini M, Filloux A. 2019. Multiple roles of c-di-GMP signaling in bacterial pathogenesis. Annu. Rev. Microbiol. 73:387–406
    [Google Scholar]
  103. 103. 
    Wall E, Majdalani N, Gottesman S 2018. The complex Rcs regulatory cascade. Annu. Rev. Microbiol. 72:111–39
    [Google Scholar]
  104. 104. 
    Whitfield C. 2006. Biosynthesis and assembly of capsular polysaccharides in Escherichia coli. Annu. Rev. . Biochem 75:39–68
    [Google Scholar]
  105. 105. 
    Whitfield C, Szymanski CM, Aebi M 2015. Eubacteria. Essentials of Glycobiology A Varki, RD Cummings, JD Esko, P Stanley, GW Hart et al.265–82 Cold Spring Harbor, NY: Cold Spring Harb. Lab. Press. , 3rd ed..
    [Google Scholar]
  106. 106. 
    Whitfield C, Vimr ER, Costerton JW, Troy FA 1984. Protein synthesis is required for in vivo activation of polysialic acid capsule synthesis in Escherichia coli K1. J. Bacteriol. 159:1321–28
    [Google Scholar]
  107. 106a. 
    Whitfield C, Williams DM, Kelly SD 2020. Lipopolysaccharide O-antigens—bacterial glycans made to measure. J. Biol. Chem In press. https://doi.org/10.1074/jbc.REV120.009402
    [Crossref] [Google Scholar]
  108. 107. 
    Whitfield GB, Marmont LS, Bundalovic-Torma C, Razvi E, Roach EJ et al. 2019. Discovery and characterization of a Gram-positive Pel polysaccharide biosynthetic gene cluster. bioRxiv 768473
  109. 108. 
    Whitfield GB, Marmont LS, Howell PL 2015. Enzymatic modifications of exopolysaccharides enhance bacterial persistence. Front. Microbiol. 6:471
    [Google Scholar]
  110. 109. 
    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 110:197868–73
    [Google Scholar]
  111. 110. 
    Willis LM, Whitfield C. 2013. Structure, biosynthesis, and function of bacterial capsular polysaccharides synthesized by ABC transporter-dependent pathways. Carbohydr. Res. 378:35–44
    [Google Scholar]
  112. 111. 
    Wolfram F, Kitova EN, Robinson H, Walvoort MTC, Codée JDC et al. 2014. Catalytic mechanism and mode of action of the periplasmic alginate epimerase AlgG. J. Biol. Chem. 289:96006–19
    [Google Scholar]
  113. 112. 
    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. 6:6418–23
    [Google Scholar]
  114. 113. 
    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 276:42361–71
    [Google Scholar]
  115. 114. 
    Wyres KL, Wick RR, Gorrie C, Jenney A, Follador R et al. 2016. Identification of Klebsiella capsule synthesis loci from whole genome data. Microb. Genom. 2:12e000102
    [Google Scholar]
  116. 115. 
    Xu R-R, Yang W-D, Niu K-X, Wang B, Wang W-M 2018. An update on the evolution of glucosyltransferase (Gtf) genes in Streptococcus. Front. . Microbiol 9:989
    [Google Scholar]
  117. 116. 
    Yother J. 2011. Capsules of Streptococcus pneumoniae and other bacteria: paradigms for polysaccharide biosynthesis and regulation. Annu. Rev. Microbiol. 65:563–81
    [Google Scholar]
  118. 117. 
    Zeidan AA, Poulsen VK, Janzen T, Buldo P, Derkx PMF et al. 2017. Polysaccharide production by lactic acid bacteria: from genes to industrial applications. FEMS Microbiol. Rev. 41:Supp. 1S168–200
    [Google Scholar]
  119. 118. 
    Zhang R, Edgar KJ. 2014. Properties, chemistry, and applications of the bioactive polysaccharide curdlan. Biomacromolecules 15:41079–96
    [Google Scholar]
  120. 119. 
    Zhao G, Wu B, Li L, Wang PG 2014. O-antigen polymerase adopts a distributive mechanism for lipopolysaccharide biosynthesis. Appl. Microbiol. Biotechnol. 98:94075–81
    [Google Scholar]
  121. 120. 
    Zheng S, Sham L-T, Rubino FA, Brock KP, Robins WP et al. 2018. Structure and mutagenic analysis of the lipid II flippase MurJ from Escherichia coli. . PNAS 115:266709–14
    [Google Scholar]
  122. 121. 
    Zhou Y, Cui Y, Qu X 2019. Exopolysaccharides of lactic acid bacteria: structure, bioactivity and associations; a review. Carbohydr. Polym. 207:317–32
    [Google Scholar]
/content/journals/10.1146/annurev-micro-011420-075607
Loading
/content/journals/10.1146/annurev-micro-011420-075607
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