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Protein and Sugar Export and Assembly in Gram-positive Bacteria pp 95–128Cite as

Membrane Translocation and Assembly of Sugar Polymer Precursors

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Part of the book series: Current Topics in Microbiology and Immunology ((CT MICROBIOLOGY,volume 404))

Abstract

Bacterial polysaccharides play an essential role in cell viability, virulence, and evasion of host defenses. Although the polysaccharides themselves are highly diverse, the pathways by which bacteria synthesize these essential polymers are conserved in both Gram-negative and Gram-positive organisms. By utilizing a lipid linker, a series of glycosyltransferases and integral membrane proteins act in concert to synthesize capsular polysaccharide, teichoic acid, and teichuronic acid. The pathways used to produce these molecules are the Wzx/Wzy-dependent, the ABC-transporter-dependent, and the synthase-dependent pathways. This chapter will cover the initiation, synthesis of the various polysaccharides on the cytoplasmic face of the membrane using nucleotide sugar precursors, and export of the nascent chain from the cytoplasm to the extracellular milieu. As microbial glycobiology is an emerging field in Gram-positive bacteria research, parallels will be drawn to the more widely studied polysaccharide biosynthesis systems in Gram-negative species in order to provide greater understanding of these biologically significant molecules.

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Abbreviations

PG:

Peptidoglycan

CPS:

Capsular polysaccharide

Und-P:

Undecaprenyl phosphate

Und-PP:

Undecaprenyl pyrophosphate

GlcNAc:

N-acetylglucosamine

ManNAc:

N-acetylmannuronic acid

MurNAc:

N-acetylmuramic acid

UDP-Glc:

UDP-glucose

TMR:

Tetramethylrhodamine cadaverine

TMS:

Transmembrane segment

MOP:

Multidrug/oligosaccharidyl-lipid/polysaccharide

MATE:

Multidrug and toxin extrusion

MTSES:

2-sulfonatoethyl methanethiosulfonate

MVF:

Mouse virulence factor

NBD:

7-nitro-2,1,3-benzoxadiazol-4-yl

PHPT:

Polyprenyl-phosphate hexose-1-phosphate transferase

PST:

Polysaccharide transporter

LCP:

LytR-CpsA-Psr

Rha:

Rhamnose

TA:

Teichoic acid

LTA:

Lipoteichoic acid

WTA:

Wall teichoic acid

GlcA:

Uronic acid

TUA:

Teichuronic acid

glycerol-3-P:

Glycerol-3-phosphate

ribitol-3-P:

Ribitol-3-phosphate

References

  • Alexeyev MF, Winkler HH (1999) Membrane topology of the Rickettsia prowazekii ATP/ADP translocase revealed by novel dual pho-lac reporters. J Mol Biol 285:1503–1513

    Article  CAS  PubMed  Google Scholar 

  • Aravind L, Koonin EV (1998) Phosphoesterase domains associated with DNA polymerases of diverse origins. Nucleic Acids Res 26:3746–3752

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Atilano ML, Pereira PM, Yates J, Reed P, Veiga H, Pinho MG, Filipe SR (2010) Teichoic acids are temporal and spatial regulators of peptidoglycan cross-linking in Staphylococcus aureus. PNAS 107:18991–18996

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bender MH, Yother J (2001) CpsB is a modulator of capsule-associated tyrosine kinase activity in Streptococcus pneumoniae

    Google Scholar 

  • Bender MH, Cartee RT, Yother J (2003) Positive correlation between tyrosine phosphorylation of CpsD and capsular polysaccharide production in Streptococcus pneumoniae positive correlation between tyrosine phosphorylation of CpsD and capsular polysaccharide production in Streptococcus pneumoniae. J Bacteriol 185:6057–6066

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bentley SD, Aanensen DM, Mavroidi A et al (2006) Genetic analysis of the capsular biosynthetic locus from all 90 pneumococcal serotypes. PLoS Genet 2:e31

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bhavsar AP, D’Elia MA, Sahakian TD, Brown ED (2007) The amino terminus of Bacillus subtilis TagB possesses separable localization and functional properties. J Bacteriol 189:6816–6823

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Botella E, Devine SK, Hubner S et al (2014) PhoR autokinase activity is controlled by an intermediate in wall teichoic acid metabolism that is sensed by the intracellular PAS domain during the PhoPR-mediated phosphate limitation response of Bacillus subtilis. Mol Microbiol 94:1242–1259

    Article  CAS  PubMed  Google Scholar 

  • Brown S, Zhang Y-H, Walker S (2008) A Revised Pathway Proposed for Staphylococcus aureus wall teichoic acid biosynthesis based on in vitro reconstitution of the intracellular steps. Chem Biol 15:12–21

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brown S, Meredith T, Swoboda J, Walker S (2010) Staphylococcus aureus and Bacillus subtilis W23 make polyribitol wall teichoic acids using different enzymatic pathways. Chem Biol 17:1101–1110

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brown S, Santa Maria JP, Walker S (2013) Wall teichoic acids of gram-positive bacteria. Annu Rev Microbiol 67:313–336

    Article  CAS  PubMed  Google Scholar 

  • Burrows LL, Lam JS (1999) Effect of wzx (rfbX) mutations on A-band and B-band lipopolysaccharide biosynthesis in Pseudomonas aeruginosa O5. J Bacteriol 181:973–980

    CAS  PubMed  PubMed Central  Google Scholar 

  • Butler EK, Davis RM, Bari V, Nicholson PA, Ruiz N (2013) Structure-function analysis of MurJ reveals a solvent-exposed cavity containing residues essential for peptidoglycan biogenesis in Escherichia coli. J Bacteriol 195:4639–4649

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Butler EK, Tan WB, Joseph H, Ruiz N (2014) Charge requirements of Lipid II flippase activity in Escherichia coli. J Bacteriol 196:4111–4119

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Campbell JA, Davies GJ, Bulone V, Henrissat B (1998) A classification of nucleotide-diphospho-sugar glycosyltransferases based on amino acid sequence similarities. Biochem J 329:719

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cartee RT, Forsee WT, Jensen JW, Yother J (2001) Expression of the Streptococcus pneumoniae type 3 synthase in Escherichia coli: assembly of th type 3 polysaccharide on a lipid primer. J Biol Chem 276:48831–48839

    Article  CAS  PubMed  Google Scholar 

  • Cartee RT, Forsee WT, Yother J (2005a) Initiation and synthesis of the Streptococcus pneumoniae type 3 capsule on a phosphatidylglycerol membrane anchor. J Bacteriol 187:4470–4479

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cartee RT, Forsee WT, Bender MH, Ambrose KD, Yother J (2005b) CpsE from type 2 Streptococcus pneumoniae catalyzes the reversible addition of Glucose-1-Phosphate to a polyprenyl phosphate acceptor, initiating type 2 Capsule repeat unit formation. J Bacteriol 187:7425–7433

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cefalo AD, Broadbent JR, Welker DL (2011) Protein–protein interactions among the components of the biosynthetic machinery responsible for exopolysaccharide production in Streptococcus thermophilus MR-1C. J Appl Microbiol 110:801–812

    Article  CAS  PubMed  Google Scholar 

  • Chan YGY, Frankel MB, Dengler V, Schneewind O, Missiakasa D (2013) Staphylococcus aureus mutants lacking the lytr-cpsa-Psr family of enzymes release cell wall teichoic acids into the extracellular medium. J Bacteriol 195:4650–4659

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chan YGY, 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 289:15680–15690

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Cieslewicz MJ, Kasper DL, Wang Y, Wessels MR (2001) Functional analysis in type Ia group B Streptococcus of a cluster of genes involved in extracellular polysaccharide production by diverse species of Streptococci. J Biol Chem 276:139–146

    Article  CAS  PubMed  Google Scholar 

  • Damjanovic M, Kharat AS, Eberhardt A, Tomasz A, Vollmer W (2007) The Essential tacF gene is responsible for the choline-dependent growth phenotype of Streptococcus pneumoniae. J Bacteriol 189:7105–7111

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Denapaite D, Hakenbeck R (2012) Biosynthesis of teichoic acids in Streptococcus pneumoniae and closely related species. Microb Drug Resist 18:344–358

    Article  CAS  PubMed  Google Scholar 

  • Denapaite D, Brückner R, Hakenbeck R, Vollmer W (2012) Biosynthesis of teichoic acids in Streptococcus pneumoniae and closely related species: lessons from genomes. Microb Drug Resist. 18:344–358

    Article  CAS  PubMed  Google Scholar 

  • Deng LL, Alexander AA, Lei S, Anderson JS (2010) The cell wall teichuronic acid synthetase (TUAS) Is an enzyme complex located in the cytoplasmic membrane of Micrococcus luteus. Biochem Res Int 2010:395758

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Dillard JP, Vandersea MW, Yother J (1995) Characterization of the cassette containing genes for type 3 capsular polysaccharide biosynthesis in Streptococcus pneumoniae. J Exp Med 181:973–983

    Article  CAS  PubMed  Google Scholar 

  • Eberhardt A, Hoyland CN, Vollmer D et al (2012) Attachment of capsular polysaccharide to the cell wall in Streptococcus pneumoniae. Microb Drug Resist (Larchmont, N.Y.) 18:240–255

    Google Scholar 

  • Ellwood DC, Tempest DW (1969) Control of teichoic acid and teichuronic acid biosynthesis in chemostat cultures of Bacillus subtilis var. niger. Biochem J 111:1–5

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Elumalai P, Rajasekaran M, Liu HL, Chen C (2010) Investigation of cation-Pi interactions in sugar-binding proteins. Protoplasma 247:13–24

    Article  CAS  PubMed  Google Scholar 

  • Fay A, Dworkin J (2009) Bacillus subtilis homologs of MviN (MurJ), the putative Escherichia coli lipid II flippase, are not essential for growth. J Bacteriol 191:6020–6028

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 274:35129–35138

    Article  CAS  PubMed  Google Scholar 

  • Fischer W (1990) Bacterial phosphoglycolipids and lipoteichoic acids. In: Kates M (ed) Glycolipids, phosphoglycolipids, and sulfoglycolipids, vol 6. Springer, US, pp 123–234

    Google Scholar 

  • Fischer H, Tomasz A (1985) Peptidoglycan cross-linking and teichoic acid attachment in Streptococcus pneumoniae. J Bacteriol 163:46–54

    CAS  PubMed  PubMed Central  Google Scholar 

  • Forsee WT, Cartee RT, Yother J (2006) Role of the carbohydrate binding site of the Streptococcus pneumoniae capsular polysaccharide type 3 synthase in the transition from oligosaccharide to polysaccharide synthesis. J Biol Chem 281:6283–6289

    Article  CAS  PubMed  Google Scholar 

  • Forsee WT, Cartee RT, Yother J (2009) Characterization of the lipid linkage region and chain length of the cellubiuronic acid capsule of Streptococcus pneumoniae. J Biol Chem 284:11826–11835

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Furlong SE, Ford A, Albarnez-Rodriguez L, Valvano MA (2015) Topological analysis of the Escherichia coli WcaJ protein reveals a new conserved configuration for the polyisoprenyl-phosphate hexose-1-phosphate transferase family. Sci Rep 5:9178. doi:10.1038/srep09178

  • Geno KA, Hauser JR, Gupta K, Yother J (2014) Streptococcus pneumoniae phosphotyrosine phosphatase CpsB and alterations in capsule production resulting from changes in oxygen availability. J Bacteriol 196:1992–2003

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ghosh A, Chaudhary SA, Apurva SR et al (2013) Whole-genome sequencing of Micrococcus luteus strain modasa, of Indian origin. Genome Announc 1:e00076–e00013

    Article  PubMed Central  Google Scholar 

  • Ghuysen JM, Hakenbeck R (1994) Bacterial cell wall. Elsevier Science, Amsterdam

    Google Scholar 

  • Ginsberg C, Zhang Y-H, Yuan Y, Walker S (2006) In vitro reconstitution of two essential steps in wall teichoic acid biosynthesis. ACS Chem Biol 1:25–28

    Article  CAS  PubMed  Google Scholar 

  • Gisch N, Kohler T, Ulmer AJ et al (2013) Structural reevaluation of Streptococcus pneumoniae lipoteichoic acid and new insights into its immunostimulatory potency. J Biol Chem 288:15654–15667

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • González A, Llull D, Morales M, García P, García E (2008) Mutations in the tacF gene of clinical strains and laboratory transformants of Streptococcus pneumoniae: impact on choline auxotrophy and growth rate. J Bacteriol 190:4129–4138

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Grant WD (1979) Cell wall teichoic acid as a reserve phosphate source in Bacillus subtilis. J Bacteriol 137:35–43

    CAS  PubMed  PubMed Central  Google Scholar 

  • Guidolin A, Morona JK, Morona R, Hansman D, Paton JC (1994) Nucleotide sequence analysis of genes essential for capsular polysaccharide biosynthesis in Streptococcus pneumoniae type 19F. Infect Immun 62:5384–5396

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 392:678–688

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hancock IC, Wiseman G, Baddiley J (1976) Biosynthesis of the unit that links teichoic acid to the bacterial wall: inhibition by tunicamycin. FEBS Lett 69:75–80

    Article  CAS  PubMed  Google Scholar 

  • Hanson BR, Lowe BA, Neely MN (2011) Membrane topology and DNA-binding ability of the Streptococcal CpsA protein. J Bacteriol 193:411–420

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Hase S, Matsushima Y (1972) Structural studies on a glucose-containing polysaccharide obtained from cell walls of Micrococcus lysodeikticus: III. Determination of the structure. J Biochem 72:1117–1128

    Article  CAS  PubMed  Google Scholar 

  • He X, Szewczyk P, Karyakin A, Evin M, Hong W-X, Zhang Q, Chang G (2010) Structure of a cation-bound multidrug and toxic compound extrusion transporter. Nature 467:991–994

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Henrichfreise B, Schiefer A, Schneider T et al (2009) Functional conservation of the lipid II biosynthesis pathway in the cell wall-less bacteria chlamydia and wolbachia: why is lipid II needed? Mol Microbiol 73:913–923

    Article  CAS  PubMed  Google Scholar 

  • Henrichsen J (1995) Six newly recognized types of Streptococcus pneumoniae. J Clin Microbiol 33:2759–2762

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hildebrandt KM, Anderson JS (1990) Biosynthetic elongation of isolated teichuronic acid polymers via glucosyl- and N-acetylmannosaminuronosyl transferases from solubilized cytoplasmic membrane fragments of Micrococcus luteus. J Bacteriol 172:5160–5164

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Höltje J-V (1998) Growth of the stress-bearing and shape-maintaining murein sacculus of Escherichia coli. Microbiol Mol Biol Rev 62:181–203

    PubMed  PubMed Central  Google Scholar 

  • Honeyman AL, Stewart GC (1989) The nucleotide sequence of the rodC operon of Bacillus subtilis. Mol Microbiol 3:1257–1268

    Article  CAS  PubMed  Google Scholar 

  • Hong Y, Reeves PR (2014) Diversity of O-Antigen repeat unit structures can account for the substantial sequence variation of Wzx translocases. J Bacteriol 196:1713–1722

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hong Y, Cunneen MM, Reeves PR (2012) The Wzx translocases for Salmonella enterica O-antigen processing have unexpected serotype specificity. Mol Microbiol 1–11

    Google Scholar 

  • Hübscher J, Lüthy L, Berger-bächi B, Stutzmann P (2008) Phylogenetic distribution and membrane topology of the LytR-CpsA-Psr protein family. BMC Genom 16:1–16

    Google Scholar 

  • Hulett FM (1996) The signal-transduction network for Pho regulation in Bacillus subtilis. Mol Microbiol 19:933–939

    Article  CAS  PubMed  Google Scholar 

  • Hvorup RN, Winnen B, Chang AB, Jiang Y, Zhou X-F, Saier MH (2003a) The multidrug/oligosaccharidyl-lipid/polysaccharide (MOP) exporter superfamily. Eur J Biochem 270:799–813

    Article  CAS  PubMed  Google Scholar 

  • Hvorup RN, Winnen B, Chang AB, Jiang Y, Zhou X-F, Saier MH (2003b) The multidrug/oligosaccharidyl-lipid/polysaccharide (MOP) exporter superfamily. Fed Eur Biochem Soc J 270:799–813

    Article  CAS  Google Scholar 

  • Iannelli F, Pearce BJ, Pozzi G (1999) The type 2 capsule locus of Streptococcus pneumoniae. J Bacteriol 181:2652–2654

    CAS  PubMed  PubMed Central  Google Scholar 

  • Inoue A, Murata Y, Takahashi H, Tsuji N, Fujisaki S, Kato JI (2008) Involvement of an essential gene, mviN, in murein synthesis in Escherichia coli. J Bacteriol 190:7298–7301

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Islam ST, Lam JS (2013) Topological mapping methods for α-helical bacterial membrane proteins—an update and a guide. MicrobiologyOpen 2:350–64

    Google Scholar 

  • Islam ST, Lam JS (2014) Synthesis of bacterial polysaccharides via the Wzx/Wzy-dependent pathway. Can J Microbiol 60:697–716

    Article  CAS  PubMed  Google Scholar 

  • 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(3):e00189–10. doi: 10.1128/mBio.00189-10

  • Islam ST, Gold AC, Taylor VL, Anderson EM, Ford RC, Lam JS (2011) Dual conserved periplasmic loops possess essential charge characteristics that support a catch-and-release mechanism of O-antigen polymerization by Wzy in Pseudomonas aeruginosa PAO1. J Biol Chem 286:20600–20605

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Islam ST, Fieldhouse RJ, Anderson EM, Taylor VL, Keates RAB, Ford RC, Lam JS (2012a) A cationic lumen in the Wzx flippase mediates anionic O-antigen subunit translocation in Pseudomonas aeruginosa PAO1. Mol Microbiol 84:1165–1176

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Islam ST, Fieldhouse RJ, Anderson EM, Taylor VL, Keates RAB, Ford RC, Lam JS (2012b) A cationic lumen in the Wzx flippase mediates anionic O-antigen subunit translocation in Pseudomonas aeruginosa PAO1. Mol Microbiol 84:1165–1176

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Islam ST, Huszczynski SM, Nugent T, Gold AC, Lam JS (2013) Conserved-residue mutations in Wzy affect O-antigen polymerization and Wzz-mediated chain-length regulation in Pseudomonas aeruginosa PAO1. Sci Rep 3:3441. doi: 10.1038/srep03441

  • Islam ST, Eckford PDW, Jones ML, Nugent T, Bear CE, Vogel C, Lam JS (2013) Proton-dependent gating and proton uptake by Wzx support O-antigen-subunit antiport across the bacterial inner membrane. mBio 4(5): e00678–13. doi: 10.1128/mBio.00678-13

  • James DBA, Yother J (2012) Genetic and biochemical characterizations of enzymes involved in Streptococcus pneumoniae serotype 2 capsule synthesis demonstrate that Cps2T (WchF) catalyzes the committed step by addition of β1-4 rhamnose, the second sugar residue in the repeat unit. J Bacteriol 194:6479–6489

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • James DBA, Gupta K, Hauser JR, Yother J (2013) Biochemical activities of Streptococcus pneumoniae serotype 2 capsular glycosyltransferases and significance of suppressor mutations affecting the initiating glycosyltransferase Cps2E. J Bacteriol 195:5469–5478

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Johnson GL, Hoger JH, Ratnayake JH, Anderson JS (1984) Characterization of three intermediates in the biosynthesis of teichuronic acid of Micrococcus luteus. Arch Biochem Biophys 235:679–691

    Article  CAS  PubMed  Google Scholar 

  • Kawai Y, Marles-Wright J, Cleverley RM et al (2011) A widespread family of bacterial cell wall assembly proteins. EMBO J 30:4931–4941

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kolkman MA, Morrison DA, Van Der Zeijst BA, Nuijten PJ (1996) The capsule polysaccharide synthesis locus of Streptococcus pneumoniae serotype 14: identification of the glycosyl transferase gene cps14E. J Bacteriol 178:3736–3741

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kolkman MAB, van der Zeijst BAM, Nuijten PJM (1998) Diversity of capsular polysaccharide synthesis gene clusters in Streptococcus pneumoniae. J Biochem 123:937–945

    Article  CAS  PubMed  Google Scholar 

  • Kuroda T, Tsuchiya T (2009) Multidrug efflux transporters in the MATE family. Biochim Biophys Acta 1794:763–768

    Article  CAS  PubMed  Google Scholar 

  • Lazarevic V, Mauël C, Soldo B, Freymond P-P, Margot P, Karamata D (1995) Sequence analysis of the 308° to 311° segment of the Bacillus subtilis 168 chromosome, a region devoted to cell wall metabolism, containing non-coding grey holes which reveal chromosomal rearrangements. Microbiology 141:329–335

    Article  CAS  PubMed  Google Scholar 

  • Lin WS, Cunneen T, Lee CY (1994) Sequence analysis and molecular characterization of genes required for the biosynthesis of type 1 capsular polysaccharide in Staphylococcus aureus. J Bacteriol 176:7005–7016

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu W, Hulett FM (1998) Comparison of PhoP binding to the tuaA promoter with PhoP binding to other Pho-regulon promoters establishes a Bacillus subtilis Pho core binding site. Microbiology 144:1443–1450

    Article  CAS  PubMed  Google Scholar 

  • Liu MA, Stent TL, Hong Y, Reeves PR (2015) Inefficient translocation of a truncated O unit by a Salmonella Wzx affects both O-antigen production and cell growth. FEMS Microbiol Lett 1–7

    Google Scholar 

  • Lovering AL, Lin LYC, Sewell EW, Spreter T, Brown ED, Strynadka NCJ (2010) Structure of the bacterial teichoic acid polymerase TagF provides insights into membrane association and catalysis. Nat Struct Mol Biol 17:582–589

    Article  CAS  PubMed  Google Scholar 

  • Lunderberg JM, Liszewski Zilla M, Missiakas D, Schneewind O (2015) Bacillus anthracis tagO Is required for vegetative growth and secondary cell wall polysaccharide synthesis. J Bacteriol 197:3511–3520

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Malik A, Ahmad S (2007) Sequence and structural features of carbohydrate binding in proteins and assessment of predictability using a neural network. BMC Struct Biol 7:1

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Manat G, Roure S, Auger R, Bouhss A, Barreteau H, Mengin-Lecreulx D, Touzé T (2014) Deciphering the metabolism of undecaprenyl-phosphate: the bacterial cell-wall unit carrier at the membrane frontier. Microb Drug Resist 20:199–214

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 (Reading, England) 150:4095–4105

    Google Scholar 

  • Mauël C, Young M, Margot P, Karamata D (1989) The essential nature of teichoic acids in Bacillus subtilis as revealed by insertional mutagenesis. Mol Gen Genet 215:388–394

    Article  PubMed  Google Scholar 

  • Mauël C, Young M, Karamata D (1991) Genes concerned with synthesis of poly(glycerol phosphate), the essential teichoic acid in Bacillus subtilis strain 168, are organized in two divergent transcription units. J Gen Microbiol 137:929–941

    Article  PubMed  Google Scholar 

  • Meeske AJ, L-T Sham, Kimsey H, B-M Koo, Gross CA, Bernhardt TG (2015) MurJ and a novel lipid II flippase are required for cell wall biogenesis in Bacillus subtilis. PNAS 112:6437–6442

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Miyafusa T, Caaveiro JMM, Tanaka Y, Tsumoto K (2013) Dynamic elements govern the catalytic activity of CapE, a capsular polysaccharide-synthesizing enzyme from Staphylococcus aureus. FEBS Lett 587:3824–3830

    Article  CAS  PubMed  Google Scholar 

  • Mohammadi T, van Dam V, Sijbrandi R et al (2011) Identification of FtsW as a transporter of lipid-linked cell wall precursors across the membrane. The EMBO J 30:1425–1432

    Article  CAS  PubMed  Google Scholar 

  • Mohammadi T, Sijbrandi R, Lutters M et al (2014) Specificity of the transport of lipid II by FtsW in Escherichia coli. J Biol Chem 289:14707–14718

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moreau M, Richards JC, Fournier J-M, Byrd RA, Karakawa WW, Vann WF (1990) Structure of the type 5 capsular polysaccharide of Staphylococcus aureus. Carbohydr Res 201:285–297

    Article  CAS  PubMed  Google Scholar 

  • Morona JK, Morona R, Paton JC (1999) Analysis of the 5′ portion of the type 19A capsule locus identifies two classes of cpsC, cpsD, and cpsE Genes in Streptococcus pneumoniae. J Bacteriol 181:3599–3605

    CAS  PubMed  PubMed Central  Google Scholar 

  • Morona JK, Paton JC, Miller DC, Morona R (2000) Tyrosine phosphorylation of CpsD negatively regulates capsular polysaccharide biosynthesis in Streptococcus pneumoniae. Mol Microbiol 35:1431–1442

    Article  CAS  PubMed  Google Scholar 

  • Morona JK, Morona R, Miller DC, Paton JC (2002) Streptococcus pneumoniae capsule biosynthesis protein CpsB is a novel manganese-dependent phosphotyrosine-protein phosphatase. J Bacteriol 184:577–583

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Morona JK, Morona R, Miller DC, Paton JC (2003) Mutational analysis of the carboxy-terminal (YGX)4 repeat domain of CpsD, an autophosphorylating tyrosine kinase required for capsule biosynthesis in Streptococcus pneumoniae. J Bacteriol 185:3009–3019

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Morona JK, Morona R, Paton JC (2006) Attachment of capsular polysaccharide to the cell wall of Streptococcus pneumoniae type 2 is required for invasive disease. Proc Natl Acad Sci USA 103:8505–8510

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nath P, Morona R (2015) Mutational analysis of the major periplasmic loops of Shigella flexneri Wzy: identification of the residues affecting O antigen modal chain length control, and Wzz-dependent polymerization activity. Microbiology 161:774–785

    Article  CAS  PubMed  Google Scholar 

  • 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 111:8203–8208

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nikolaidis I, Favini-Stabile S, Dessen A (2014) Resistance to antibiotics targeted to the bacterial cell wall. Protein Sci 23:243–259

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Olivares-Illana V, Meyer P, Bechet E et al (2008) Structural basis for the regulation mechanism of the tyrosine kinase CapB from Staphylococcus aureus. PLoS Biol 6:1321–1331

    Article  CAS  Google Scholar 

  • Pagni M, Lazarevic V, Soldo B, Karamata D (1999) Assay for UDPglucose 6-dehydrogenase in phosphate-starved cells: gene tuaD of Bacillus subtilis 168 encodes the UDPglucose 6-dehydrogenase involved in teichuronic acid synthesis. Microbiology 145:1049–1053

    Article  CAS  PubMed  Google Scholar 

  • Pelosi L, Boumedienne M, Saksouk N, Geiselmann J, Geremia RA (2005) The glucosyl-1-phosphate transferase WchA (Cap8E) primes the capsular polysaccharide repeat unit biosynthesis of Streptococcus pneumoniae serotype 8. Biochem Biophys Res Commun 327:857–865

    Article  CAS  PubMed  Google Scholar 

  • Pereira MP, Schertzer JW, D’Elia MA, Koteva KP, Hughes DW, Wright GD, Brown ED (2008) The wall teichoic acid polymerase TagF efficiently synthesizes poly(glycerol phosphate) on the TagB product lipid III. ChemBioChem 9:1385–1390

    Article  CAS  PubMed  Google Scholar 

  • Qi Y, Hulett FM (1998) Role of PhoP ∼ P in transcriptional regulation of genes involved in cell wall anionic polymer biosynthesis in Bacillus subtilis. J Bacteriol 180:4007–4010

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rahim R, Burrows LL, Monteiro MA, Perry MB, Lam JS (2000) Involvement of the rml locus in core oligosaccharide and O polysaccharide assembly in Pseudomonas aeruginosa. Microbiology 146:2803–2814

    Article  CAS  PubMed  Google Scholar 

  • Reichmann NT, Gründling 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Roman E, Roberts I, Lidholt K, Kusche-Gullberg M (2003) Overexpression of UDP-glucose dehydrogenase in Escherichia coli results in decreased biosynthesis of K5 polysaccharide. Biochem J 374:767–772

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rowe HM, Hanson BR, Runft DL, Lin Q, Firestine SM, Neely MN (2015) Modification of the CpsA protein reveals a role in alteration of the Streptococcus agalactiae cell envelope. Infect Immun 83:1497–1506

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rudnick PA, Arcondéguy T, Kennedy CK, Kahn D (2001) glnD and mviN are genes of an essential operon in Sinorhizobium meliloti. J Bacteriol 183:2682–2685

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ruiz N (2008) Bioinformatics identification of MurJ (MviN) as the peptidoglycan lipid II flippase in Escherichia coli. PNAS 105:15553–15557

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Saldías MS, Patel K, Marolda CL, Bittner M, Contreras I, Valvano MA (2008) Distinct functional domains of the Salmonella enterica WbaP transferase that is involved in the initiation reaction for synthesis of the O antigen subunit. Microbiology 154:440–453

    Article  PubMed  CAS  Google Scholar 

  • Sau S, Bhasin N, Wann ER, Lee JC, Foster TJ, Lee CY (1997) The Staphylococcus aureus allelic genetic loci for serotype 5 and 8 capsule expression contain the type-specific genes flanked by common genes. Microbiology 143:2395–2405

    Article  CAS  PubMed  Google Scholar 

  • Schertzer JW, Bhavsar AP, Brown ED (2005) Two conserved histidine residues are critical to the function of the TagF-like family of enzymes. J Biol Chem 280:36683–36690

    Article  CAS  PubMed  Google Scholar 

  • 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 407–412

    Google Scholar 

  • Seki T, Yoshikawa H, Takahashi H, Saito H (1987) Cloning and nucleotide sequence of phoP, the regulatory gene for alkaline phosphatase and phosphodiesterase in Bacillus subtilis. J Bacteriol 169:2913–2916

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Seki T, Yoshikawa H, Takahashi H, Saito H (1988) Nucleotide sequence of the Bacillus subtilis phoR gene. J Bacteriol 170:5935–5938

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sewell EWC, Pereira MP, Brown ED (2009) The wall teichoic acid polymerase TagF is non-processive in vitro and amenable to study using steady state kinetic analysis. J Biol Chem 284:21132–21138

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sham LT, Butler EK, Lebar MD, Kahne D, Bernhardt TG, Ruiz N (2014) MurJ is the flippase of lipid-linked precursors for peptidoglycan biogenesis. Science 345:220–222

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shibaev VN, Duckworth M, Archibald AR, Baddiley J (1973) The structure of a polymer containing galactosamine from walls of Bacillus subtilis 168. Biochem J 135:383–384

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Soldo B, Lazarevic V, Pagni M, Karamata D (1999) Teichuronic acid operon of Bacillus subtilis 168. Mol Microbiol 31:795–805

    Article  CAS  PubMed  Google Scholar 

  • Soldo B, Lazarevic V, Karamata D (2002) tagO is involved in the synthesis of all anionic cell-wall polymers in Bacillus subtilis 168. Microbiology 148:2079–2087

    Article  CAS  PubMed  Google Scholar 

  • Tarahomjoo S (2014) Recent approaches in vaccine development against Streptococcus pneumoniae. J Mol Microbiol Biotechnol 24:215–227

    Article  CAS  PubMed  Google Scholar 

  • Tomasz A (1967) Choline in the cell wall of a bacterium: novel type of polymer-linked choline in Pneumococcus. Science (New York, N.Y.) 157:694–697

    Article  CAS  Google Scholar 

  • Toniolo C, Balducci E, Romano MR et al (2015) Streptococcus agalactiae capsule polymer length and attachment is determined by the proteins CpsABCD. J Biol Chem 290:9521–9532

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Traxler CI, Goustin AS, Anderson JS (1982) Elongation of teichuronic acid chains by a wall-membrane preparation from Micrococcus luteus. J Bacteriol 150:649–656

    CAS  PubMed  PubMed Central  Google Scholar 

  • Trombe M-C, Lanéelle M-A, Lanéelle G (1979) Lipid composition of aminopterin-resistant and sensitive strains of Streptococcus pneumoniae effect of aminopterin inhibition. Biochim Biophys Acta 574:290–300

    Article  CAS  PubMed  Google Scholar 

  • Valtersson C, van Duÿn G, Verkleij AJ, Chojnacki T, de Kruijff B, Dallner G (1985) The influence of dolichol, dolichol esters, and dolichyl phosphate on phospholipid polymorphism and fluidity in model membranes. J Biol Chem 260:2742–2751

    CAS  PubMed  Google Scholar 

  • Valvano MA (2011) Common themes in glycoconjugate assembly using the biogenesis of O-antigen lipopolysaccharide as a model system. Biochem (Moscow) 76:729–735

    Article  CAS  Google Scholar 

  • van Selm S, Kolkman MAB, van der Zeijst BAM, Zwaagstra KA, Gaastra W, van Putten JPM (2002) Organization and characterization of the capsule biosynthesis locus of Streptococcus pneumoniae serotype 9V. Microbiology 148:1747–1755

    Article  PubMed  Google Scholar 

  • Ventura CL, Cartee RT, Forsee WT, Yother J (2006) Control of capsular polysaccharide chain length by UDP-sugar substrate concentrations in Streptococcus pneumoniae. Mol Microbiol 61:723–733

    Article  CAS  PubMed  Google Scholar 

  • Wang X, Mansourian AR, Quinn PJ (2008) The effect of dolichol on the structure and phase behaviour of phospholipid model membranes. Mol Membr Biol 25:547–556

    Article  PubMed  CAS  Google Scholar 

  • Wang X, Yang F, von Bodman SB (2012) The genetic and structural basis of two distinct terminal side branch residues in stewartan and amylovoran exopolysaccharides and their potential role in host adaptation. Mol Microbiol 83:195–207

    Article  CAS  PubMed  Google Scholar 

  • Webb AJ, Karatsa-Dodgson M, Gründling A (2009) Two-enzyme systems for glycolipid and polyglycerolphosphate lipoteichoic acid synthesis in Listeria monocytogenes. Mol Microbiol 74:299–314

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Weigel PH (2002) Functional characteristics and catalytic mechanisms of the bacterial hyaluronan synthases. IUBMB Life 54:201–211

    Article  CAS  PubMed  Google Scholar 

  • Whitfield C (2006) Biosynthesis and assembly of capsular polysaccharides in Escherichia coli. Annu Rev Biochem 75:39–68

    Article  CAS  PubMed  Google Scholar 

  • Woodward R, Yi W, Li L et al (2010) In vitro bacterial polysaccharide biosynthesis: defining the functions of Wzy and Wzz. Nat Chem Biol 6:418–423

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xayarath B, Yother J (2007) Mutations blocking side chain assembly, polymerization, or transport of a Wzy-dependent Streptococcus pneumoniae capsule are lethal in the absence of suppressor mutations and can affect polymer transfer to the cell wall. J Bacteriol 189:3369–3381

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang J, Ritchey M, Yoshida Y, Bush CA, Cisar JO (2009) Comparative structural and molecular characterization of ribitol-5-phosphate-containing Streptococcus oralis coaggregation receptor polysaccharides. J Bacteriol 191:1891–1900

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yother J (2011) Capsules of Streptococcus pneumoniae and other bacteria: paradigms for polysaccharide biosynthesis and regulation. Annu Rev Microbiol 65:563–581

    Article  CAS  PubMed  Google Scholar 

  • Zhang Y-H, Ginsberg C, Yuan Y, Walker S (2006) Acceptor substrate selectivity and kinetic mechanism of Bacillus subtilis TagA. Biochemistry 45:10895–10904

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao G, Wu B, Li L, Wang P (2014) O-antigen polymerase adopts a distributive mechanism for lipopolysaccharide biosynthesis. Appl Microbiol Biotechnol 98:4075–4081

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

Research in the Lam laboratory was supported by funding from the Canadian Institutes of Health Research (CIHR) (grant# MOP-14687) to J.S.L. V.L.T. is a recipient of a Cystic Fibrosis Canada Doctoral Studentship and a Queen Elizabeth II Graduate Student Scholarships in Science and Technology, S.M.H. is a recipient of an Ontario Graduate Scholarship and a CIHR Canada Graduate Scholarship Masters, and J.S.L. holds a Canada Research Chair in Cystic Fibrosis and Microbial Glycobiology.

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  1. Department of Molecular and Cellular Biology, University of Guelph, Guelph, ON, N1G 2W1, Canada

    Véronique L. Taylor, Steven M. Huszczynski & Joseph S. Lam

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  1. Véronique L. Taylor
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  1. GSK Vaccines , Siena, Siena, Italy

    Fabio Bagnoli

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    Rino Rappuoli

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Taylor, V.L., Huszczynski, S.M., Lam, J.S. (2015). Membrane Translocation and Assembly of Sugar Polymer Precursors. In: Bagnoli, F., Rappuoli, R. (eds) Protein and Sugar Export and Assembly in Gram-positive Bacteria . Current Topics in Microbiology and Immunology, vol 404. Springer, Cham. https://doi.org/10.1007/82_2015_5014

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