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Biology and Assembly of the Bacterial Envelope

  • Chapter
Prokaryotic Systems Biology

Part of the book series: Advances in Experimental Medicine and Biology ((AEMB,volume 883))

Abstract

All free-living bacterial cells are delimited and protected by an envelope of high complexity. This physiological barrier is essential for bacterial survival and assures multiple functions. The molecular assembly of the different envelope components into a functional structure represents a tremendous biological challenge and is of high interest for fundamental sciences. The study of bacterial envelope assembly has also been fostered by the need for novel classes of antibacterial agents to fight the problematic of bacterial resistance to antibiotics. This chapter focuses on the two most intensively studied classes of bacterial envelopes that belong to the phyla Firmicutes and Proteobacteria. The envelope of Firmicutes typically has one membrane and is defined as being monoderm whereas the envelope of Proteobacteria contains two distinct membranes and is referred to as being diderm. In this chapter, we will first discuss the multiple roles of the bacterial envelope and clarify the nomenclature used to describe the different types of envelopes. We will then define the architecture and composition of the envelopes of Firmicutes and Proteobacteria while outlining their similarities and differences. We will further cover the extensive progress made in the field of bacterial envelope assembly over the last decades, using Bacillus subtilis and Escherichia coli as model systems for the study of the monoderm and diderm bacterial envelopes, respectively. We will detail our current understanding of how molecular machines assure the secretion, insertion and folding of the envelope proteins as well as the assembly of the glycosidic components of the envelope. Finally, we will highlight the topics that are still under investigation, and that will surely lead to important discoveries in the near future.

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References

  • Andersson H, von Heijne G (1993) Sec dependent and sec independent assembly of E. coli inner membrane proteins: the topological rules depend on chain length. EMBO J 12(2):683–691

    PubMed Central  CAS  PubMed  Google Scholar 

  • Angelini S, Deitermann S, Koch HG (2005) FtsY, the bacterial signal-recognition particle receptor, interacts functionally and physically with the SecYEG translocon. EMBO Rep 6(5):476–481

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Angelini S et al (2006) Membrane binding of the bacterial signal recognition particle receptor involves two distinct binding sites. J Cell Biol 174(5):715–724

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Barreteau H et al (2008) Cytoplasmic steps of peptidoglycan biosynthesis. FEMS Microbiol Rev 32(2):168–207

    Article  CAS  PubMed  Google Scholar 

  • Bartholomew JW, Mittwer T (1952) The gram stain. Bacteriol Rev 16(1):1–29

    PubMed Central  CAS  PubMed  Google Scholar 

  • Beck K et al (2000) Discrimination between SRP- and SecA/SecB-dependent substrates involves selective recognition of nascent chains by SRP and trigger factor. EMBO J 19(1):134–143

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Beveridge TJ (2001) Use of the gram stain in microbiology. Biotech Histochem 76(3):111–118

    Article  CAS  PubMed  Google Scholar 

  • Beveridge TJ, Graham LL (1991) Surface layers of bacteria. Microbiol Rev 55(4):684–705

    PubMed Central  CAS  PubMed  Google Scholar 

  • Boone DR, Castenholz RW, Garrity GM (2001) Bergey’s manual of systematic bacteriology, 2nd edn. Springer, New York

    Google Scholar 

  • Bos MP, Robert V, Tommassen J (2007) Biogenesis of the gram-negative bacterial outer membrane. Annu Rev Microbiol 61:191–214

    Article  CAS  PubMed  Google Scholar 

  • Bouhss A et al (2008) The biosynthesis of peptidoglycan lipid-linked intermediates. FEMS Microbiol Rev 32(2):208–233

    Article  CAS  PubMed  Google Scholar 

  • Braun V, Rehn K (1969) Chemical characterization, spatial distribution and function of a lipoprotein (murein-lipoprotein) of the E. coli cell wall. The specific effect of trypsin on the membrane structure. Eur J Biochem 10(3):426–438

    Article  CAS  PubMed  Google Scholar 

  • Briggs MS et al (1986) Conformations of signal peptides induced by lipids suggest initial steps in protein export. Science 233(4760):206–208

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Buddelmeijer N, Young R (2010) The essential Escherichia coli apolipoprotein N-acyltransferase (Lnt) exists as an extracytoplasmic thioester acyl-enzyme intermediate. Biochemistry 49(2):341–346

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Chevance FF, Hughes KT (2008) Coordinating assembly of a bacterial macromolecular machine. Nat Rev Microbiol 6(6):455–465

    Article  CAS  PubMed  Google Scholar 

  • Chng SS, Gronenberg LS, Kahne D (2010) Proteins required for lipopolysaccharide assembly in Escherichia coli form a transenvelope complex. Biochemistry 49(22):4565–4567

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Clark DP (2010) Molecular biology: academic cell update, vol xviii. Academic Press/Elsevier, Amsterdam/Boston, p 784

    Google Scholar 

  • Collins LV et al (2002) Staphylococcus aureus strains lacking D-alanine modifications of teichoic acids are highly susceptible to human neutrophil killing and are virulence attenuated in mice. J Infect Dis 186(2):214–219

    Article  CAS  PubMed  Google Scholar 

  • Comfort D, Clubb RT (2004) A comparative genome analysis identifies distinct sorting pathways in gram-positive bacteria. Infect Immun 72(5):2710–2722

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Dalbey RE, Wang P, Kuhn A (2011) Assembly of bacterial inner membrane proteins. Annu Rev Biochem 80:161–187

    Article  CAS  PubMed  Google Scholar 

  • de Pedro MA et al (2001) Constitutive septal murein synthesis in Escherichia coli with impaired activity of the morphogenetic proteins RodA and penicillin-binding protein 2. J Bacteriol 183(14):4115–4126

    Article  PubMed Central  PubMed  Google Scholar 

  • Delcour AH (2009) Outer membrane permeability and antibiotic resistance. Biochim Biophys Acta 1794(5):808–816

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • den Blaauwen T et al (2008) Morphogenesis of rod-shaped sacculi. FEMS Microbiol Rev 32(2):321–344

    Article  CAS  Google Scholar 

  • Dengler V et al (2012) Deletion of hypothetical wall teichoic acid ligases in Staphylococcus aureus activates the cell wall stress response. FEMS Microbiol Lett 333(2):109–120

    Article  CAS  PubMed  Google Scholar 

  • Denoncin K et al (2012) Dissecting the Escherichia coli periplasmic chaperone network using differential proteomics. Proteomics 12(9):1391–1401

    Article  CAS  PubMed  Google Scholar 

  • Depuydt M, Messens J, Collet JF (2011) How proteins form disulfide bonds. Antioxid Redox Signal 15(1):49–66

    Article  CAS  PubMed  Google Scholar 

  • Di Berardino M et al (1996) The monofunctional glycosyltransferase of Escherichia coli is a member of a new class of peptidoglycan-synthesising enzymes. FEBS Lett 392(2):184–188

    Article  PubMed  Google Scholar 

  • Dilks K et al (2003) Prokaryotic utilization of the twin-arginine translocation pathway: a genomic survey. J Bacteriol 185(4):1478–1483

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Doerrler WT (2006) Lipid trafficking to the outer membrane of Gram-negative bacteria. Mol Microbiol 60(3):542–552

    Article  CAS  PubMed  Google Scholar 

  • Dorr T et al (2014) Differential requirement for PBP1a and PBP1b in in vivo and in vitro fitness of Vibrio cholerae. Infect Immun 82(5):2115–2124

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Dramsi S et al (2008) Covalent attachment of proteins to peptidoglycan. FEMS Microbiol Rev 32(2):307–320

    Article  CAS  PubMed  Google Scholar 

  • Driessen AJ, Nouwen N (2008) Protein translocation across the bacterial cytoplasmic membrane. Annu Rev Biochem 77:643–667

    Article  CAS  PubMed  Google Scholar 

  • du Plessis DJ, Nouwen N, Driessen AJ (2011) The Sec translocase. Biochim Biophys Acta 1808(3):851–865

    Article  PubMed  CAS  Google Scholar 

  • Duguay AR, Silhavy TJ (2004) Quality control in the bacterial periplasm. Biochim Biophys Acta 1694(1–3):121–134

    Article  CAS  PubMed  Google Scholar 

  • Dutton RJ et al (2008) Bacterial species exhibit diversity in their mechanisms and capacity for protein disulfide bond formation. Proc Natl Acad Sci U S A 105(33):11933–11938

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Dziarski R, Gupta D (2005) Peptidoglycan recognition in innate immunity. J Endotoxin Res 11(5):304–310

    Article  CAS  PubMed  Google Scholar 

  • Eberhardt A et al (2012) Attachment of capsular polysaccharide to the cell wall in Streptococcus pneumoniae. Microb Drug Resist 18(3):240–255

    Article  CAS  PubMed  Google Scholar 

  • Egan AJ et al (2014) Outer-membrane lipoprotein LpoB spans the periplasm to stimulate the peptidoglycan synthase PBP1B. Proc Natl Acad Sci U S A 111(22):8197–8202

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Egea PF et al (2004) Substrate twinning activates the signal recognition particle and its receptor. Nature 427(6971):215–221

    Article  CAS  PubMed  Google Scholar 

  • Eisner G et al (2003) Ligand crowding at a nascent signal sequence. J Cell Biol 163(1):35–44

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Facey SJ, Kuhn A (2010) Biogenesis of bacterial inner-membrane proteins. Cell Mol Life Sci 67(14):2343–2362

    Article  CAS  PubMed  Google Scholar 

  • Fagan RP, Fairweather NF (2014) Biogenesis and functions of bacterial S-layers. Nat Rev Microbiol 12(3):211–222

    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(19):6020–6028

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ferbitz L et al (2004) Trigger factor in complex with the ribosome forms a molecular cradle for nascent proteins. Nature 431(7008):590–596

    Article  CAS  PubMed  Google Scholar 

  • Fischer W (1988) Physiology of lipoteichoic acids in bacteria. Adv Microb Physiol 29:233–302

    Article  CAS  PubMed  Google Scholar 

  • Fischer W (1994) Lipoteichoic acid and lipids in the membrane of Staphylococcus aureus. Med Microbiol Immunol 183(2):61–76

    Article  CAS  PubMed  Google Scholar 

  • Focia PJ et al (2004) Heterodimeric GTPase core of the SRP targeting complex. Science 303(5656):373–377

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Freinkman E et al (2012) Regulated assembly of the transenvelope protein complex required for lipopolysaccharide export. Biochemistry 51(24):4800–4806

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Frobel J, Rose P, Muller M (2011) Early contacts between substrate proteins and TatA translocase component in twin-arginine translocation. J Biol Chem 286(51):43679–43689

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Frobel J et al (2012) Transmembrane insertion of twin-arginine signal peptides is driven by TatC and regulated by TatB. Nat Commun 3:1311

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Ganfield MC, Pieringer RA (1980) The biosynthesis of nascent membrane lipoteichoic acid of Streptococcus faecium (S. faecalis ATCC 9790) from phosphatidylkojibiosyl diacylglycerol and phosphatidylglycerol. J Biol Chem 255(11):5164–5169

    CAS  PubMed  Google Scholar 

  • Glauner B, Holtje JV, Schwarz U (1988) The composition of the murein of Escherichia coli. J Biol Chem 263(21):10088–10095

    CAS  PubMed  Google Scholar 

  • Goemans C, Denoncin K, Collet JF (2014) Folding mechanisms of periplasmic proteins. Biochim Biophys Acta 1843(8):1517–1528

    Article  CAS  PubMed  Google Scholar 

  • Goffin C, Ghuysen JM (1998) Multimodular penicillin-binding proteins: an enigmatic family of orthologs and paralogs. Microbiol Mol Biol Rev 62(4):1079–1093

    PubMed Central  CAS  PubMed  Google Scholar 

  • Goosens VJ, Monteferrante CG, van Dijl JM (2014) The Tat system of Gram-positive bacteria. Biochim Biophys Acta 1843(8):1698–1706

    Article  CAS  PubMed  Google Scholar 

  • Graumann PL (2009) Dynamics of bacterial cytoskeletal elements. Cell Motil Cytoskeleton 66(11):909–914

    Article  CAS  PubMed  Google Scholar 

  • Grundling A, Schneewind O (2007a) Genes required for glycolipid synthesis and lipoteichoic acid anchoring in Staphylococcus aureus. J Bacteriol 189(6):2521–2530

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Grundling A, Schneewind O (2007b) Synthesis of glycerol phosphate lipoteichoic acid in Staphylococcus aureus. Proc Natl Acad Sci U S A 104(20):8478–8483

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Hagan CL, Kim S, Kahne D (2010) Reconstitution of outer membrane protein assembly from purified components. Science 328(5980):890–892

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hagan CL, Silhavy TJ, Kahne D (2011) beta-Barrel membrane protein assembly by the Bam complex. Annu Rev Biochem 80:189–210

    Article  CAS  PubMed  Google Scholar 

  • Haiko J, Westerlund-Wikstrom B (2013) The role of the bacterial flagellum in adhesion and virulence. Biology (Basel) 2(4):1242–1267

    Google Scholar 

  • Han W et al (2012) Defining function of lipopolysaccharide O-antigen ligase WaaL using chemoenzymatically synthesized substrates. J Biol Chem 287(8):5357–5365

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hancock IC (1997) Bacterial cell surface carbohydrates: structure and assembly. Biochem Soc Trans 25(1):183–187

    Article  CAS  PubMed  Google Scholar 

  • Harold FM (1972) Conservation and transformation of energy by bacterial membranes. Bacteriol Rev 36(2):172–230

    PubMed Central  CAS  PubMed  Google Scholar 

  • Harshey RM (2003) Bacterial motility on a surface: many ways to a common goal. Annu Rev Microbiol 57:249–273

    Article  CAS  PubMed  Google Scholar 

  • Hatahet F, Boyd D, Beckwith J (2014) Disulfide bond formation in prokaryotes: history, diversity and design. Biochim Biophys Acta 1844(8):1402–1414

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Henriques AO et al (1998) Control of cell shape and elongation by the rodA gene in Bacillus subtilis. Mol Microbiol 28(2):235–247

    Article  CAS  PubMed  Google Scholar 

  • Holst O (2007) The structures of core regions from enterobacterial lipopolysaccharides – an update. FEMS Microbiol Lett 271(1):3–11

    Article  CAS  PubMed  Google Scholar 

  • Holtje JV (1998) Growth of the stress-bearing and shape-maintaining murein sacculus of Escherichia coli. Microbiol Mol Biol Rev 62(1):181–203

    PubMed Central  CAS  PubMed  Google Scholar 

  • Hutchings MI et al (2009) Lipoprotein biogenesis in Gram-positive bacteria: knowing when to hold ‘em, knowing when to fold ‘em. Trends Microbiol 17(1):13–21

    Article  CAS  PubMed  Google Scholar 

  • Hvorup RN et al (2003) The multidrug/oligosaccharidyl-lipid/polysaccharide (MOP) exporter superfamily. Eur J Biochem 270(5):799–813

    Article  CAS  PubMed  Google Scholar 

  • Islam ST et al (2013) Proton-dependent gating and proton uptake by Wzx support O-antigen-subunit antiport across the bacterial inner membrane. MBio 4(5):e00678-13

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Iwasaki H, Shimada A, Ito E (1986) Comparative studies of lipoteichoic acids from several Bacillus strains. J Bacteriol 167(2):508–516

    PubMed Central  CAS  PubMed  Google Scholar 

  • Iwasaki H et al (1989) Structure and glycosylation of lipoteichoic acids in Bacillus strains. J Bacteriol 171(1):424–429

    PubMed Central  CAS  PubMed  Google Scholar 

  • Jordan S, Hutchings MI, Mascher T (2008) Cell envelope stress response in Gram-positive bacteria. FEMS Microbiol Rev 32(1):107–146

    Article  CAS  PubMed  Google Scholar 

  • Kadokura H, Beckwith J (2010) Mechanisms of oxidative protein folding in the bacterial cell envelope. Antioxid Redox Signal 13(8):1231–1246

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kamio Y, Nikaido H (1976) Outer membrane of Salmonella typhimurium: accessibility of phospholipid head groups to phospholipase c and cyanogen bromide activated dextran in the external medium. Biochemistry 15(12):2561–2570

    Article  CAS  PubMed  Google Scholar 

  • Karatsa-Dodgson M, Wormann ME, Grundling A (2010) In vitro analysis of the Staphylococcus aureus lipoteichoic acid synthase enzyme using fluorescently labeled lipids. J Bacteriol 192(20):5341–5349

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kawai Y et al (2011) A widespread family of bacterial cell wall assembly proteins. EMBO J 30(24):4931–4941

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Khattar MM, Begg KJ, Donachie WD (1994) Identification of FtsW and characterization of a new ftsW division mutant of Escherichia coli. J Bacteriol 176(23):7140–7147

    PubMed Central  CAS  PubMed  Google Scholar 

  • Kim S et al (2007) Structure and function of an essential component of the outer membrane protein assembly machine. Science 317(5840):961–964

    Article  CAS  PubMed  Google Scholar 

  • King G, Sharom FJ (2012) Proteins that bind and move lipids: MsbA and NPC1. Crit Rev Biochem Mol Biol 47(1):75–95

    Article  CAS  PubMed  Google Scholar 

  • Koch HG, Muller M (2000) Dissecting the translocase and integrase functions of the Escherichia coli SecYEG translocon. J Cell Biol 150(3):689–694

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Koch HU, Haas R, Fischer W (1984) The role of lipoteichoic acid biosynthesis in membrane lipid metabolism of growing Staphylococcus aureus. Eur J Biochem 138(2):357–363

    Article  CAS  PubMed  Google Scholar 

  • Kojima N, Araki Y, Ito E (1985) Structure of the linkage units between ribitol teichoic acids and peptidoglycan. J Bacteriol 161(1):299–306

    PubMed Central  CAS  PubMed  Google Scholar 

  • Kouidmi I, Levesque RC, Paradis-Bleau C (2014) The biology of Mur ligases as an antibacterial target. Mol Microbiol 94(2):242–253

    Article  CAS  PubMed  Google Scholar 

  • Kovacs M et al (2006) A functional dlt operon, encoding proteins required for incorporation of d-alanine in teichoic acids in gram-positive bacteria, confers resistance to cationic antimicrobial peptides in Streptococcus pneumoniae. J Bacteriol 188(16):5797–5805

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kunst F et al (1997) The complete genome sequence of the gram-positive bacterium Bacillus subtilis. Nature 390(6657):249–256

    Article  CAS  PubMed  Google Scholar 

  • Lara B et al (2005) Peptidoglycan precursor pools associated with MraY and FtsW deficiencies or antibiotic treatments. FEMS Microbiol Lett 250(2):195–200

    Article  CAS  PubMed  Google Scholar 

  • Lazarevic V, Karamata D (1995) The tagGH operon of Bacillus subtilis 168 encodes a two-component ABC transporter involved in the metabolism of two wall teichoic acids. Mol Microbiol 16(2):345–355

    Article  CAS  PubMed  Google Scholar 

  • Lecoq L et al (2012) Dynamics induced by beta-lactam antibiotics in the active site of Bacillus subtilis L,D-transpeptidase. Structure 20(5):850–861

    Article  CAS  PubMed  Google Scholar 

  • Li J, Lee DS, Madrenas J (2013) Evolving bacterial envelopes and plasticity of TLR2-dependent responses: basic research and translational opportunities. Front Immunol 4:347

    PubMed Central  PubMed  Google Scholar 

  • Lovering AL, Safadi SS, Strynadka NC (2012) Structural perspective of peptidoglycan biosynthesis and assembly. Annu Rev Biochem 81:451–478

    Article  CAS  PubMed  Google Scholar 

  • Lu D et al (2009) Structure-based mechanism of lipoteichoic acid synthesis by Staphylococcus aureus LtaS. Proc Natl Acad Sci U S A 106(5):1584–1589

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Lugtenberg EJ, Peters R (1976) Distribution of lipids in cytoplasmic and outer membranes of Escherichia coli K12. Biochim Biophys Acta 441(1):38–47

    Article  CAS  PubMed  Google Scholar 

  • Lupoli TJ et al (2014) Lipoprotein activators stimulate Escherichia coli penicillin-binding proteins by different mechanisms. J Am Chem Soc 136(1):52–55

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Lycklama ANJA, Driessen AJ (2012) The bacterial Sec-translocase: structure and mechanism. Philos Trans R Soc Lond B Biol Sci 367(1592):1016–1028

    Article  CAS  Google Scholar 

  • Magnet S et al (2007a) Identification of the L,D-transpeptidases responsible for attachment of the Braun lipoprotein to Escherichia coli peptidoglycan. J Bacteriol 189(10):3927–3931

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Magnet S et al (2007b) Specificity of L,D-transpeptidases from gram-positive bacteria producing different peptidoglycan chemotypes. J Biol Chem 282(18):13151–13159

    Article  CAS  PubMed  Google Scholar 

  • Magnet S et al (2008) Identification of the L,D-transpeptidases for peptidoglycan cross-linking in Escherichia coli. J Bacteriol 190(13):4782–4785

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Mainardi JL et al (2000) Novel mechanism of beta-lactam resistance due to bypass of DD-transpeptidation in Enterococcus faecium. J Biol Chem 275(22):16490–16496

    Article  CAS  PubMed  Google Scholar 

  • Mainardi JL et al (2005) A novel peptidoglycan cross-linking enzyme for a beta-lactam-resistant transpeptidation pathway. J Biol Chem 280(46):38146–38152

    Article  CAS  PubMed  Google Scholar 

  • Mainardi JL et al (2008) Evolution of peptidoglycan biosynthesis under the selective pressure of antibiotics in Gram-positive bacteria. FEMS Microbiol Rev 32(2):386–408

    Article  CAS  PubMed  Google Scholar 

  • Maloney PC, Kashket ER, Wilson TH (1974) A protonmotive force drives ATP synthesis in bacteria. Proc Natl Acad Sci U S A 71(10):3896–3900

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Manat G et al (2014) Deciphering the metabolism of undecaprenyl-phosphate: the bacterial cell-wall unit carrier at the membrane frontier. Microb Drug Resist 20(3):199–214

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Mancuso DJ, Chiu TH (1982) Biosynthesis of glucosyl monophosphoryl undecaprenol and its role in lipoteichoic acid biosynthesis. J Bacteriol 152(2):616–625

    PubMed Central  CAS  PubMed  Google Scholar 

  • Margolin W (2009) Sculpting the bacterial cell. Curr Biol 19(17):R812–R822

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Matias VR, Beveridge TJ (2008) Lipoteichoic acid is a major component of the Bacillus subtilis periplasm. J Bacteriol 190(22):7414–7418

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • McPherson DC, Popham DL (2003) Peptidoglycan synthesis in the absence of class A penicillin-binding proteins in Bacillus subtilis. J Bacteriol 185(4):1423–1431

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Merdanovic M et al (2011) Protein quality control in the bacterial periplasm. Annu Rev Microbiol 65:149–168

    Article  CAS  PubMed  Google Scholar 

  • Millman JS et al (2001) FtsY binds to the Escherichia coli inner membrane via interactions with phosphatidylethanolamine and membrane proteins. J Biol Chem 276(28):25982–25989

    Article  CAS  PubMed  Google Scholar 

  • Mohamed YF, Valvano MA (2014) A Burkholderia cenocepacia MurJ (MviN) homolog is essential for cell wall peptidoglycan synthesis and bacterial viability. Glycobiology 24(6):564–576

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Mohammadi T et al (2011) Identification of FtsW as a transporter of lipid-linked cell wall precursors across the membrane. EMBO J 30(8):1425–1432

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Mohammadi T et al (2014) Specificity of the transport of lipid II by FtsW in Escherichia coli. J Biol Chem 289(21):14707–14718

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Muhlradt PF, Golecki JR (1975) Asymmetrical distribution and artifactual reorientation of lipopolysaccharide in the outer membrane bilayer of Salmonella typhimurium. Eur J Biochem 51(2):343–352

    Article  CAS  PubMed  Google Scholar 

  • Mullineaux CW et al (2006) Diffusion of green fluorescent protein in three cell environments in Escherichia coli. J Bacteriol 188(10):3442–3448

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Nakayama H, Kurokawa K, Lee BL (2012) Lipoproteins in bacteria: structures and biosynthetic pathways. FEBS J 279(23):4247–4268

    Article  CAS  PubMed  Google Scholar 

  • Narita S, Tokuda H (2010) Sorting of bacterial lipoproteins to the outer membrane by the Lol system. Methods Mol Biol 619:117–129

    Article  CAS  PubMed  Google Scholar 

  • Natale P, Bruser T, Driessen AJ (2008) Sec- and Tat-mediated protein secretion across the bacterial cytoplasmic membrane—distinct translocases and mechanisms. Biochim Biophys Acta 1778(9):1735–1756

    Article  CAS  PubMed  Google Scholar 

  • Nelson N (1994) Energizing porters by proton-motive force. J Exp Biol 196:7–13

    CAS  PubMed  Google Scholar 

  • Neuhaus FC, Baddiley J (2003) A continuum of anionic charge: structures and functions of D-alanyl-teichoic acids in gram-positive bacteria. Microbiol Mol Biol Rev 67(4):686–723

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Nikaido H (1989) Outer membrane barrier as a mechanism of antimicrobial resistance. Antimicrob Agents Chemother 33(11):1831–1836

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Nikaido H (2003) Molecular basis of bacterial outer membrane permeability revisited. Microbiol Mol Biol Rev 67(4):593–656

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Okuda S, Tokuda H (2011) Lipoprotein sorting in bacteria. Annu Rev Microbiol 65:239–259

    Article  CAS  PubMed  Google Scholar 

  • Okuda S, Freinkman E, Kahne D (2012) Cytoplasmic ATP hydrolysis powers transport of lipopolysaccharide across the periplasm in E. coli. Science 338(6111):1214–1217

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Oliver DB (1996) Periplasm. ASM Press, Washington

    Google Scholar 

  • Over B et al (2011) LytR-CpsA-Psr proteins in Staphylococcus aureus display partial functional redundancy and the deletion of all three severely impairs septum placement and cell separation. FEMS Microbiol Lett 320(2):142–151

    Article  CAS  PubMed  Google Scholar 

  • Paetzel M et al (2002) Signal peptidases. Chem Rev 102(12):4549–4580

    Article  CAS  PubMed  Google Scholar 

  • Pailler J et al (2012) Phosphatidylglycerol::prolipoprotein diacylglyceryl transferase (Lgt) of Escherichia coli has seven transmembrane segments, and its essential residues are embedded in the membrane. J Bacteriol 194(9):2142–2151

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Pallen MJ, Chaudhuri RR, Henderson IR (2003) Genomic analysis of secretion systems. Curr Opin Microbiol 6(5):519–527

    Article  CAS  PubMed  Google Scholar 

  • Palmer T, Berks BC (2012) The twin-arginine translocation (Tat) protein export pathway. Nat Rev Microbiol 10(7):483–496

    CAS  PubMed  Google Scholar 

  • Palmer T, Sargent F, Berks BC (2010) The Tat protein export pathway. In the Escherichia coli and Salmonella: cellular and molecular biology. ASM Press, Washington

    Google Scholar 

  • Paradis-Bleau C et al (2010) Lipoprotein cofactors located in the outer membrane activate bacterial cell wall polymerases. Cell 143(7):1110–1120

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Percy MG, Grundling A (2014) Lipoteichoic acid synthesis and function in gram-positive bacteria. Annu Rev Microbiol 68:81–100

    Article  CAS  PubMed  Google Scholar 

  • Perego M et al (1995) Incorporation of D-alanine into lipoteichoic acid and wall teichoic acid in Bacillus subtilis. Identification of genes and regulation. J Biol Chem 270(26):15598–15606

    Article  CAS  PubMed  Google Scholar 

  • Perlstein DL et al (2007) The direction of glycan chain elongation by peptidoglycan glycosyltransferases. J Am Chem Soc 129(42):12674–12675

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Piddock LJ (2006) Multidrug-resistance efflux pumps – not just for resistance. Nat Rev Microbiol 4(8):629–636

    Article  CAS  PubMed  Google Scholar 

  • Pisabarro AG, de Pedro MA, Vazquez D (1985) Structural modifications in the peptidoglycan of Escherichia coli associated with changes in the state of growth of the culture. J Bacteriol 161(1):238–242

    PubMed Central  CAS  PubMed  Google Scholar 

  • Polissi A, Sperandeo P (2014) The lipopolysaccharide export pathway in Escherichia coli: structure, organization and regulated assembly of the Lpt machinery. Mar Drugs 12(2):1023–1042

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Raetz CR (1978) Enzymology, genetics, and regulation of membrane phospholipid synthesis in Escherichia coli. Microbiol Rev 42(3):614–659

    PubMed Central  CAS  PubMed  Google Scholar 

  • Raetz CR, Whitfield C (2002) Lipopolysaccharide endotoxins. Annu Rev Biochem 71:635–700

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Raetz CR et al (2007) Lipid A modification systems in gram-negative bacteria. Annu Rev Biochem 76:295–329

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Raivio TL (2005) Envelope stress responses and Gram-negative bacterial pathogenesis. Mol Microbiol 56(5):1119–1128

    Article  CAS  PubMed  Google Scholar 

  • Ramos HC, Rumbo M, Sirard JC (2004) Bacterial flagellins: mediators of pathogenicity and host immune responses in mucosa. Trends Microbiol 12(11):509–517

    Article  CAS  PubMed  Google Scholar 

  • Reeves PR et al (1996) Bacterial polysaccharide synthesis and gene nomenclature. Trends Microbiol 4(12):495–503

    Article  CAS  PubMed  Google Scholar 

  • 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(2):97–105

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ricci DP, Silhavy TJ (2012) The Bam machine: a molecular cooper. Biochim Biophys Acta 1818(4):1067–1084

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Rizzitello AE, Harper JR, Silhavy TJ (2001) Genetic evidence for parallel pathways of chaperone activity in the periplasm of Escherichia coli. J Bacteriol 183(23):6794–6800

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Robichon C, Vidal-Ingigliardi D, Pugsley AP (2005) Depletion of apolipoprotein N-acyltransferase causes mislocalization of outer membrane lipoproteins in Escherichia coli. J Biol Chem 280(2):974–983

    Article  CAS  PubMed  Google Scholar 

  • Royet J, Dziarski R (2007) Peptidoglycan recognition proteins: pleiotropic sensors and effectors of antimicrobial defences. Nat Rev Microbiol 5(4):264–277

    Article  CAS  PubMed  Google Scholar 

  • Ruiz N (2008) Bioinformatics identification of MurJ (MviN) as the peptidoglycan lipid II flippase in Escherichia coli. Proc Natl Acad Sci U S A 105(40):15553–15557

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ruiz N (2009) Streptococcus pyogenes YtgP (Spy_0390) complements Escherichia coli strains depleted of the putative peptidoglycan flippase MurJ. Antimicrob Agents Chemother 53(8):3604–3605

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ruiz N, Kahne D, Silhavy TJ (2009) Transport of lipopolysaccharide across the cell envelope: the long road of discovery. Nat Rev Microbiol 7(9):677–683

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Samuelson JC et al (2000) YidC mediates membrane protein insertion in bacteria. Nature 406(6796):637–641

    Article  CAS  PubMed  Google Scholar 

  • Sankaran K, Wu HC (1994) Lipid modification of bacterial prolipoprotein. Transfer of diacylglyceryl moiety from phosphatidylglycerol. J Biol Chem 269(31):19701–19706

    CAS  PubMed  Google Scholar 

  • Sanyal S, Menon AK (2009) Flipping lipids: why an’ what’s the reason for? ACS Chem Biol 4(11):895–909

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Sarvas M et al (2004) Post-translocational folding of secretory proteins in Gram-positive bacteria. Biochim Biophys Acta 1694(1–3):311–327

    CAS  PubMed  Google Scholar 

  • Sauvage E et al (2008) The penicillin-binding proteins: structure and role in peptidoglycan biosynthesis. FEMS Microbiol Rev 32(2):234–258

    Article  CAS  PubMed  Google Scholar 

  • Schirner K et al (2009) Distinct and essential morphogenic functions for wall- and lipo-teichoic acids in Bacillus subtilis. EMBO J 28(7):830–842

    Article  PubMed Central  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 6(5):407–412

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Schneewind O, Missiakas DM (2012) Protein secretion and surface display in Gram-positive bacteria. Philos Trans R Soc Lond B Biol Sci 367(1592):1123–1139

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Schneewind O, Missiakas D (2014) Lipoteichoic acids, phosphate-containing polymers in the envelope of gram-positive bacteria. J Bacteriol 196(6):1133–1142

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Schneewind O, Model P, Fischetti VA (1992) Sorting of protein A to the staphylococcal cell wall. Cell 70(2):267–281

    Article  CAS  PubMed  Google Scholar 

  • Sewell EW, Brown ED (2014) Taking aim at wall teichoic acid synthesis: new biology and new leads for antibiotics. J Antibiot (Tokyo) 67(1):43–51

    Article  CAS  Google Scholar 

  • Sham LT, Butler EK, Lebar MD, Kahne D, Bernhardt TG, Ruiz N (2014) Bacterial cell wall. MurJ is the flippase of lipid-linked precursors for peptidoglycan biogenesis. Science 345(6193):220–222

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Silhavy TJ, Kahne D, Walker S (2010) The bacterial cell envelope. Cold Spring Harb Perspect Biol 2(5):a000414

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Sklar JG et al (2007) Defining the roles of the periplasmic chaperones SurA, Skp, and DegP in Escherichia coli. Genes Dev 21(19):2473–2484

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Sperandeo P et al (2008) Functional analysis of the protein machinery required for transport of lipopolysaccharide to the outer membrane of Escherichia coli. J Bacteriol 190(13):4460–4469

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Sperandeo P, Deho G, Polissi A (2009) The lipopolysaccharide transport system of Gram-negative bacteria. Biochim Biophys Acta 1791(7):594–602

    Article  CAS  PubMed  Google Scholar 

  • Sperandeo P et al (2011) New insights into the Lpt machinery for lipopolysaccharide transport to the cell surface: LptA–LptC interaction and LptA stability as sensors of a properly assembled transenvelope complex. J Bacteriol 193(5):1042–1053

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Spirig T, Weiner EM, Clubb RT (2011) Sortase enzymes in Gram-positive bacteria. Mol Microbiol 82(5):1044–1059

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Spratt BG, Pardee AB (1975) Penicillin-binding proteins and cell shape in E. coli. Nature 254(5500):516–517

    Article  CAS  PubMed  Google Scholar 

  • Sutcliffe IC (2010) A phylum level perspective on bacterial cell envelope architecture. Trends Microbiol 18(10):464–470

    Article  CAS  PubMed  Google Scholar 

  • Sutcliffe IC (2011) Priming and elongation: dissection of the lipoteichoic acid biosynthetic pathway in Gram-positive bacteria. Mol Microbiol 79(3):553–556

    Article  CAS  PubMed  Google Scholar 

  • Swoboda JG et al (2010) Wall teichoic acid function, biosynthesis, and inhibition. Chembiochem 11(1):35–45

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Taron DJ, Childs WC 3rd, Neuhaus FC (1983) Biosynthesis of D-alanyl-lipoteichoic acid: role of diglyceride kinase in the synthesis of phosphatidylglycerol for chain elongation. J Bacteriol 154(3):1110–1116

    PubMed Central  CAS  PubMed  Google Scholar 

  • Taylor BL (1983) Role of proton motive force in sensory transduction in bacteria. Annu Rev Microbiol 37:551–573

    Article  CAS  PubMed  Google Scholar 

  • Thanassi JA et al (2002) Identification of 113 conserved essential genes using a high-throughput gene disruption system in Streptococcus pneumoniae. Nucleic Acids Res 30(14):3152–3162

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Thanassi DG, Bliska JB, Christie PJ (2012) Surface organelles assembled by secretion systems of Gram-negative bacteria: diversity in structure and function. FEMS Microbiol Rev 36(6):1046–1082

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Trent MS et al (2006) Diversity of endotoxin and its impact on pathogenesis. J Endotoxin Res 12(4):205–223

    Article  CAS  PubMed  Google Scholar 

  • Typas A et al (2010) Regulation of peptidoglycan synthesis by outer-membrane proteins. Cell 143(7):1097–1109

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Typas A et al (2012) From the regulation of peptidoglycan synthesis to bacterial growth and morphology. Nat Rev Microbiol 10(2):123–136

    CAS  Google Scholar 

  • Ulbrandt ND, Newitt JA, Bernstein HD (1997) The E. coli signal recognition particle is required for the insertion of a subset of inner membrane proteins. Cell 88(2):187–196

    Article  CAS  PubMed  Google Scholar 

  • Utsumi R (2008) Bacterial signal transduction: networks and drug targets. Preface. Adv Exp Med Biol 631:v

    Google Scholar 

  • Valvano MA (2008) Undecaprenyl phosphate recycling comes out of age. Mol Microbiol 67(2):232–235

    Article  CAS  PubMed  Google Scholar 

  • van der Does C et al (2000) Non-bilayer lipids stimulate the activity of the reconstituted bacterial protein translocase. J Biol Chem 275(4):2472–2478

    Article  PubMed  Google Scholar 

  • van der Sluis EO, Driessen AJ (2006) Stepwise evolution of the Sec machinery in Proteobacteria. Trends Microbiol 14(3):105–108

    Article  PubMed  CAS  Google Scholar 

  • van Wely KH et al (2001) Translocation of proteins across the cell envelope of Gram-positive bacteria. FEMS Microbiol Rev 25(4):437–454

    Article  PubMed  Google Scholar 

  • Villa R et al (2013) The Escherichia coli Lpt transenvelope protein complex for lipopolysaccharide export is assembled via conserved structurally homologous domains. J Bacteriol 195(5):1100–1108

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Visweswaran GR, Dijkstra BW, Kok J (2011) Murein and pseudomurein cell wall binding domains of bacteria and archaea—a comparative view. Appl Microbiol Biotechnol 92(5):921–928

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Vollmer W, Blanot D, de Pedro MA (2008a) Peptidoglycan structure and architecture. FEMS Microbiol Rev 32(2):149–167

    Article  CAS  PubMed  Google Scholar 

  • Vollmer W et al (2008b) Bacterial peptidoglycan (murein) hydrolases. FEMS Microbiol Rev 32(2):259–286

    Article  CAS  PubMed  Google Scholar 

  • Weiner JH, Li L (2008) Proteome of the Escherichia coli envelope and technological challenges in membrane proteome analysis. Biochim Biophys Acta 1778(9):1698–1713

    Article  CAS  PubMed  Google Scholar 

  • Welte T et al (2012) Promiscuous targeting of polytopic membrane proteins to SecYEG or YidC by the Escherichia coli signal recognition particle. Mol Biol Cell 23(3):464–479

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Whitfield C (1995) Biosynthesis of lipopolysaccharide O antigens. Trends Microbiol 3(5):178–185

    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 

  • Wimley WC (2003) The versatile beta-barrel membrane protein. Curr Opin Struct Biol 13(4):404–411

    Article  CAS  PubMed  Google Scholar 

  • Wooldridge K (2009) Bacterial secreted proteins: secretory mechanisms and role in pathogenesis, vol xii. Caister Academic Press, Wymondham, p 511

    Google Scholar 

  • Xia G, Peschel A (2008) Toward the pathway of S. aureus WTA biosynthesis. Chem Biol 15(2):95–96

    Article  CAS  PubMed  Google Scholar 

  • Xia G et al (2010) Glycosylation of wall teichoic acid in Staphylococcus aureus by TarM. J Biol Chem 285(18):13405–13415

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Yakushi T et al (2000) A new ABC transporter mediating the detachment of lipid-modified proteins from membranes. Nat Cell Biol 2(4):212–218

    Article  CAS  PubMed  Google Scholar 

  • Yokoyama K, Araki Y, Ito E (1988) The function of galactosyl phosphorylpolyprenol in biosynthesis of lipoteichoic acid in Bacillus coagulans. Eur J Biochem 173(2):453–458

    Article  CAS  PubMed  Google Scholar 

  • Young KD (2010) New ways to make old walls: bacterial surprises. Cell 143(7):1042–1044

    Article  CAS  PubMed  Google Scholar 

  • Young KD (2014) Microbiology. A flipping cell wall ferry. Science 345(6193):139–140

    Article  CAS  PubMed  Google Scholar 

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Dufresne, K., Paradis-Bleau, C. (2015). Biology and Assembly of the Bacterial Envelope. In: Krogan, PhD, N., Babu, PhD, M. (eds) Prokaryotic Systems Biology. Advances in Experimental Medicine and Biology, vol 883. Springer, Cham. https://doi.org/10.1007/978-3-319-23603-2_3

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