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Structure: Function of Transmembrane Appendages in Gram-Negative Bacteria

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Book cover Biogenesis of Fatty Acids, Lipids and Membranes

Abstract

Gram-negative bacteria possess diverse transmembrane appendages that allow them to colonize different ecological niches. An essential prokaryotic strategy used for adaptation to various environments is the secretion of several molecules such as proteins and DNA, which is accomplished by specialized secretion systems that enable substrate transport across the cell envelope. Moreover, bacterial motility and adherence, driven by filamentous surface structures as flagella, pili, and curli, also play a crucial role in bacterial colonization. The construction of these macromolecular complexes faces a physical barrier since they must traverse two distinct lipid membrane bilayers and a peptidoglycan cell wall. Therefore, proteins that display special physicochemical characteristics to assemble within the hydrophobic lipid environment serve as building blocks for the biogenesis of the different transmembrane appendages. Here, we review the architecture and function of the main appendages of diderm bacteria and discuss how the interplay between membrane lipids and proteins influences their assembly and activity.

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References

  • Aas FE, Egge-Jacobsen W, Winther-Larsen HC, Lovold C, Hitchen PG, Dell A, Koomey M (2006) Neisseria gonorrhoeae type IV pili undergo multisite, hierarchical modifications with phosphoethanolamine and phosphocholine requiring an enzyme structurally related to lipopolysaccharide phosphoethanolamine transferases. J Biol Chem 281:27712–27723

    Article  CAS  Google Scholar 

  • Ahn T, Kim H (1998) Effects of nonlamellar-prone lipids on the ATPase activity of SecA bound to model membranes. J Biol Chem 273:21692–21698

    Article  CAS  Google Scholar 

  • Albenne C, Ieva R (2017) Job contenders: roles of the beta-barrel assembly machinery and the translocation and assembly module in autotransporter secretion. Mol Microbiol 106:505–517

    Article  CAS  Google Scholar 

  • Alteri CJ, Mobley HL (2016) The versatile type VI secretion system. Microbiol Spectr 4. https://doi.org/10.1128/microbiolspec.VMBF-0026-2015

  • Anne J, Economou A, Bernaerts K (2017) Protein secretion in Gram-positive Bacteria: from multiple pathways to biotechnology. Curr Top Microbiol Immunol 404:267–308

    PubMed  Google Scholar 

  • Auvray F, Ozin AJ, Claret L, Hughes C (2002) Intrinsic membrane targeting of the flagellar export ATPase FliI: interaction with acidic phospholipids and FliH. J Mol Biol 318:941–950

    Article  CAS  Google Scholar 

  • Brehmer T, Kerth A, Graubner W, Malesevic M, Hou B, Bruser T, Blume A (2012) Negatively charged phospholipids trigger the interaction of a bacterial Tat substrate precursor protein with lipid monolayers. Langmuir 28:3534–3541

    Article  CAS  Google Scholar 

  • Breukink E, Demel RA, de Korte-Kool G, de Kruijff B (1992) SecA insertion into phospholipids is stimulated by negatively charged lipids and inhibited by ATP: a monolayer study. Biochemistry 31:1119–1124

    Article  CAS  Google Scholar 

  • Camberg JL, Johnson TL, Patrick M, Abendroth J, Hol WG, Sandkvist M (2007) Synergistic stimulation of EpsE ATP hydrolysis by EpsL and acidic phospholipids. EMBO J 26:19–27

    Article  CAS  Google Scholar 

  • Cao B, Zhao Y, Kou Y, Ni D, Zhang XC, Huang Y (2014) Structure of the nonameric bacterial amyloid secretion channel. Proc Natl Acad Sci U S A 111:E5439–E5444

    Article  CAS  Google Scholar 

  • Chamot-Rooke J, Mikaty G, Malosse C, Soyer M, Dumont A, Gault J, Imhaus AF, Martin P, Trellet M, Clary G, Chafey P, Camoin L, Nilges M, Nassif X, Dumenil G (2011) Posttranslational modification of pili upon cell contact triggers N. meningitidis dissemination. Science 331:778–782

    Article  CAS  Google Scholar 

  • Chandran V, Fronzes R, Duquerroy S, Cronin N, Navaza J, Waksman G (2009) Structure of the outer membrane complex of a type IV secretion system. Nature 462:1011–1015

    Article  CAS  Google Scholar 

  • Cianfanelli FR, Monlezun L, Coulthurst SJ (2016) Aim, load, fire: the type VI secretion system, a bacterial Nanoweapon. Trends Microbiol 24:51–62

    Article  CAS  Google Scholar 

  • Costa TR, Felisberto-Rodrigues C, Meir A, Prevost MS, Redzej A, Trokter M, Waksman G (2015) Secretion systems in Gram-negative bacteria: structural and mechanistic insights. Nat Rev Microbiol 13:343–359

    Article  CAS  Google Scholar 

  • Costa TRD, Ilangovan A, Ukleja M, Redzej A, Santini JM, Smith TK, Egelman EH, Waksman G (2016) Structure of the bacterial sex F pilus reveals an assembly of a stoichiometric protein-phospholipid complex. Cell 166(1436–1444):e1410

    Google Scholar 

  • Cullen TW, Trent MS (2010) A link between the assembly of flagella and lipooligosaccharide of the Gram-negative bacterium Campylobacter jejuni. Proc Natl Acad Sci U S A 107:5160–5165

    Article  CAS  Google Scholar 

  • Cullen TW, Madsen JA, Ivanov PL, Brodbelt JS, Trent MS (2012) Characterization of unique modification of flagellar rod protein FlgG by Campylobacter jejuni lipid A phosphoethanolamine transferase, linking bacterial locomotion and antimicrobial peptide resistance. J Biol Chem 287:3326–3336

    Article  CAS  Google Scholar 

  • Dalbey RE, Kuhn A (2012) Protein traffic in Gram-negative bacteria – how exported and secreted proteins find their way. FEMS Microbiol Rev 36:1023–1045

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Deng W, Marshall NC, Rowland JL, McCoy JM, Worrall LJ, Santos AS, Strynadka NCJ, Finlay BB (2017) Assembly, structure, function and regulation of type III secretion systems. Nat Rev Microbiol 15:323–337

    Article  CAS  Google Scholar 

  • Diepold A, Armitage JP (2015) Type III secretion systems: the bacterial flagellum and the injectisome. Philos Trans R Soc Lond Ser B Biol Sci 370. https://doi.org/10.1098/rstb.2015.0020

    Article  Google Scholar 

  • Erhardt M, Namba K, Hughes KT (2010) Bacterial nanomachines: the flagellum and type III injectisome. Cold Spring Harb Perspect Biol 2. https://doi.org/10.1101/cshperspect.a000299

    Article  CAS  Google Scholar 

  • Evans ML, Chapman MR (2014) Curli biogenesis: order out of disorder. Biochim Biophys Acta 1843:1551–1558

    Article  CAS  Google Scholar 

  • Fan E, Chauhan N, Udatha DB, Leo JC, Linke D (2016) Type V secretion systems in bacteria. Microbiol Spectr 4. https://doi.org/10.1128/microbiolspec.VMBF-0009-2015

  • Filloux A, Voulhoux R (2018) Multiple structures disclose the Secretins’ secrets. J Bacteriol 200. https://doi.org/10.1128/JB.00702-17

  • Fronzes R, Remaut H, Waksman G (2008) Architectures and biogenesis of non-flagellar protein appendages in Gram-negative bacteria. EMBO J 27:2271–2280

    Article  CAS  Google Scholar 

  • Galan JE, Waksman G (2018) Protein-injection machines in bacteria. Cell 172:1306–1318

    Article  CAS  Google Scholar 

  • Gallique M, Bouteiller M, Merieau A (2017) The type VI secretion system: a dynamic system for bacterial communication? Front Microbiol 8:1454

    Article  Google Scholar 

  • Gaytan MO, Martinez-Santos VI, Soto E, Gonzalez-Pedrajo B (2016) Type three secretion system in attaching and effacing pathogens. Front Cell Infect Microbiol 6:129

    Article  Google Scholar 

  • Gold V, Kudryashev M (2016) Recent progress in structure and dynamics of dual-membrane-spanning bacterial nanomachines. Curr Opin Struct Biol 39:1–7

    Article  CAS  Google Scholar 

  • Gold VA, Robson A, Bao H, Romantsov T, Duong F, Collinson I (2010) The action of cardiolipin on the bacterial translocon. Proc Natl Acad Sci U S A 107:10044–10049

    Article  CAS  Google Scholar 

  • Green ER, Mecsas J (2016) Bacterial secretion systems: an overview. Microbiol Spectr 4. https://doi.org/10.1128/microbiolspec.VMBF-0012-2015

  • Grohmann E, Christie PJ, Waksman G, Backert S (2018) Type IV secretion in Gram-negative and Gram-positive bacteria. Mol Microbiol 107:455–471

    Article  CAS  Google Scholar 

  • Holland IB, Schmitt L, Young J (2005) Type 1 protein secretion in bacteria, the ABC-transporter dependent pathway (review). Mol Membr Biol 22:29–39

    Article  CAS  Google Scholar 

  • Hospenthal MK, Costa TRD, Waksman G (2017) A comprehensive guide to pilus biogenesis in Gram-negative bacteria. Nat Rev Microbiol 15:365–379

    Article  CAS  Google Scholar 

  • Jarrell KF, Ding Y, Nair DB, Siu S (2013) Surface appendages of archaea: structure, function, genetics and assembly. Life (Basel) 3:86–117

    Google Scholar 

  • Koo J, Lamers RP, Rubinstein JL, Burrows LL, Howell PL (2016) Structure of the Pseudomonas aeruginosa Type IVa pilus secretin at 7.4 A. Structure 24:1778–1787

    Article  CAS  Google Scholar 

  • Koronakis V, Sharff A, Koronakis E, Luisi B, Hughes C (2000) Crystal structure of the bacterial membrane protein TolC central to multidrug efflux and protein export. Nature 405:914–919

    Article  CAS  Google Scholar 

  • Korotkov KV, Sandkvist M, Hol WG (2012) The type II secretion system: biogenesis, molecular architecture and mechanism. Nat Rev Microbiol 10:336–351

    Article  CAS  Google Scholar 

  • Krause S, Pansegrau W, Lurz R, de la Cruz F, Lanka E (2000) Enzymology of type IV macromolecule secretion systems: the conjugative transfer regions of plasmids RP4 and R388 and the cag pathogenicity island of Helicobacter pylori encode structurally and functionally related nucleoside triphosphate hydrolases. J Bacteriol 182:2761–2770

    Article  CAS  Google Scholar 

  • Lill R, Dowhan W, Wickner W (1990) The ATPase activity of SecA is regulated by acidic phospholipids, SecY, and the leader and mature domains of precursor proteins. Cell 60:271–280

    Article  CAS  Google Scholar 

  • Low HH, Gubellini F, Rivera-Calzada A, Braun N, Connery S, Dujeancourt A, Lu F, Redzej A, Fronzes R, Orlova EV, Waksman G (2014) Structure of a type IV secretion system. Nature 508:550–553

    Article  CAS  Google Scholar 

  • Minamino T (2014) Protein export through the bacterial flagellar type III export pathway. Biochim Biophys Acta 1843:1642–1648

    Article  CAS  Google Scholar 

  • Pansegrau W, Bagnoli F (2017) Pilus assembly in gram-positive bacteria. Curr Top Microbiol Immunol 404:203–233

    CAS  PubMed  Google Scholar 

  • Patel R, Smith SM, Robinson C (2014) Protein transport by the bacterial Tat pathway. Biochim Biophys Acta 1843:1620–1628

    Article  CAS  Google Scholar 

  • Phoenix DA, Kusters R, Hikita C, Mizushima S, de Kruijff B (1993) OmpF-Lpp signal sequence mutants with varying charge hydrophobicity ratios provide evidence for a phosphatidylglycerol-signal sequence interaction during protein translocation across the Escherichia coli inner membrane. J Biol Chem 268:17069–17073

    CAS  PubMed  Google Scholar 

  • Prabudiansyah I, Kusters I, Caforio A, Driessen AJ (2015) Characterization of the annular lipid shell of the Sec translocon. Biochim Biophys Acta 1848:2050–2056

    Article  CAS  Google Scholar 

  • Rivera-Calzada A, Fronzes R, Savva CG, Chandran V, Lian PW, Laeremans T, Pardon E, Steyaert J, Remaut H, Waksman G, Orlova EV (2013) Structure of a bacterial type IV secretion core complex at subnanometre resolution. EMBO J 32:1195–1204

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Sohlenkamp C, Geiger O (2016) Bacterial membrane lipids: diversity in structures and pathways. FEMS Microbiol Rev 40:133–159

    Article  CAS  Google Scholar 

  • Thomas S, Holland IB, Schmitt L (2014) The Type 1 secretion pathway – the hemolysin system and beyond. Biochim Biophys Acta 1843:1629–1641

    Article  CAS  Google Scholar 

  • Thomassin JL, Santos Moreno J, Guilvout I, Tran Van Nhieu G, Francetic O (2017) The trans-envelope architecture and function of the type 2 secretion system: new insights raising new questions. Mol Microbiol 105:211–226

    Article  CAS  Google Scholar 

  • Tsirigotaki A, De Geyter J, Šoštaric N, Economou A, Karamanou S (2016) Protein export through the bacterial Sec pathway. Nat Rev Microbiol 15:21

    Article  Google Scholar 

  • Ulbrandt ND, London E, Oliver DB (1992) Deep penetration of a portion of Escherichia coli SecA protein into model membranes is promoted by anionic phospholipids and by partial unfolding. J Biol Chem 267:15184–15192

    CAS  PubMed  Google Scholar 

  • Van Gerven N, Waksman G, Remaut H (2011) Pili and flagella biology, structure, and biotechnological applications. Prog Mol Biol Transl Sci 103:21–72

    Article  Google Scholar 

  • Van Gerven N, Klein RD, Hultgren SJ, Remaut H (2015) Bacterial amyloid formation: structural insights into curli biogensis. Trends Microbiol 23:693–706

    Article  Google Scholar 

  • Weise CF, Login FH, Ho O, Grobner G, Wolf-Watz H, Wolf-Watz M (2014) Negatively charged lipid membranes promote a disorder-order transition in the Yersinia YscU protein. Biophys J 107:1950–1961

    Article  CAS  Google Scholar 

  • Worrall LJ, Hong C, Vuckovic M, Deng W, Bergeron JRC, Majewski DD, Huang RK, Spreter T, Finlay BB, Yu Z, Strynadka NCJ (2016) Near-atomic-resolution cryo-EM analysis of the Salmonella T3S injectisome basal body. Nature 540:597

    Article  CAS  Google Scholar 

  • Yan Z, Yin M, Xu D, Zhu Y, Li X (2017) Structural insights into the secretin translocation channel in the type II secretion system. Nat Struct Mol Biol 24:177–183

    Article  CAS  Google Scholar 

  • Zilkenat S, Franz-Wachtel M, Stierhof YD, Galan JE, Macek B, Wagner S (2016) Determination of the stoichiometry of the complete bacterial type III secretion needle complex using a combined quantitative proteomic approach. Mol Cell Proteomics 15:1598–1609

    Article  CAS  Google Scholar 

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Acknowledgments

Work in our laboratory is supported by grants from Dirección General de Asuntos del Personal Académico, Universidad Nacional Autónoma de México (DGAPA, UNAM; PAPIIT IN209617) and Consejo Nacional de Ciencia y Tecnología (CONACyT 284081). We acknowledge Dra. Norma Espinosa Sánchez for critical reading of the manuscript and excellent technical assistance.

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Correspondence to Bertha González-Pedrajo .

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Díaz-Guerrero, M.Á., Gaytán, M.O., González-Pedrajo, B. (2019). Structure: Function of Transmembrane Appendages in Gram-Negative Bacteria. In: Geiger, O. (eds) Biogenesis of Fatty Acids, Lipids and Membranes. Handbook of Hydrocarbon and Lipid Microbiology . Springer, Cham. https://doi.org/10.1007/978-3-319-50430-8_51

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