1887
No metrics data to plot.
The attempt to load metrics for this article has failed.
The attempt to plot a graph for these metrics has failed.

EcoSal Plus

Domain 4:

Synthesis and Processing of Macromolecules

Type V Secretion in Gram-Negative Bacteria

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.
  • Author: Harris D. Bernstein1
  • Editors: Maria Sandkvist2, Eric Cascales3, Peter J. Christie4
  • VIEW AFFILIATIONS HIDE AFFILIATIONS
    Affiliations: 1: Genetics and Biochemistry Branch, National Institute of Diabetes and Digestive and Kidney Diseases, National Institutes of Health, Bethesda, MD 20892; 2: Department of Microbiology and Immunology, University of Michigan, Ann Arbor, Michigan; 3: CNRS Aix-Marseille Université, Mediterranean Institute of Microbiology, Marseille, France; 4: Department of Microbiology and Molecular Genetics, McGovern Medical School, Houston, Texas
  • Received 27 August 2018 Accepted 05 December 2018 Published 06 March 2019
  • Address correspondence to Harris D. Bernstein, [email protected]
image of Type V Secretion in Gram-Negative Bacteria
    Preview this reference work article:
    Zoom in
    Zoomout

    Type V Secretion in Gram-Negative Bacteria, Page 1 of 2

    | /docserver/preview/fulltext/ecosalplus/8/2/ESP-0031-2018-1.gif /docserver/preview/fulltext/ecosalplus/8/2/ESP-0031-2018-2.gif
  • Abstract:

    Type V, or “autotransporter,” secretion is a term used to refer to several simple protein export pathways that are found in a wide range of Gram-negative bacteria. Autotransporters are generally single polypeptides that consist of an extracellular (“passenger”) domain and a β barrel domain that anchors the protein to the outer membrane (OM). Although it was originally proposed that the passenger domain is secreted through a channel formed solely by the covalently linked β barrel domain, experiments performed primarily on the type Va, or “classical,” autotransporter pathway have challenged this hypothesis. Several lines of evidence strongly suggest that both the secretion of the passenger domain and the membrane integration of the β barrel domain are catalyzed by the arrel ssembly achinery (Bam) complex, a conserved hetero-oligomer that plays an essential role in the assembly of most integral OM proteins. The secretion reaction appears to be driven at least in part by the folding of the passenger domain in the extracellular space. Although many aspects of autotransporter biogenesis remain to be elucidated, it will be especially interesting to determine whether the different classes of proteins that fall under the type V rubric—most of which have not been examined in detail—are assembled by the same basic mechanism as classical autotransporters.

  • Citation: Bernstein H. 2019. Type V Secretion in Gram-Negative Bacteria, EcoSal Plus 2019; doi:10.1128/ecosalplus.ESP-0031-2018

Article Version

This article is an updated version of the following content:

References

1. Henderson IR, Nataro JP. 2001. Virulence functions of autotransporter proteins. Infect Immun 69:1231–1243. http://dx.doi.org/10.1128/IAI.69.3.1231-1243.2001. [PubMed]
2. Pohlner J, Halter R, Beyreuther K, Meyer TF. 1987. Gene structure and extracellular secretion of Neisseria gonorrhoeae IgA protease. Nature 325:458–462. http://dx.doi.org/10.1038/325458a0. [PubMed]
3. Celik N, Webb CT, Leyton DL, Holt KE, Heinz E, Gorrell R, Kwok T, Naderer T, Strugnell RA, Speed TP, Teasdale RD, Likić VA, Lithgow T. 2012. A bioinformatic strategy for the detection, classification and analysis of bacterial autotransporters. PLoS One 7:e43245. http://dx.doi.org/10.1371/journal.pone.0043245. [PubMed]
4. Emsley P, Charles IG, Fairweather NF, Isaacs NW. 1996. Structure of Bordetella pertussis virulence factor P.69 pertactin. Nature 381:90–92. http://dx.doi.org/10.1038/381090a0. [PubMed]
5. Otto BR, Sijbrandi R, Luirink J, Oudega B, Heddle JG, Mizutani K, Park SY, Tame JR. 2005. Crystal structure of hemoglobin protease, a heme binding autotransporter protein from pathogenic Escherichia coli. J Biol Chem 280:17339–17345. http://dx.doi.org/10.1074/jbc.M412885200. [PubMed]
6. Junker M, Schuster CC, McDonnell AV, Sorg KA, Finn MC, Berger B, Clark PL. 2006. Pertactin beta-helix folding mechanism suggests common themes for the secretion and folding of autotransporter proteins. Proc Natl Acad Sci U S A 103:4918–4923. http://dx.doi.org/10.1073/pnas.0507923103. [PubMed]
7. Gangwer KA, Mushrush DJ, Stauff DL, Spiller B, McClain MS, Cover TL, Lacy DB. 2007. Crystal structure of the Helicobacter pylori vacuolating toxin p55 domain. Proc Natl Acad Sci U S A 104:16293–16298. http://dx.doi.org/10.1073/pnas.0707447104. [PubMed]
8. Heras B, Totsika M, Peters KM, Paxman JJ, Gee CL, Jarrott RJ, Perugini MA, Whitten AE, Schembri MA. 2014. The antigen 43 structure reveals a molecular Velcro-like mechanism of autotransporter-mediated bacterial clumping. Proc Natl Acad Sci U S A 111:457–462. http://dx.doi.org/10.1073/pnas.1311592111. [PubMed]
9. Leyton DL, Johnson MD, Thapa R, Huysmans GH, Dunstan RA, Celik N, Shen HH, Loo D, Belousoff MJ, Purcell AW, Henderson IR, Beddoe T, Rossjohn J, Martin LL, Strugnell RA, Lithgow T. 2014. A mortise-tenon joint in the transmembrane domain modulates autotransporter assembly into bacterial outer membranes. Nat Commun 5:4239. http://dx.doi.org/10.1038/ncomms5239. [PubMed]
10. Oomen CJ, van Ulsen P, van Gelder P, Feijen M, Tommassen J, Gros P. 2004. Structure of the translocator domain of a bacterial autotransporter. EMBO J 23:1257–1266. http://dx.doi.org/10.1038/sj.emboj.7600148. [PubMed]
11. Barnard TJ, Dautin N, Lukacik P, Bernstein HD, Buchanan SK. 2007. Autotransporter structure reveals intra-barrel cleavage followed by conformational changes. Nat Struct Mol Biol 14:1214–1220. http://dx.doi.org/10.1038/nsmb1322. [PubMed]
12. van den Berg B. 2010. Crystal structure of a full-length autotransporter. J Mol Biol 396:627–633. http://dx.doi.org/10.1016/j.jmb.2009.12.061. [PubMed]
13. Tajima N, Kawai F, Park SY, Tame JR. 2010. A novel intein-like autoproteolytic mechanism in autotransporter proteins. J Mol Biol 402:645–656. http://dx.doi.org/10.1016/j.jmb.2010.06.068. [PubMed]
14. Zhai Y, Zhang K, Huo Y, Zhu Y, Zhou Q, Lu J, Black I, Pang X, Roszak AW, Zhang X, Isaacs NW, Sun F. 2011. Autotransporter passenger domain secretion requires a hydrophobic cavity at the extracellular entrance of the β-domain pore. Biochem J 435:577–587. http://dx.doi.org/10.1042/BJ20101548. [PubMed]
15. Gawarzewski I, DiMaio F, Winterer E, Tschapek B, Smits SHJ, Jose J, Schmitt L. 2014. Crystal structure of the transport unit of the autotransporter adhesin involved in diffuse adherence from Escherichia coli. J Struct Biol 187:20–29. http://dx.doi.org/10.1016/j.jsb.2014.05.003. [PubMed]
16. Barnard TJ, Gumbart J, Peterson JH, Noinaj N, Easley NC, Dautin N, Kuszak AJ, Tajkhorshid E, Bernstein HD, Buchanan SK. 2012. Molecular basis for the activation of a catalytic asparagine residue in a self-cleaving bacterial autotransporter. J Mol Biol 415:128–142. http://dx.doi.org/10.1016/j.jmb.2011.10.049. [PubMed]
17. Dautin N, Bernstein HD. 2007. Protein secretion in gram-negative bacteria via the autotransporter pathway. Annu Rev Microbiol 61:89–112. http://dx.doi.org/10.1146/annurev.micro.61.080706.093233. [PubMed]
18. Meng G, Surana NK, St Geme JW, III, Waksman G. 2006. Structure of the outer membrane translocator domain of the Haemophilus influenzae Hia trimeric autotransporter. EMBO J 25:2297–2304. http://dx.doi.org/10.1038/sj.emboj.7601132. [PubMed]
19. Shahid SA, Bardiaux B, Franks WT, Krabben L, Habeck M, van Rossum BJ, Linke D. 2012. Membrane-protein structure determination by solid-state NMR spectroscopy of microcrystals. Nat Methods 9:1212–1217. http://dx.doi.org/10.1038/nmeth.2248. [PubMed]
20. Nummelin H, Merckel MC, Leo JC, Lankinen H, Skurnik M,Goldman A. 2004. The Yersinia adhesin YadA collagen-binding domain structure is a novel left-handed parallel β-roll. EMBO J 23:701–711. http://dx.doi.org/10.1038/sj.emboj.7600100. [PubMed]
21. Szczesny P, Linke D, Ursinus A, Bär K, Schwarz H, Riess TM, Kempf VA, Lupas AN, Martin J, Zeth K. 2008. Structure of the head of the Bartonella adhesin BadA. PLoS Pathog 4:e1000119. http://dx.doi.org/10.1371/journal.ppat.1000119. [PubMed]
22. Edwards TE, Phan I, Abendroth J, Dieterich SH, Masoudi A, Guo W, Hewitt SN, Kelley A, Leibly D, Brittnacher MJ, Staker BL, Miller SI, Van Voorhis WC, Myler PJ, Stewart LJ. 2010. Structure of a Burkholderia pseudomallei trimeric autotransporter adhesin head. PLoS One 5:e12803. http://dx.doi.org/10.1371/journal.pone.0012803. [PubMed]
23. Agnew C, Borodina E, Zaccai NR, Conners R, Burton NM, Vicary JA, Cole DK, Antognozzi M, Virji M, Brady RL. 2011. Correlation of in situ mechanosensitive responses of the Moraxella catarrhalis adhesin UspA1 with fibronectin and receptor CEACAM1 binding. Proc Natl Acad Sci U S A 108:15174–15178. http://dx.doi.org/10.1073/pnas.1106341108. [PubMed]
24. Leo JC, Lyskowski A, Hattula K, Hartmann MD, Schwarz H, Butcher SJ, Linke D, Lupas AN, Goldman A. 2011. The structure of E. coli IgG-binding protein D suggests a general model for bending and binding in trimeric autotransporter adhesins. Structure 19:1021–1030. http://dx.doi.org/10.1016/j.str.2011.03.021. [PubMed]
25. Hartmann MD, Grin I, Dunin-Horkawicz S, Deiss S, Linke D, Lupas AN, Hernandez Alvarez B. 2012. Complete fiber structures of complex trimeric autotransporter adhesins conserved in enterobacteria. Proc Natl Acad Sci U S A 109:20907–20912. http://dx.doi.org/10.1073/pnas.1211872110. [PubMed]
26. Malito E, Biancucci M, Faleri A, Ferlenghi I, Scarselli M, Maruggi G, Lo Surdo P, Veggi D, Liguori A, Santini L, Bertoldi I, Petracca R, Marchi S, Romagnoli G, Cartocci E, Vercellino I, Savino S, Spraggon G, Norais N, Pizza M, Rappuoli R, Masignani V, Bottomley MJ. 2014. Structure of the meningococcal vaccine antigen NadA and epitope mapping of a bactericidal antibody. Proc Natl Acad Sci U S A 111:17128–17133. http://dx.doi.org/10.1073/pnas.1419686111. [PubMed]
27. Koiwai K, Hartmann MD, Linke D, Lupas AN, Hori K. 2016. Structural basis for toughness and flexibility in the C-terminal passenger domain of an Acinetobacter trimeric autotransporter adhesin. J Biol Chem 291:3705–3724. http://dx.doi.org/10.1074/jbc.M115.701698. [PubMed]
28. Hamburger ZA, Brown MS, Isberg RR, Bjorkman PJ. 1999. Crystal structure of invasin: a bacterial integrin-binding protein. Science 286:291–295. http://dx.doi.org/10.1126/science.286.5438.291. [PubMed]
29. Fairman JW, Dautin N, Wojtowicz D, Liu W, Noinaj N, Barnard TJ, Udho E, Przytycka TM, Cherezov V, Buchanan SK. 2012. Crystal structures of the outer membrane domain of intimin and invasin from enterohemorrhagic E. coli and enteropathogenic Y. pseudotuberculosis. Structure 20:1233–1243. http://dx.doi.org/10.1016/j.str.2012.04.011. [PubMed]
30. Leo JC, Oberhettinger P, Schütz M, Linke D. 2015. The inverse autotransporter family: intimin, invasin and related proteins. Int J Med Microbiol 305:276–282. http://dx.doi.org/10.1016/j.ijmm.2014.12.011. [PubMed]
31. Gentle IE, Burri L, Lithgow T. 2005. Molecular architecture and function of the Omp85 family of proteins. Mol Microbiol 58:1216–1225. http://dx.doi.org/10.1111/j.1365-2958.2005.04906.x. [PubMed]
32. Arnold T, Zeth K, Linke D. 2010. Omp85 from the thermophilic cyanobacterium Thermosynechococcus elongatus differs from proteobacterial Omp85 in structure and domain composition. J Biol Chem 285:18003–18015. http://dx.doi.org/10.1074/jbc.M110.112516. [PubMed]
33. Salacha R, Kovacić F, Brochier-Armanet C, Wilhelm S, Tommassen J, Filloux A, Voulhoux R, Bleves S. 2010. The Pseudomonas aeruginosa patatin-like protein PlpD is the archetype of a novel type V secretion system. Environ Microbiol 12:1498–1512. [PubMed]
34. da Mata Madeira PV, Zouhir S, Basso P, Neves D, Laubier A, Salacha R, Bleves S, Faudry E, Contreras-Martel C, Dessen A. 2016. Structural basis of lipid targeting and destruction by the type V secretion system of Pseudomonas aeruginosa. J Mol Biol 428(9 Part A) :1790–1803. http://dx.doi.org/10.1016/j.jmb.2016.03.012. [PubMed]
35. Casasanta MA, Yoo CC, Smith HB, Duncan AJ, Cochrane K, Varano AC, Allen-Vercoe E, Slade DJ. 2017. A chemical and biological toolbox for type Vd secretion: characterization of the phospholipase A1 autotransporter FplA from Fusobacterium nucleatum. J Biol Chem 292:20240–20254. http://dx.doi.org/10.1074/jbc.M117.819144. [PubMed]
36. Pang SS, Nguyen ST, Perry AJ, Day CJ, Panjikar S, Tiralongo J, Whisstock JC, Kwok T. 2014. The three-dimensional structure of the extracellular adhesion domain of the sialic acid-binding adhesin SabA from Helicobacter pylori. J Biol Chem 289:6332–6340. http://dx.doi.org/10.1074/jbc.M113.513135. [PubMed]
37. Hage N, Howard T, Phillips C, Brassington C, Overman R, Debreczeni J, Gellert P, Stolnik S, Winkler GS, Falcone FH. 2015. Structural basis of Lewis(b) antigen binding by the Helicobacter pylori adhesin BabA. Sci Adv 1:e1500315. http://dx.doi.org/10.1126/sciadv.1500315. [PubMed]
38. Javaheri A, Kruse T, Moonens K, Mejías-Luque R, Debraekeleer A, Asche CI, Tegtmeyer N, Kalali B, Bach NC, Sieber SA, Hill DJ, Königer V, Hauck CR, Moskalenko R, Haas R, Busch DH, Klaile E, Slevogt H, Schmidt A, Backert S, Remaut H, Singer BB, Gerhard M. 2016. Helicobacter pylori adhesin HopQ engages in a virulence-enhancing interaction with human CEACAMs. Nat Microbiol 2:16189. http://dx.doi.org/10.1038/nmicrobiol.2016.189. [PubMed]
39. Moonens K, Gideonsson P, Subedi S, Bugaytsova J, Romaõ E, Mendez M, Nordén J, Fallah M, Rakhimova L, Shevtsova A, Lahmann M, Castaldo G, Brännström K, Coppens F, Lo AW, Ny T, Solnick JV, Vandenbussche G, Oscarson S, Hammarström L, Arnqvist A, Berg DE, Muyldermans S, Borén T, Remaut H. 2016. Structural insights into polymorphic ABO glycan binding by Helicobacter pylori. Cell Host Microbe 19:55–66. http://dx.doi.org/10.1016/j.chom.2015.12.004. [PubMed]
40. Coppens F, Castaldo G, Debraekeleer A, Subedi S, Moonens K, Lo A, Remaut H. 2018. Hop-family Helicobacter outer membrane adhesins form a novel class of type 5-like secretion proteins with an interrupted β-barrel domain. Mol Microbiol 110:33–46. http://dx.doi.org/10.1111/mmi.14075. [PubMed]
41. Ieva R, Bernstein HD. 2009. Interaction of an autotransporter passenger domain with BamA during its translocation across the bacterial outer membrane. Proc Natl Acad Sci U S A 106:19120–19125. http://dx.doi.org/10.1073/pnas.0907912106. [PubMed]
42. Junker M, Besingi RN, Clark PL. 2009. Vectorial transport and folding of an autotransporter virulence protein during outer membrane secretion. Mol Microbiol 71:1323–1332. http://dx.doi.org/10.1111/j.1365-2958.2009.06607.x. [PubMed]
43. Saurí A, Oreshkova N, Soprova Z, Jong WS, Sani M, Peters PJ, Luirink J, van Ulsen P. 2011. Autotransporter β-domains have a specific function in protein secretion beyond outer-membrane targeting. J Mol Biol 412:553–567. http://dx.doi.org/10.1016/j.jmb.2011.07.035. [PubMed]
44. Pavlova O, Peterson JH, Ieva R, Bernstein HD. 2013. Mechanistic link between β barrel assembly and the initiation of autotransporter secretion. Proc Natl Acad Sci U S A 110:E938–E947. http://dx.doi.org/10.1073/pnas.1219076110. [PubMed]
45. Khalid S, Sansom MS. 2006. Molecular dynamics simulations of a bacterial autotransporter: NalP from Neisseria meningitidis. Mol Membr Biol 23:499–508. http://dx.doi.org/10.1080/09687860600849531. [PubMed]
46. Tian P, Bernstein HD. 2010. Molecular basis for the structural stability of an enclosed β-barrel loop. J Mol Biol 402:475–489. http://dx.doi.org/10.1016/j.jmb.2010.07.035. [PubMed]
47. Veiga E, de Lorenzo V, Fernández LA. 2004. Structural tolerance of bacterial autotransporters for folded passenger protein domains. Mol Microbiol 52:1069–1080. http://dx.doi.org/10.1111/j.1365-2958.2004.04014.x. [PubMed]
48. Skillman KM, Barnard TJ, Peterson JH, Ghirlando R, Bernstein HD. 2005. Efficient secretion of a folded protein domain by a monomeric bacterial autotransporter. Mol Microbiol 58:945–958. http://dx.doi.org/10.1111/j.1365-2958.2005.04885.x. [PubMed]
49. Swanson KA, Taylor LD, Frank SD, Sturdevant GL, Fischer ER, Carlson JH, Whitmire WM, Caldwell HD. 2009. Chlamydia trachomatis polymorphic membrane protein D is an oligomeric autotransporter with a higher-order structure. Infect Immun 77:508–516. http://dx.doi.org/10.1128/IAI.01173-08. [PubMed]
50. Leyton DL, Sevastsyanovich YR, Browning DF, Rossiter AE, Wells TJ, Fitzpatrick RE, Overduin M, Cunningham AF, Henderson IR. 2011. Size and conformation limits to secretion of disulfide-bonded loops in autotransporter proteins. J Biol Chem 286:42283–42291. http://dx.doi.org/10.1074/jbc.M111.306118.
51. Kang’ethe W, Bernstein HD. 2013. Charge-dependent secretion of an intrinsically disordered protein via the autotransporter pathway. Proc Natl Acad Sci U S A 110:E4246–E4255. http://dx.doi.org/10.1073/pnas.1310345110. [PubMed]
52. Saurí A, Ten Hagen-Jongman CM, van Ulsen P, Luirink J. 2012. Estimating the size of the active translocation pore of an autotransporter. J Mol Biol 416:335–345. http://dx.doi.org/10.1016/j.jmb.2011.12.047. [PubMed]
53. Ieva R, Skillman KM, Bernstein HD. 2008. Incorporation of a polypeptide segment into the β-domain pore during the assembly of a bacterial autotransporter. Mol Microbiol 67:188–201. http://dx.doi.org/10.1111/j.1365-2958.2007.06048.x. [PubMed]
54. Peterson JH, Tian P, Ieva R, Dautin N, Bernstein HD. 2010. Secretion of a bacterial virulence factor is driven by the folding of a C-terminal segment. Proc Natl Acad Sci U S A 107:17739–17744. http://dx.doi.org/10.1073/pnas.1009491107. [PubMed]
55. Sauri A, Soprova Z, Wickström D, de Gier JW, Van der Schors RC, Smit AB, Jong WS, Luirink J. 2009. The Bam (Omp85) complex is involved in secretion of the autotransporter haemoglobin protease. Microbiology 155:3982–3991. http://dx.doi.org/10.1099/mic.0.034991-0. [PubMed]
56. Ieva R, Tian P, Peterson JH, Bernstein HD. 2011. Sequential and spatially restricted interactions of assembly factors with an autotransporter β domain. Proc Natl Acad Sci U S A 108:E383–E391. http://dx.doi.org/10.1073/pnas.1103827108. [PubMed]
57. Peterson JH, Hussain S, Bernstein HD. 2018. Identification of a novel post-insertion step in the assembly of a bacterial outer membrane protein. Mol Microbiol 110:143–159. http://dx.doi.org/10.1111/mmi.14102. [PubMed]
58. Voulhoux R, Bos MP, Geurtsen J, Mols M, Tommassen J. 2003. Role of a highly conserved bacterial protein in outer membrane protein assembly. Science 299:262–265. http://dx.doi.org/10.1126/science.1078973. [PubMed]
59. Wu T, Malinverni J, Ruiz N, Kim S, Silhavy TJ, Kahne D. 2005. Identification of a multicomponent complex required for outer membrane biogenesis in Escherichia coli. Cell 121:235–245. http://dx.doi.org/10.1016/j.cell.2005.02.015. [PubMed]
60. Jain S, Goldberg MB. 2007. Requirement for YaeT in the outer membrane assembly of autotransporter proteins. J Bacteriol 189:5393–5398. http://dx.doi.org/10.1128/JB.00228-07. [PubMed]
61. Hagan CL, Kim S, Kahne D. 2010. Reconstitution of outer membrane protein assembly from purified components. Science 328:890–892. http://dx.doi.org/10.1126/science.1188919. [PubMed]
62. Noinaj N, Kuszak AJ, Gumbart JC, Lukacik P, Chang H, Easley NC, Lithgow T, Buchanan SK. 2013. Structural insight into the biogenesis of β-barrel membrane proteins. Nature 501:385–390. http://dx.doi.org/10.1038/nature12521. [PubMed]
63. Sikdar R, Peterson JH, Anderson DE, Bernstein HD. 2017. Folding of a bacterial integral outer membrane protein is initiated in the periplasm. Nat Commun 8:1309. http://dx.doi.org/10.1038/s41467-017-01246-4. [PubMed]
64. Hussain S, Bernstein HD. 2018. The Bam complex catalyzes efficient insertion of bacterial outer membrane proteins into membrane vesicles of variable lipid composition. J Biol Chem 293:2959–2973. http://dx.doi.org/10.1074/jbc.RA117.000349. [PubMed]
65. Walton TA, Sandoval CM, Fowler CA, Pardi A, Sousa MC. 2009. The cavity-chaperone Skp protects its substrate from aggregation but allows independent folding of substrate domains. Proc Natl Acad Sci U S A 106:1772–1777. http://dx.doi.org/10.1073/pnas.0809275106. [PubMed]
66. Schiffrin B, Calabrese AN, Devine PWA, Harris SA, Ashcroft AE, Brockwell DJ, Radford SE. 2016. Skp is a multivalent chaperone of outer-membrane proteins. Nat Struct Mol Biol 23:786–793. http://dx.doi.org/10.1038/nsmb.3266. [PubMed]
67. Albenne C, Ieva R. 2017. Job contenders: roles of the β-barrel assembly machinery and the translocation and assembly module in autotransporter secretion. Mol Microbiol 106:505–517. http://dx.doi.org/10.1111/mmi.13832. [PubMed]
68. Soprova Z, Sauri A, van Ulsen P, Tame JR, den Blaauwen T, Jong WS, Luirink J. 2010. A conserved aromatic residue in the autochaperone domain of the autotransporter Hbp is critical for initiation of outer membrane translocation. J Biol Chem 285:38224–38233. http://dx.doi.org/10.1074/jbc.M110.180505. [PubMed]
69. Bennion D, Charlson ES, Coon E, Misra R. 2010. Dissection of β-barrel outer membrane protein assembly pathways through characterizing BamA POTRA 1 mutants of Escherichia coli. Mol Microbiol 77:1153–1171. http://dx.doi.org/10.1111/j.1365-2958.2010.07280.x. [PubMed]
70. Baud C, Guérin J, Petit E, Lesne E, Dupré E, Locht C, Jacob-Dubuisson F. 2014. Translocation path of a substrate protein through its Omp85 transporter. Nat Commun 5:5271. http://dx.doi.org/10.1038/ncomms6271. [PubMed]
71. Roman-Hernandez G, Peterson JH, Bernstein HD. 2014. Reconstitution of bacterial autotransporter assembly using purified components. eLife 3:e04234. http://dx.doi.org/10.7554/eLife.04234. [PubMed]
72. Klauser T, Pohlner J, Meyer TF. 1992. Selective extracellular release of cholera toxin B subunit by Escherichia coli: dissection of Neisseria Iga β-mediated outer membrane transport. EMBO J 11:2327–2335. http://dx.doi.org/10.1002/j.1460-2075.1992.tb05292.x. [PubMed]
73. Doyle MT, Tran EN, Morona R. 2015. The passenger-associated transport repeat promotes virulence factor secretion efficiency and delineates a distinct autotransporter subtype. Mol Microbiol 97:315–329. http://dx.doi.org/10.1111/mmi.13027. [PubMed]
74. Velarde JJ, Nataro JP. 2004. Hydrophobic residues of the autotransporter EspP linker domain are important for outer membrane translocation of its passenger. J Biol Chem 279:31495–31504. http://dx.doi.org/10.1074/jbc.M404424200. [PubMed]
75. Renn JP, Clark PL. 2008. A conserved stable core structure in the passenger domain β-helix of autotransporter virulence proteins. Biopolymers 89:420–427. http://dx.doi.org/10.1002/bip.20924. [PubMed]
76. Baclayon M, Ulsen P, Mouhib H, Shabestari MH, Verzijden T, Abeln S, Roos WH, Wuite GJ. 2016. Mechanical unfolding of an autotransporter passenger protein reveals the secretion starting point and processive transport intermediates. ACS Nano 10:5710–5719. http://dx.doi.org/10.1021/acsnano.5b07072. [PubMed]
77. Besingi RN, Chaney JL, Clark PL. 2013. An alternative outer membrane secretion mechanism for an autotransporter protein lacking a C-terminal stable core. Mol Microbiol 90:1028–1045. http://dx.doi.org/10.1111/mmi.12414. [PubMed]
78. Leo JC, Oberhettinger P, Yoshimoto S, Udatha DB, Morth JP, Schütz M, Hori K, Linke D. 2016. Secretion of the intimin passenger domain is driven by protein folding. J Biol Chem 291:20096–20112. http://dx.doi.org/10.1074/jbc.M116.731497. [PubMed]
79. Yuan X, Johnson MD, Zhang J, Lo AW, Schembri MA, Wijeyewickrema LC, Pike RN, Huysmans GHM, Henderson IR, Leyton DL. 2018. Molecular basis for the folding of β-helical autotransporter passenger domains. Nat Commun 9:1395. http://dx.doi.org/10.1038/s41467-018-03593-2. [PubMed]
80. Kang’ethe W, Bernstein HD. 2013. Stepwise folding of an autotransporter passenger domain is not essential for its secretion. J Biol Chem 288:35028–35038. http://dx.doi.org/10.1074/jbc.M113.515635. [PubMed]
81. Stock JB, Rauch B, Roseman S. 1977. Periplasmic space in Salmonella typhimurium and Escherichia coli. J Biol Chem 252:7850–7861. [PubMed]
82. Geibel S, Procko E, Hultgren SJ, Baker D, Waksman G. 2013. Structural and energetic basis of folded-protein transport by the FimD usher. Nature 496:243–246. http://dx.doi.org/10.1038/nature12007. [PubMed]
83. Goyal P, Krasteva PV, Van Gerven N, Gubellini F, Van den Broeck I, Troupiotis-Tsaïlaki A, Jonckheere W, Péhau-Arnaudet G, Pinkner JS, Chapman MR, Hultgren SJ, Howorka S, Fronzes R, Remaut H. 2014. Structural and mechanistic insights into the bacterial amyloid secretion channel CsgG. Nature 516:250–253. http://dx.doi.org/10.1038/nature13768. [PubMed]
84. Ruiz-Perez F, Henderson IR, Leyton DL, Rossiter AE, Zhang Y, Nataro JP. 2009. Roles of periplasmic chaperone proteins in the biogenesis of serine protease autotransporters of Enterobacteriaceae. J Bacteriol 191:6571–6583. http://dx.doi.org/10.1128/JB.00754-09. [PubMed]
85. Ruiz-Perez F, Henderson IR, Nataro JP. 2010. Interaction of FkpA, a peptidyl-prolyl cis/trans isomerase with EspP autotransporter protein. Gut Microbes 1:339–344. http://dx.doi.org/10.4161/gmic.1.5.13436. [PubMed]
86. Rizzitello AE, Harper JR, Silhavy TJ. 2001. Genetic evidence for parallel pathways of chaperone activity in the periplasm of Escherichia coli. J Bacteriol 183:6794–6800. http://dx.doi.org/10.1128/JB.183.23.6794-6800.2001. [PubMed]
87. Purdy GE, Fisher CR, Payne SM. 2007. IcsA surface presentation in Shigella flexneri requires the periplasmic chaperones DegP, Skp, and SurA. J Bacteriol 189:5566–5573. http://dx.doi.org/10.1128/JB.00483-07. [PubMed]
88. Peterson JH, Plummer AM, Fleming KG, Bernstein HD. 2017. Selective pressure for rapid membrane integration constrains the sequence of bacterial outer membrane proteins. Mol Microbiol 106:777–792. http://dx.doi.org/10.1111/mmi.13845. [PubMed]
89. Norell D, Heuck A, Tran-Thi TA, Götzke H, Jacob-Dubuisson F, Clausen T, Daley DO, Braun V, Müller M, Fan E. 2014. Versatile in vitro system to study translocation and functional integration of bacterial outer membrane proteins. Nat Commun 5:5396. http://dx.doi.org/10.1038/ncomms6396. [PubMed]
90. Selkrig J, Mosbahi K, Webb CT, Belousoff MJ, Perry AJ, Wells TJ, Morris F, Leyton DL, Totsika M, Phan MD, Celik N, Kelly M, Oates C, Hartland EL, Robins-Browne RM, Ramarathinam SH, Purcell AW, Schembri MA, Strugnell RA, Henderson IR, Walker D, Lithgow T. 2012. Discovery of an archetypal protein transport system in bacterial outer membranes. Nat Struct Mol Biol 19:506–510, S1. http://dx.doi.org/10.1038/nsmb.2261.
91. Shen HH, Leyton DL, Shiota T, Belousoff MJ, Noinaj N, Lu J, Holt SA, Tan K, Selkrig J, Webb CT, Buchanan SK, Martin LL, Lithgow T. 2014. Reconstitution of a nanomachine driving the assembly of proteins into bacterial outer membranes. Nat Commun 5:5078. http://dx.doi.org/10.1038/ncomms6078. [PubMed]
92. Heinz E, Stubenrauch CJ, Grinter R, Croft NP, Purcell AW, Strugnell RA, Dougan G, Lithgow T. 2016. Conserved features in the structure, mechanism, and biogenesis of the inverse autotransporter protein family. Genome Biol Evol 8:1690–1705. http://dx.doi.org/10.1093/gbe/evw112. [PubMed]
93. Bamert RS, Lundquist K, Hwang H, Webb CT, Shiota T, Stubenrauch CJ, Belousoff MJ, Goode RJA, Schittenhelm RB, Zimmerman R, Jung M, Gumbart JC, Lithgow T. 2017. Structural basis for substrate selection by the translocation and assembly module of the β-barrel assembly machinery. Mol Microbiol 106:142–156. http://dx.doi.org/10.1111/mmi.13757. [PubMed]
94. Stubenrauch C, Belousoff MJ, Hay ID, Shen HH, Lillington J, Tuck KL, Peters KM, Phan MD, Lo AW, Schembri MA, Strugnell RA, Waksman G, Lithgow T. 2016. Effective assembly of fimbriae in Escherichia coli depends on the translocation assembly module nanomachine. Nat Microbiol 1:16064. http://dx.doi.org/10.1038/nmicrobiol.2016.64. [PubMed]
95. Grin I, Hartmann MD, Sauer G, Hernandez Alvarez B, Schütz M, Wagner S, Madlung J, Macek B, Felipe-Lopez A, Hensel M, Lupas A, Linke D. 2014. A trimeric lipoprotein assists in trimeric autotransporter biogenesis in enterobacteria. J Biol Chem 289:7388–7398. http://dx.doi.org/10.1074/jbc.M113.513275. [PubMed]
96. Noinaj N, Gumbart JC, Buchanan SK. 2017. The β-barrel assembly machinery in motion. Nat Rev Microbiol 15:197–204. http://dx.doi.org/10.1038/nrmicro.2016.191. [PubMed]
97. Janssen R, Tommassen J. 1994. PhoE protein as a carrier for foreign epitopes. Int Rev Immunol 11:113–121. http://dx.doi.org/10.3109/08830189409061719. [PubMed]
98. Yeo HJ, Yokoyama T, Walkiewicz K, Kim Y, Grass S, Geme JW, III. 2007. The structure of the Haemophilus influenzae HMW1 pro-piece reveals a structural domain essential for bacterial two-partner secretion. J Biol Chem 282:31076–31084. http://dx.doi.org/10.1074/jbc.M705750200. [PubMed]
99. Clantin B, Delattre AS, Rucktooa P, Saint N, Méli AC, Locht C, Jacob-Dubuisson F, Villeret V. 2007. Structure of the membrane protein FhaC: a member of the Omp85-TpsB transporter superfamily. Science 317:957–961. http://dx.doi.org/10.1126/science.1143860. [PubMed]
100. Bernstein HD. 2015. Looks can be deceiving: recent insights into the mechanism of protein secretion by the autotransporter pathway. Mol Microbiol 97:205–215. http://dx.doi.org/10.1111/mmi.13031. [PubMed]
101. Nash ZM, Cotter PA. 2019. Bordetella filamentous hemagglutinin, a model for the two partner secretion pathway. Microbiol Spectr 7:PSIB-0024-2019.
102. journal-id:
Loading

Article metrics loading...

/content/journal/ecosalplus/10.1128/ecosalplus.ESP-0031-2018
2019-03-06
2019-10-21

Abstract:

Type V, or “autotransporter,” secretion is a term used to refer to several simple protein export pathways that are found in a wide range of Gram-negative bacteria. Autotransporters are generally single polypeptides that consist of an extracellular (“passenger”) domain and a β barrel domain that anchors the protein to the outer membrane (OM). Although it was originally proposed that the passenger domain is secreted through a channel formed solely by the covalently linked β barrel domain, experiments performed primarily on the type Va, or “classical,” autotransporter pathway have challenged this hypothesis. Several lines of evidence strongly suggest that both the secretion of the passenger domain and the membrane integration of the β barrel domain are catalyzed by the arrel ssembly achinery (Bam) complex, a conserved hetero-oligomer that plays an essential role in the assembly of most integral OM proteins. The secretion reaction appears to be driven at least in part by the folding of the passenger domain in the extracellular space. Although many aspects of autotransporter biogenesis remain to be elucidated, it will be especially interesting to determine whether the different classes of proteins that fall under the type V rubric—most of which have not been examined in detail—are assembled by the same basic mechanism as classical autotransporters.

Highlighted Text: Show | Hide
Loading full text...

Full text loading...

Comment has been disabled for this content
Submit comment
Close
Comment moderation successfully completed

Figures

Image of Figure 1
Figure 1

Proteins in type V (and type V-like) secretion pathways consist of a 12-stranded (red), 16-stranded (green), or predicted 8-stranded (pink) β barrel domain and an extracellular (“passenger”) domain that typically folds into a β-helical (blue), mixed coiled-coil/β roll/β prism (purple) or globular (brown) structure. The 16-stranded β barrel domains are members of the Omp85 superfamily and contain periplasmic POTRA domains. In most cases the β barrel and passenger domains are covalently linked, but in the type Vb pathway the β barrel domain and the extracellular component (“exoprotein”) are separate polypeptides. In the type Vc pathway both domains are formed through the assembly of three identical subunits. The passenger domain is located at the N terminus of the protein in the type Va, Vb, Vc, and Vd pathways, but it is found at the C terminus in the type Ve pathway. In the type V-like pathway the extracellular domain is located in a loop that connects the first two β strands of the β barrel domain. Crystal structures of representative polypeptides from each pathway are shown. α-helical segments are colored red and β strands are colored yellow. The structures include the pertactin (Prn) passenger domain ( 4 ) (PDB code 1DAB), a fragment of the HMW1 exoprotein ( 98 ) (PDB code 2ODL), a fragment of the EibD passenger domain ( 24 ) (PDB code 2XQH), the phospholipase D (PlpD) passenger domain ( 34 ) (PDB code 5FYA), the invasin (Inv) passenger domain ( 28 ) (1CWV), the SabA extracellular domain ( 36 ) (PDB code 4O5J), and the NalP, FhaC, Hia, and intimin (Int) β barrel domains (PDB codes 1UYO, 4QKY, 2GR7, and 4E1S) ( 10 , 18 , 29 , 99 ). The helix inside the FhaC β barrel was generated from a neighboring asymmetric unit in the crystal lattice. No structures of β barrel domains of type Vd or type V-like proteins have been reported. Modified from ( 100 ), with permission.

Citation: Bernstein H. 2019. Type V Secretion in Gram-Negative Bacteria, EcoSal Plus 2019; doi:10.1128/ecosalplus.ESP-0031-2018
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 2
Figure 2

Available evidence suggests that the β barrel domain (red) begins to fold in the periplasm (step I) and incorporates the C terminus of the passenger domain (blue) in a hairpin conformation. At this stage the β barrel domain interacts with the molecular chaperone Skp. The partially folded β barrel domain is then targeted to the OM, where it binds to BamA, BamB, and BamD in a stereospecific fashion (step II). The surface exposure of the passenger domain and the initiation of translocation require an additional assembly step in which the β barrel domain moves into the membrane (step III). Both autotransporter and BamA β barrels are in an open conformation at this stage. Translocation involves the progressive movement of passenger domain segments from the chaperone SurA to the POTRA domains of BamA to the transport channel and is driven at least in part by vectorial folding (step IV). Following the completion of translocation the hairpin is resolved (step V), and an unusual lipid-facing basic or large polar residue found in at least a subset of autotransporters facilitates the completion of β barrel domain assembly (step VI). The β barrel domain is then released from the Bam complex, and, in some cases, the two domains are separated by an intrabarrel cleavage or an extrabarrel cleavage mediated by a -acting protease (step VII). In the Bam complex contains five subunits, but BamC and BamE have been omitted for clarity. Modified from ( 57 , 100 ), with permission.

Citation: Bernstein H. 2019. Type V Secretion in Gram-Negative Bacteria, EcoSal Plus 2019; doi:10.1128/ecosalplus.ESP-0031-2018
Permissions and Reprints Request Permissions
Download as Powerpoint

Supplemental Material

No supplementary material available for this content.

This is a required field
Please enter a valid email address
Please check the format of the address you have entered.
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error