1887

Chapter 8 : Bacterial Secretion Systems: An Overview

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.

Ebook: Choose a downloadable PDF or ePub file. Chapter is a downloadable PDF file. File must be downloaded within 48 hours of purchase

Buy this Chapter
Digital (?) $15.00

Preview this chapter:
Zoom in
Zoomout

Bacterial Secretion Systems: An Overview, Page 1 of 2

| /docserver/preview/fulltext/10.1128/9781555819286/9781555819279_Chap08-1.gif /docserver/preview/fulltext/10.1128/9781555819286/9781555819279_Chap08-2.gif

Abstract:

One essential prokaryotic cell function is the transport of proteins from the cytoplasm into other compartments of the cell, the environment, and/or other bacteria or eukaryotic cells—a process known as protein secretion. Prokaryotes have developed numerous ways of transporting protein cargo between locations, which largely involve the assistance of dedicated protein secretion systems. Protein secretion systems are essential for the growth of bacteria and are used in an array of processes. Some secretion systems are found in almost all bacteria and secrete a wide variety of substrates, while others have been identified in only a small number of bacterial species or are dedicated to secreting only one or a few proteins. In certain cases, these dedicated secretion systems are used by bacterial pathogens to manipulate the host and establish a replicative niche. Other times, they are required to take advantage of an environmental niche, perhaps by secreting proteins that help bacteria to compete with nearby microorganisms. There are several different classes of bacterial secretion systems, and their designs can differ based on whether their protein substrates cross a single phospholipid membrane, two membranes, or even three membranes, where two are bacterial and one is a host membrane. Due to the specificity of expression of some of these secretion systems in bacterial pathogens, antimicrobials are being developed against these systems to augment our current repertoire of antibiotics. This topic is discussed in Section VII, “Targeted Therapies”.

Citation: Green E, Mecsas J. 2016. Bacterial Secretion Systems: An Overview, p 215-239. In Kudva I, Cornick N, Plummer P, Zhang Q, Nicholson T, Bannantine J, Bellaire B (ed),

Virulence Mechanisms of Bacterial Pathogens, Fifth Edition

. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.VMBF-0012-2015
Highlighted Text: Show | Hide
Loading full text...

Full text loading...

Figures

Image of Figure 1
Figure 1

Export through the Sec pathway. In bacteria, the Sec pathway transports unfolded proteins across the cytoplasmic membrane. Proteins secreted by this pathway may either become embedded in the inner membrane or will be released into the periplasm. In Gram-negative organisms, these periplasmic proteins may be released extracellularly with the help of an additional secretion system. Proteins destined for the periplasm (or extracellular release) are translocated by a posttranslational mechanism and contain a removable signal sequence recognized by the SecB protein. SecB binds presecretory proteins and prevents them from folding while also delivering its substrates to SecA. SecA both guides proteins to the SecYEG channel and serves as the ATPase that provides the energy for protein translocation. Following transport through the SecYEG channel, proteins are folded in the periplasm. () The Sec pathway utilizes a cotranslational mechanism of export to secrete proteins destined for the inner membrane. These proteins contain a signal sequence recognized by the signal recognition particle (SRP). During translation, the SRP binds target proteins as they emerge from the ribosome and recruits the docking protein FtsY. FtsY delivers the ribosome-protein complex to the SecYEG channel, which translocates the nascent protein across the cytoplasmic membrane. During translocation across the channel, the transmembrane domain is able to escape through the side of the channel into the membrane, where the protein remains attached.

Citation: Green E, Mecsas J. 2016. Bacterial Secretion Systems: An Overview, p 215-239. In Kudva I, Cornick N, Plummer P, Zhang Q, Nicholson T, Bannantine J, Bellaire B (ed),

Virulence Mechanisms of Bacterial Pathogens, Fifth Edition

. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.VMBF-0012-2015
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 2
Figure 2

Secretion through the Tat pathway. Bacteria secrete folded proteins across the cytoplasmic membrane using the Tat secretion pathway. This pathway consists of two or three components (TatA, TatB, and TatC). In Gram-negative bacteria, TatB and TatC bind a specific N-terminal signal peptide containing a “twin” arginine motif on folded Tat secretion substrates. TatB and TatC then recruit TatA to the cytoplasmic membrane, where it forms a channel. Folded proteins are then translocated across the channel and into the periplasm. In Gram-negative bacteria, these proteins may remain in the periplasm or can be exported out of the cell by the T2SS.

Citation: Green E, Mecsas J. 2016. Bacterial Secretion Systems: An Overview, p 215-239. In Kudva I, Cornick N, Plummer P, Zhang Q, Nicholson T, Bannantine J, Bellaire B (ed),

Virulence Mechanisms of Bacterial Pathogens, Fifth Edition

. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.VMBF-0012-2015
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 3
Figure 3

Secretion systems in Gram-negative bacteria. Gram-negative bacteria utilize a number of dedicated protein secretion systems to transport proteins across one, two, or three phospholipid membranes. Some proteins are secreted in a two-step, Sec- or Tat-dependent mechanism. These proteins cross the inner membrane with the help of either the Sec or Tat secretion pathways and are then transported across the outer membrane using a second secretion system. The T2SS and T5SS secrete proteins in this manner. Because it secretes folded substrates, the T2SS translocates proteins initially transported by either the Tat or Sec pathway (where Sec substrates are folded in the periplasm). In contrast, autotransporters of the T5SS must be unfolded prior to outer membrane transport and thus must be secreted across the inner membrane by the Sec pathway. Additionally, several Gram-negative protein secretion systems transport their substrates across both bacterial membranes in a one-step, Sec- or Tat-independent process. These include the T1SS, T3SS, T4SS, and T6SS. All of these pathways contain periplasm-spanning channels and secrete proteins from the cytoplasm outside the cell, but their mechanisms of protein secretion are quite different. Three of these secretion systems, the T3SS, T4SS, and T6SS, can also transport proteins across an additional host cell membrane, delivering secreted proteins directly to the cytosol of a target cell.

Citation: Green E, Mecsas J. 2016. Bacterial Secretion Systems: An Overview, p 215-239. In Kudva I, Cornick N, Plummer P, Zhang Q, Nicholson T, Bannantine J, Bellaire B (ed),

Virulence Mechanisms of Bacterial Pathogens, Fifth Edition

. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.VMBF-0012-2015
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 4
Figure 4

Four secretion systems in Gram-positive bacteria. Gram-positive bacteria contain a single cytoplasmic membrane surrounded by a very thick cell wall. These organisms can secrete proteins across the membrane using the Tat and Sec secretion systems. In contrast to Gram-negative organisms, many Gram-positive bacteria use an additional factor for Sec secretion of a smaller subset of proteins, called SecA2. Additionally, there is evidence that some Gram-positive bacteria may use dedicated secretion apparatuses, called “injectosomes” to transport proteins from the bacterial cytoplasm into the cytoplasm of a host cell in a two-step process. The specific mechanism of this process has not been determined, though it has been proposed that the injectosome may utilize a protected channel to transport proteins across the cell wall during export.

Citation: Green E, Mecsas J. 2016. Bacterial Secretion Systems: An Overview, p 215-239. In Kudva I, Cornick N, Plummer P, Zhang Q, Nicholson T, Bannantine J, Bellaire B (ed),

Virulence Mechanisms of Bacterial Pathogens, Fifth Edition

. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.VMBF-0012-2015
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 5
Figure 5

The T7SS. Certain Gram-positive organisms, including members of the genus , contain a cell wall layer that is heavily modified by lipids, called a mycomembrane. These organisms contain a distinct protein secretion apparatus called a T7SS. T7SSs contain several core inner membrane proteins that interact with cytosolic chaperones and form a channel through which proteins are secreted. Additionally, it has been proposed that T7SSs may contain an additional, mycomembrane-spanning channel that aids in extracellular secretion of substrates, though this model has not been experimentally proven.

Citation: Green E, Mecsas J. 2016. Bacterial Secretion Systems: An Overview, p 215-239. In Kudva I, Cornick N, Plummer P, Zhang Q, Nicholson T, Bannantine J, Bellaire B (ed),

Virulence Mechanisms of Bacterial Pathogens, Fifth Edition

. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.VMBF-0012-2015
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 6
Figure 6

Mechanisms of innate immune recognition of bacterial secretion systems. To distinguish between pathogenic and commensal bacteria, the mammalian innate immune system has developed methods to directly recognize patterns unique to bacterial pathogens, such as the use of protein secretion apparatuses. The immune system can sense several facets of bacterial protein secretion. These include the pore formation by secretion systems or secreted proteins, aberrant translocation of bacterial molecules into the cytosol, the presence of effector proteins and/or their activities, as well as the components of the secretion systems themselves.

Citation: Green E, Mecsas J. 2016. Bacterial Secretion Systems: An Overview, p 215-239. In Kudva I, Cornick N, Plummer P, Zhang Q, Nicholson T, Bannantine J, Bellaire B (ed),

Virulence Mechanisms of Bacterial Pathogens, Fifth Edition

. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.VMBF-0012-2015
Permissions and Reprints Request Permissions
Download as Powerpoint

References

/content/book/10.1128/9781555819286.chap8
1. 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 : 17351756.[PubMed] [CrossRef]
2. Papanikou E,, Karamanou S,, Economou A . 2007. Bacterial protein secretion through the translocase nanomachine. Nat Rev Microbiol 5 : 839851.[PubMed] [CrossRef]
3. Robinson C,, Bolhuis A . 2004. Tat-dependent protein targeting in prokaryotes and chloroplasts. Biochim Biophys Acta Mol Cell Res 1694 : 135147.[PubMed] [CrossRef]
4. Korotkov KV,, Sandkvist M,, Hol WGH . 2012. The type II secretion system: biogenesis, molecular architecture and mechanism. Nat Rev Microbiol 10 : 336351.[PubMed] [CrossRef]
5. Lenz LL,, Mohammadi S,, Geissler A,, Portnoy DA . 2003. SecA2-dependent secretion of autolytic enzymes promotes Listeria monocytogenes pathogenesis. Proc Natl Acad Sci USA 100 : 1243212437.[PubMed] [CrossRef]
6. Braunstein M,, Espinosa BJ,, Chan J,, Belisle JT,, Jacobs WR . 2003. SecA2 functions in the secretion of superoxide dismutase A and in the virulence of Mycobacterium tuberculosis . Mol Microbiol 48 : 453464.[PubMed] [CrossRef]
7. Lenz LL,, Portnoy DA . 2002. Identification of a second Listeria secA gene associated with protein secretion and the rough phenotype. Mol Microbiol 45 : 10431056.[PubMed] [CrossRef]
8. Bensing BA,, Sullam PM . 2002. An accessory sec locus of Streptococcus gordonii is required for export of the surface protein GspB and for normal levels of binding to human platelets. Mol Microbiol 44 : 10811094.[PubMed] [CrossRef]
9. Randall LL,, Hardy SJ . 2002. SecB, one small chaperone in the complex milieu of the cell. Cell Mol Life Sci 59 : 16171623.[PubMed] [CrossRef]
10. Hartl FU,, Lecker S,, Schiebel E,, Hendrick JP,, Wickner W . 1990. The binding cascade of SecB to SecA to SecY/E mediates preprotein targeting to the E. coli plasma membrane. Cell 63 : 269279.[PubMed] [CrossRef]
11. Mogensen JE,, Otzen DE . 2005. Interactions between folding factors and bacterial outer membrane proteins. Mol Microbiol 57 : 326346.[PubMed] [CrossRef]
12. Luirink J,, Sinning I . 2004. SRP-mediated protein targeting: structure and function revisited. Biochim Biophys Acta Mol Cell Res 1694 : 1735.[PubMed] [CrossRef]
13. Sijbrandi R,, Urbanus ML,, ten Hagen-Jongman CM,, Bernstein HD,, Oudega B,, Otto BR,, Luirink J . 2003. Signal recognition particle (SRP)-mediated targeting and sec-dependent translocation of an extracellular Escherichia coli protein. J Biol Chem 278 : 46544659.[PubMed] [CrossRef]
14. Paetzel M,, Karla A,, Strynadka NCJ,, Dalbey RE . 2002. Signal peptidases. Chem Rev 102 : 45494579.[PubMed] [CrossRef]
15. Berks BC,, Palmer T,, Sargent F . 2005. Protein targeting by the bacterial twin-arginine translocation (Tat) pathway. Curr Opin Microbiol 8 : 174181.[PubMed] [CrossRef]
16. Sargent F,, Stanley NR,, Berks BC,, Palmer T . 1999. Sec-independent protein translocation in Escherichia coli: a distinct and pivotal role for the TatB protein. J Biol Chem 274 : 3607336082.[PubMed] [CrossRef]
17. Pop O,, Martin U,, Abel C,, Muller JP . 2002. The twin-arginine signal peptide of PhoD and the TatA(d)/C-d proteins of Bacillus subtilis form an autonomous tat translocation system. J Biol Chem 277 : 32683273.[PubMed] [CrossRef]
18. Müller M . 2005. Twin-arginine-specific protein export in Escherichia coli . Res Microbiol 156 : 131136.[PubMed] [CrossRef]
19. Ochsner UA,, Snyder A,, Vasil AI,, Vasil ML . 2002. Effects of the twin-arginine translocase on secretion of virulence factors, stress response, and pathogenesis. Proc Natl Acad Sci USA 99 : 83128317.[PubMed] [CrossRef]
20. Lavander M,, Ericsson SK,, Broms JE,, Forsberg A . 2006. The twin arginine translocation system is essential for virulence of Yersinia pseudotuberculosis . Infect Immun 74 : 17681776.[PubMed] [CrossRef]
21. Pradel N,, Ye CY,, Livrelli V,, Xu HG,, Joly B,, Wu LF . 2003. Contribution of the twin arginine translocation system to the virulence of enterohemorrhagic Escherichia coli O157:H7. Infect Immun 71 : 49084916.[PubMed] [CrossRef]
22. Rossier O,, Cianciotto NP . 2005. The Legionella pneumophila tatB gene facilitates secretion of phospholipase C, growth under iron-limiting conditions, and intracellular infection. Infect Immun 73 : 20202032.[PubMed] [CrossRef]
23. McDonough JA,, McCann JR,, Tekippe EM,, Silverman JS,, Rigel NW,, Braunstein M . 2008. Identification of functional Tat signal sequences in Mycobacterium tuberculosis proteins. J Bacteriol 190 : 64286438.[PubMed] [CrossRef]
24. Songer JG . 1997. Bacterial phospholipases and their role in virulence. Trends Microbiol 5 : 156161.[PubMed] [CrossRef]
25. Thomas S,, Holland IB,, Schmitt L . 2014. The type 1 secretion pathway: the hemolysin system and beyond. Biochim Biophys Acta 1843 : 16291641.[PubMed] [CrossRef]
26. Symmons MF,, Bokma E,, Koronakis E,, Hughes C,, Koronakis V . 2009. The assembled structure of a complete tripartite bacterial multidrug efflux pump. Proc Natl Acad Sci USA 106 : 71737178.[PubMed] [CrossRef]
27. Delepelaire P . 2004. Type I secretion in Gram-negative bacteria. Biochim Biophys Acta 1694 : 149161.[PubMed] [CrossRef]
28. Kanonenberg K,, Schwarz CK,, Schmitt L . 2013. Type I secretion systems: a story of appendices. Res Microbiol 164 : 596604.[PubMed] [CrossRef]
29. Letoffe S,, Delepelaire P,, Wandersman C . 1996. Protein secretion in Gram-negative bacteria: assembly of the three components of ABC protein-mediated exporters is ordered and promoted by substrate binding. EMBO J 15 : 58045811.[PubMed]
30. Pimenta AL,, Young J,, Holland IB,, Blight MA . 1999. Antibody analysis of the localisation, expression and stability of HlyD, the MFP component of the E. coli haemolysin translocator. Mol Gen Genet 261 : 122132.[PubMed] [CrossRef]
31. Lee M,, Jun SY,, Yoon BY,, Song S,, Lee K,, Ha NC . 2012. Membrane fusion proteins of type I secretion system and tripartite efflux pumps share a binding motif for TolC in Gram-negative bacteria. PLoS One 7 : e40460. doi:10.1371/journal.pone.0040460. [CrossRef]
32. Balakrishnan L,, Hughes C,, Koronakis V . 2001. Substrate-triggered recruitment of the TolC channel-tunnel during type I export of hemolysin by Escherichia coli . J Mol Biol 313 : 501510.[PubMed] [CrossRef]
33. Wu KH,, Tai PC . 2004. Cys32 and His105 are the critical residues for the calcium-dependent cysteine proteolytic activity of CvaB, an ATP-binding cassette transporter. J Biol Chem 279 : 901919.[PubMed] [CrossRef]
34. Lecher J,, Schwarz CK,, Stoldt M,, Smits SH,, Willbold D,, Schmitt L . 2012. An RTX transporter tethers its unfolded substrate during secretion via a unique N-terminal domain. Structure 20 : 17781787.[PubMed] [CrossRef]
35. Linhartova I,, Bumba L,, Masin J,, Basler M,, Osicka R,, Kamanova J,, Prochazkova K,, Adkins I,, Hejnova-Holubova J,, Sadilkova L,, Morova J,, Sebo P . 2010. RTX proteins: a highly diverse family secreted by a common mechanism. FEMS Microbiol Rev 34 : 10761112.[PubMed] [CrossRef]
36. Dolores JS,, Agarwal S,, Egerer M,, Satchell KJ . 2015. Vibrio cholerae MARTX toxin heterologous translocation of beta-lactamase and roles of individual effector domains on cytoskeleton dynamics. Mol Microbiol 95 : 590604.[PubMed] [CrossRef]
37. Welch RA,, Dellinger EP,, Minshew B,, Falkow S . 1981. Haemolysin contributes to virulence of extra-intestinal E. coli infections. Nature 294 : 665667.[PubMed] [CrossRef]
38. Hughes C,, Muller D,, Hacker J,, Goebel W . 1982. Genetics and pathogenic role of Escherichia coli haemolysin. Toxicon 20 : 247252.[PubMed] [CrossRef]
39. Mackman N,, Holland IB . 1984. Functional characterization of a cloned haemolysin determinant from E. coli of human origin, encoding information for the secretion of a 107K polypeptide. Mol Gen Genet 196 : 129134.[PubMed] [CrossRef]
40. Voulhoux R,, Ball G,, Ize B,, Vasil ML,, Lazdunski A,, Wu LF,, Filloux A . 2001. Involvement of the twin-arginine translocation system in protein secretion via the type II pathway. EMBO J 20 : 67356741.[PubMed] [CrossRef]
41. Cianciotto NP . 2005. Type II secretion: a protein secretion system for all seasons. Trends Microbiol 13 : 581588.[PubMed] [CrossRef]
42. Korotkov KV,, Gonen T,, Hol WGJ . 2100. Secretins: dynamic channels for protein transport across membranes. Trends Biochem Sci 36 : 433443.[PubMed] [CrossRef]
43. Sauvonnet N,, Vignon G,, Pugsley AP,, Gounon P . 2000. Pilus formation and protein secretion by the same machinery in Escherichia coli . EMBO J 19 : 22212228.[PubMed] [CrossRef]
44. Hobbs M,, Mattick JS . 1993. Common components in the assembly of type-4 fimbriae, DNA transfer systems, filamentous phage and protein-secretion apparatus: a general system for the formation of surface-associated protein complexes. Mol Microbiol 10 : 233243.[PubMed] [CrossRef]
45. Shevchik VE,, Robert-Baudouy J,, Condemine G . 1997. Specific interaction between OutD, an Erwinia chrysanthemi outer membrane protein of the general secretory pathway, and secreted proteins. EMBO J 16 : 30073016.[PubMed] [CrossRef]
46. Sandkvist M,, Michel LO,, Hough LP,, Morales VM,, Bagdasarian M,, Koomey M,, DiRita VJ,, Bagdasarian M . 1997. General secretion pathway (eps) genes required for toxin secretion and outer membrane biogenesis in Vibrio cholerae . J Bacteriol 179 : 69947003.[PubMed]
47. Lu HM,, Lory S . 1996. A specific targeting domain in mature exotoxin A is required for its extracellular secretion from Pseudomonas aeruginosa . EMBO J 15 : 429436.[PubMed]
48. Cianciotto NP . 2013. Type II secretion and Legionella virulence . Curr Topics Microbiol Immunol 376 : 81102.[PubMed] [CrossRef]
49. Kulkarni R,, Dhakal BK,, Slechta ES,, Kurtz Z,, Mulvey MA,, Thanassi DG . 2009. Roles of putative type II secretion and type IV pilus systems in the virulence of uropathogenic Escherichia coli . Plos One 4 : e4752. doi:10.1371/journal.pone.0004752. [PubMed] [CrossRef]
50. Tauschek M,, Gorrell RJ,, Strugnell RA,, Robins-Browne RM . 2002. Identification of a protein secretory pathway for the secretion of heat-labile enterotoxin by an enterotoxigenic strain of Escherichia coli . Proc Natl Acad Sci USA 99 : 70667071.[PubMed] [CrossRef]
51. Lathem WW,, Grys TE,, Witowski SE,, Torres AG,, Kaper JB,, Tarr PI,, Welch RS . 2002. StcE, a metalloprotease secreted by Escherichia coli O157:H7, specifically cleaves C1 esterase inhibitor. Mol Microbiol 45 : 277288.[PubMed] [CrossRef]
52. Pugsley AP,, Chapon C,, Schwartz M . 1986. Extracellular pullulanase of Klebsiella pneumoniae is a lipoprotein. J Bacteriol 166 : 10831088.[PubMed]
53. Jiang B,, Howard SP . 1992. The aeromonas-hydrophila exeE gene, required both for protein secretion and normal outer-membrane biogenesis, is a member of a general secretion pathway. Mol Microbiol 6 : 13511361.[PubMed] [CrossRef]
54. He SY,, Lindeberg M,, Chatterjee AK,, Collmer A . 1991. Cloned Erwinia chrysanthemi out genes enable Escherichia coli to selectively secrete a diverse family of heterologous proteins to its milieu. Proc Natl Acad Sci USA 88 : 10791083.[PubMed] [CrossRef]
55. Buttner D . 2012. Protein export according to schedule: architecture, assembly, and regulation of type III secretion systems from plant- and animal-pathogenic bacteria. Microbiol Mol Biol Rev 76 : 262310.[PubMed] [CrossRef]
56. Abrusci P,, McDowell MA,, Lea SM,, Johnson S . 2014. Building a secreting nanomachine: a structural overview of the T3SS. Curr Opin Struct Biol 25 : 111117.[PubMed] [CrossRef]
57. Burkinshaw BJ,, Strynadka NC . 2014. Assembly and structure of the T3SS. Biochim Biophys Acta 1843 : 16491663.[PubMed] [CrossRef]
58. Troisfontaines P,, Cornelis GR . 2005. Type III secretion: more systems than you think. Physiology (Bethesda) 20 : 326339.[PubMed] [CrossRef]
59. Kubori T,, Matsushima Y,, Nakamura D,, Uralil J,, Lara-Tejero M,, Sukhan A,, Galan JE,, Aizawa SI . 1998. Supramolecular structure of the Salmonella typhimurium type III protein secretion system. Science 280 : 602605.[PubMed] [CrossRef]
60. Deane JE,, Cordes FS,, Roversi P,, Johnson S,, Kenjale R,, Picking WD,, Picking WL,, Lea SM,, Blocker S . 2006. Expression, purification, crystallization and preliminary crystallographic analysis of MxiH, a subunit of the Shigella flexneri type III secretion system needle. Acta Crystallogr Sect F Struct Biol Cryst Commun 62(Pt 3): 302305.[PubMed] [CrossRef]
61. Demers JP,, Habenstein B,, Loquet A,, Kumar Vasa S,, Giller K,, Becker S,, Baker D,, Lange A,, Sgourakis NG . 2014. High-resolution structure of the Shigella type-III secretion needle by solid-state NMR and cryo-electron microscopy. Nat Commun 5 : 4976. [PubMed] [CrossRef]
62. Dohlich K,, Zumsteg AB,, Goosmann C,, Kolbe M . 2014. A substrate-fusion protein is trapped inside the type III secretion system channel in Shigella flexneri . PLoS Pathog 10 : e1003881. doi:10.1371/journal.ppat.1003881. [CrossRef]
63. Radics J,, Konigsmaier L,, Marlovits TC . 2014. Structure of a pathogenic type 3 secretion system in action. Nat Struct Mol Biol 21 : 8287.[PubMed] [CrossRef]
64. Price SB,, Cowan C,, Perry RD,, Straley SC . 1991. The Yersinia pestis V antigen is a regulatory protein necessary for Ca2(+)-dependent growth and maximal expression of low-Ca2+ response virulence genes. J Bacteriol 173 : 26492657.[PubMed]
65. Picking WL,, Nishioka H,, Hearn PD,, Baxter MA,, Harrington AT,, Blocker A,, Picking WD . 2005. IpaD of Shigella flexneri is independently required for regulation of Ipa protein secretion and efficient insertion of IpaB and IpaC into host membranes. Infect Immun 73 : 14321440.[PubMed] [CrossRef]
66. Holmstrom A,, Olsson J,, Cherepanov P,, Maier E,, Nordfelth R,, Pettersson J,, Benz R,, Wolf-Watz H,, Forsberg S . 2001. LcrV is a channel size-determining component of the Yop effector translocon of Yersinia . Mol Microbiol 39 : 620632.[PubMed] [CrossRef]
67. Hakansson S,, Bergman T,, Vanooteghem JC,, Cornelis G,, Wolf-Watz H . 1993. YopB and YopD constitute a novel class of Yersinia Yop proteins. Infect Immun 61 : 7180.[PubMed]
68. Hakansson S,, Schesser K,, Persson C,, Galyov EE,, Rosqvist R,, Homble F,, Wolf-Watz H . 1996. The YopB protein of Yersinia pseudotuberculosis is essential for the translocation of Yop effector proteins across the target cell plasma membrane and displays a contact-dependent membrane disrupting activity. EMBO J 15 : 58125823.[PubMed]
69. Akopyan K,, Edgren T,, Wang-Edgren H,, Rosqvist R,, Fahlgren A,, Wolf-Watz H,, Fallman M . 2011. Translocation of surface-localized effectors in type III secretion. Proc Natl Acad Sci USA 108 : 16391644.[PubMed] [CrossRef]
70. Edgren T,, Forsberg A,, Rosqvist R,, Wolf-Watz H . 2012. Type III secretion in Yersinia: injectisome or not? PLoS Pathog 8 : e1002669. doi:10.1371/journal.ppat.1002669. [PubMed] [CrossRef]
71. Angot A,, Vergunst A,, Genin S,, Peeters N . 2007. Exploitation of eukaryotic ubiquitin signaling pathways by effectors translocated by bacterial type III and type IV secretion systems. PLoS Pathog 3 : e3. doi:10.1371/journal.ppat.0030003. [PubMed] [CrossRef]
72. Ham H,, Sreelatha A,, Orth K . 2011. Manipulation of host membranes by bacterial effectors. Nat Rev Microbiol 9 : 635646.[PubMed] [CrossRef]
73. Spano S,, Galan JE . 2013. A novel anti-microbial function for a familiar Rab GTPase. Small GTPases 4 : 252254.[PubMed] [CrossRef]
74. Tosi T,, Pflug A,, Discola KF,, Neves D,, Dessen A . 2013. Structural basis of eukaryotic cell targeting by type III secretion system (T3SS) effectors. Res Microbiol 164 : 605619.[PubMed] [CrossRef]
75. Cascales E,, Christie PJ . 2003. The versatile bacterial type IV secretion systems. Nat Rev Microbiol 1 : 137149.[PubMed] [CrossRef]
76. Lessl M,, Lanka E . 1994. Common mechanisms in bacterial conjugation and Ti-mediated T-DNA transfer to plant cells. Cell 77 : 321324.[PubMed] [CrossRef]
77. Bundock P,, den Dulk-Ras A,, Beijersbergen A,, Hooykaas PJ . 1995. Trans-kingdom T-DNA transfer from Agrobacterium tumefaciens to Saccharomyces cerevisiae . EMBO J 14 : 32063214.[PubMed]
78. Fronzes R,, Christie PJ,, Waksman G . 2009. The structural biology of type IV secretion systems. Nat Rev Microbiol 7 : 703714.[PubMed] [CrossRef]
79. Atmakuri K,, Cascales E,, Christie PJ . 2004. Energetic components VirD4, VirB11 and VirB4 mediate early DNA transfer reactions required for bacterial type IV secretion. Mol Microbiol 54 : 11991211.[PubMed] [CrossRef]
80. Babic A,, Lindner AB,, Vulic M,, Stewart EJ,, Radman M . 2008. Direct visualization of horizontal gene transfer. Science 319 : 15331536.[PubMed] [CrossRef]
81. Hamilton HL,, Dillard JP . 2006. Natural transformation of Neisseria gonorrhoeae: from DNA donation to homologous recombination. Mol Microbiol 59 : 376385.[PubMed] [CrossRef]
82. Backert S,, Meyer TF . 2006. Type IV secretion systems and their effectors in bacterial pathogenesis. Curr Opin Microbiol 9 : 207217.[PubMed] [CrossRef]
83. Isberg RR,, O’Connor TJ,, Heidtman M . 2009. The Legionella pneumophila replication vacuole: making a cosy niche inside host cells. Nat Rev Microbiol 7 : 1324.[PubMed] [CrossRef]
84. Pohlner J,, Halter R,, Beyreuther K,, Meyer TF . 1987. Gene structure and extracellular secretion of Neisseria gonorrhoeae IgA protease. Nature 325 : 458462.[PubMed] [CrossRef]
85. Leyton DL,, Rossiter AE,, Henderson IR . 2012. From self sufficiency to dependence: mechanisms and factors important for autotransporter biogenesis. Nat Rev Microbiol 10 : 213225.[PubMed] [CrossRef]
86. van Ulsen P,, Rahman SU,, Jong WSP,, Daleke-Schermerhorn MH,, Luirink J . 2014. Type V secretion: from biogenesis to biotechnology. Biochim Biophys Acta Mol Cell Res 1843 : 15921611.[PubMed] [CrossRef]
87. Pohlner J,, Halter R,, Meyer TF . 1987. Neisseria gonorrhoeae IgA protease. Secretion and implications for pathogenesis. Antonie Van Leeuwenhoek 53 : 479484.[PubMed] [CrossRef]
88. Brandon LD,, Goehring N,, Janakiraman A,, Yan AW,, Wu T,, Beckwith J,, Goldberg MB . 2003. IcsA, a polarly localized autotransporter with an atypical signal peptide, uses the Sec apparatus for secretion, although the Sec apparatus is circumferentially distributed. Mol Microbiol 50 : 4560.[PubMed] [CrossRef]
89. Zumsteg AB,, Goosmann C,, Brinkmann V,, Morona R,, Zychlinsky A . 2014. IcsA is a Shigella flexneri adhesion regulated by the type III secretion system and required for pathogenesis. Cell Host Microbe 15 : 435445.[PubMed] [CrossRef]
90. Roggenkamp A,, Ackermann N,, Jacobi CA,, Truelzsch K,, Hoffmann H,, Heesemann H . 2003. Molecular analysis of transport and oligomerization of the Yersinia enterocolitica adhesin YadA. J Bacteriol 185 : 37353744.[PubMed] [CrossRef]
91. Mikula KM,, Kolodziejczyk R,, Goldman A . 2013. Yersinia infection tools: characterization of structure and function of adhesins. Front Cell Infect Microbiol 2 : 169. [PubMed] [CrossRef]
92. Leyton DL,, Rossiter AE,, Henderson IR . 2012. From self sufficiency to dependence: mechanisms and factors important for autotransporter biogenesis. Nat Rev Microbiol 10 : 213225.[PubMed] [CrossRef]
93. Wagner JK,, Heindl JE,, Gray AN,, Jain S,, Goldberg MB . 2009. Contribution of the periplasmic chaperone Skp to efficient presentation of the autotransporter IcsA on the surface of Shigella flexneri . J Bacteriol 191 : 815821.[PubMed] [CrossRef]
94. 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 : 65716583.[PubMed] [CrossRef]
95. Henderson IR,, Navarro-Garcia F,, Desvaux M,, Fernandez RC,, Ala’Aldeen D . 2004. Type V protein secretion pathway: the autotransporter story. Microbiol Mol Biol Rev 68 : 692744.[PubMed] [CrossRef]
96. Lambert-Buisine C,, Willery E,, Locht C,, Jacob-Dubuisson F . 1998. N-terminal characterization of the Bordetella pertussis filamentous haemagglutinin. Mol Microbiol 28 : 12831293.[PubMed] [CrossRef]
97. McCann JR,, St Geme JW 3rd . 2014. The HMW1C-like glycosyltransferases: an enzyme family with a sweet tooth for simple sugars. PLoS Pathog 10 : e1003977. doi:10.1371/journal.ppat.1003977. [PubMed] [CrossRef]
98. Waksman G,, Hultgren SJ . 2009. Structural biology of the chaperone-usher pathway of pilus biogenesis. Nat Rev Microbiol 7 : 765774.[PubMed] [CrossRef]
99. Mougous JD,, Cuff ME,, Raunser S,, Shen A,, Zhou M,, Gifford CA,, Goodman AL,, Joachimiak G,, Ordoñez CL,, Lory S,, Walz T,, Joachimiak A,, Mekalanos JJ . 2006. A virulence locus of Pseudomonas aeruginosa encodes a protein secretion apparatus. Science 312 : 15261530.[PubMed] [CrossRef]
100. Russell AB,, Peterson SB,, Mougous JD . 2014. Type VI secretion system effectors: poisons with a purpose. Nat Rev Microbiol 12 : 137148.[PubMed] [CrossRef]
101. Russell AB,, Hood RD,, Bui NK,, LeRoux M,, Vollmer W,, Mougous JD . 2011. Type VI secretion delivers bacteriolytic effectors to target cells. Nature 475 : 343347.[PubMed] [CrossRef]
102. Pukatzki S,, Ma AT,, Revel AT,, Sturtevant D,, Mekalanos JJ . 2007. Type VI secretion system translocates a phage tail spike-like protein into target cells where it cross-links actin. Proc Natl Acad Sci USA 104 : 1550815513.[PubMed] [CrossRef]
103. English G,, Trunk K,, Rao VA,, Srikannathasan V,, Hunter WN,, Coulthurst SJ . 2012. New secreted toxins and immunity proteins encoded within the type VI secretion system gene cluster of Serratia marcescens . Mol Microbiol 86 : 921936.[PubMed] [CrossRef]
104. Feltcher ME,, Braunstein M . 2012. Emerging themes in SecA2-mediated protein export. Nat Rev Microbiol 10 : 779789.[PubMed] [CrossRef]
105. Freudl R . 2013. Leaving home ain’t easy: protein export systems in Gram-positive bacteria. Res Microbiol 164 : 664674.[PubMed] [CrossRef]
106. Rigel NW,, Braunstein M . 2008. A new twist on an old pathway: accessory Sec [corrected] systems. Mol Microbiol 69 : 291302.[PubMed] [CrossRef]
107. Bensing BA,, Seepersaud R,, Yen YT,, Sullam PM . 2014. Selective transport by SecA2: an expanding family of customized motor proteins. Biochim Biophys Acta 1843 : 16741686.[PubMed] [CrossRef]
108. Hou JM,, D’Lima NG,, Rigel NW,, Gibbons HS,, McCann JR,, Braunstein M,, Teschke CM . 2008. ATPase activity of Mycobacterium tuberculosis SecA1 and SecA2 proteins and its importance for SecA2 function in macrophages. J Bacteriol 190 : 48804887.[PubMed] [CrossRef]
109. Fagan RP,, Fairweather NF . 2011. Clostridium difficile has two parallel and essential Sec secretion systems. J Biol Chem 286 : 2748327493.[PubMed] [CrossRef]
110. Siboo IR,, Chaffin DO,, Rubens CE,, Sullam PM . 2008. Characterization of the accessory Sec system of Staphylococcus aureus . J Bacteriol 190 : 61886196.[PubMed] [CrossRef]
111. Mistou MY,, Dramsi S,, Brega S,, Poyart C,, Trieu-Cuot P . 2009. Molecular dissection of the secA2 locus of group B Streptococcus reveals that glycosylation of the Srr1 LPXTG protein is required for full virulence. J Bacteriol 191 : 41954206.[PubMed] [CrossRef]
112. Seepersaud R,, Bensing BA,, Yen YT,, Sullam PM . 2010. Asp3 mediates multiple protein-protein interactions within the accessory Sec system of Streptococcus gordonii . Mol Microbiol 78 : 490505.[PubMed] [CrossRef]
113. Telford JL,, Barocchi MA,, Margarit I,, Rappuoli R,, Grandi G . 2006. Pili in Gram-positive pathogens. Nat Rev Microbiol 4 : 509519.[PubMed] [CrossRef]
114. Hendrickx AP,, Budzik JM,, Oh SY,, Schneewind O . 2011. Architects at the bacterial surface: sortases and the assembly of pili with isopeptide bonds. Nat Rev Microbiol 9 : 166176.[PubMed] [CrossRef]
115. Mazmanian SK,, Liu G,, Hung TT,, Schneewind O . 1999. Staphylococcus aureus sortase, an enzyme that anchors surface proteins to the cell wall. Science 285 : 760763.[PubMed] [CrossRef]
116. Madden JC,, Ruiz N,, Caparon M . 2001. Cytolysin-mediated translocation (CMT): A functional equivalent of type III secretion in Gram-positive bacteria. Cell 104 : 143152.[CrossRef]
117. Ghosh J,, Caparon MG . 2006. Specificity of Streptococcus pyogenes NAD(+) glycohydrolase in cytolysin-mediated translocation. Mol Microbiol. 62 : 12031214.[PubMed] [CrossRef]
118. Tweten RK . 2005. Cholesterol-dependent cytolysins, a family of versatile pore-forming toxins. Infect Immun 73 : 61996209.[PubMed] [CrossRef]
119. Madden JC,, Ruiz N,, Caparon M . 2001. Cytolysin-mediated translocation (CMT): a functional equivalent of type III secretion in Gram-positive bacteria. Cell 104 : 143152.[CrossRef]
120. Ghosh J,, Anderson PJ,, Chandrasekaran S,, Caparon MG . 2010. Characterization of Streptococcus pyogenes beta-NAD(+) glycohydrolase re-evaluation of enzymatic properties associated with pathogenesis. J Biol Chem 285 : 56835694.[PubMed] [CrossRef]
121. Magassa NG,, Chandrasekaran S,, Caparon MG . 2010. Streptococcus pyogenes cytolysin-mediated translocation does not require pore formation by streptolysin O. EMBO Rep 11 : 400405.[PubMed] [CrossRef]
122. Simeone R,, Bottai D,, Brosch R . 2009. ESX/type VII secretion systems and their role in host-pathogen interaction. Curr Opin Microbiol 12 : 410.[PubMed] [CrossRef]
123. Houben EN,, Korotkov KV,, Bitter W . 2014. Take five: type VII secretion systems of Mycobacteria . Biochim Biophys Acta 1843 : 17071716.[PubMed] [CrossRef]
124. Stanley SA,, Raghavan S,, Hwang WW,, Cox JS . 2003. Acute infection and macrophage subversion by Mycobacterium tuberculosis require a specialized secretion system. Proc Natl Acad Sci USA 100 : 1300113006.[PubMed] [CrossRef]
125. Burts ML,, Williams WA,, DeBord K,, Missiakas DM . 2005. EsxA and EsxB are secreted by an ESAT-6-like system that is required for the pathogenesis of Staphylococcus aureus infections. Proc Natl Acad Sci USA 102 : 11691174.[PubMed] [CrossRef]
126. Way SS,, Wilson CB . 2005. The Mycobacterium tuberculosis ESAT-6 homologue in Listeria monocytogenes is dispensable for growth in vitro and in vivo . Infect Immun 73 : 61516153.[PubMed] [CrossRef]
127. Baptista C,, Barreto HC,, Sao-Jose C . 2013. High levels of DegU-P activate an Esat-6-like secretion system in Bacillus subtilis . PLoS One 8 : e67840. doi:10.1371/journal.pone.0067840. [CrossRef]
128. Houben EN,, Bestebroer J,, Ummels R,, Wilson L,, Piersma SR,, Jimenez CR,, Ottenhoff TH,, Luirink J,, Bitter W . 2012. Composition of the type VII secretion system membrane complex. Mol Microbiol 86 : 472484.[PubMed] [CrossRef]
129. Luthra A,, Mahmood A,, Arora A,, Ramachandran R . 2008. Characterization of Rv3868, an essential hypothetical protein of the ESX-1 secretion system in Mycobacterium tuberculosis . J Biol Chem 283 : 3653236541.[PubMed] [CrossRef]
130. Ohol YM,, Goetz DH,, Chan K,, Shiloh MU,, Craik CS,, Cox JS . 2010. Mycobacterium tuberculosis MycP1 protease plays a dual role in regulation of ESX-1 secretion and virulence. Cell Host Microbe 7 : 210220.[PubMed] [CrossRef]
131. Champion PAD,, Stanley SA,, Champion MM,, Brown EJ,, Cox JS . 2006. C-terminal signal sequence promotes virulence factor secretion in Mycobacterium tuberculosis . Science 313 : 16321636.[PubMed] [CrossRef]
132. Daleke MH,, van der Woude AD,, Parret AH,, Ummels R,, de Groot AM,, Watson D,, Piersma SR,, Jimenez CR,, Luirink J,, Bitter W,, Houben EN . 2012. Specific chaperones for the type VII protein secretion pathway. J Biol Chem 287 : 3193931947.[PubMed] [CrossRef]
133. Hoffmann C,, Leis A,, Niederweis M,, Plitzko JM,, Engelhardt H . 2008. Disclosure of the mycobacterial outer membrane: cryo-electron tomography and vitreous sections reveal the lipid bilayer structure. Proc Natl Acad Sci USA 105 : 39633967.[PubMed] [CrossRef]
134. Zuber B,, Chami M,, Houssin C,, Dubochet J,, Griffiths G,, Daffe M . 2008. Direct visualization of the outer membrane of Mycobacteria and Corynebacteria in their native state. J Bacteriol 190 : 56725680.[PubMed] [CrossRef]
135. Pym AS,, Brodin P,, Brosch R,, Huerre M,, Cole ST . 2002. Loss of RD1 contributed to the attenuation of the live tuberculosis vaccines Mycobacterium bovis BCG and Mycobacterium microti . Mol Microbiol 46 : 709717.[PubMed] [CrossRef]
136. Lewis KN,, Liao R,, Guinn KM,, Hickey MJ,, Smith S,, Behr MA,, Sherman DR . 2003. Deletion of RD1 from Mycobacterium tuberculosis mimics bacille Calmette-Guerin attenuation. J Infect Dis 187 : 117123.[PubMed] [CrossRef]
137. Gey Van Pittius NC,, Gamieldien J,, Hide W,, Brown GD,, Siezen RJ,, Beyers AD . 2001. The ESAT-6 gene cluster of Mycobacterium tuberculosis and other high G+C Gram-positive bacteria. Genome Biol 2 : RESEARCH0044.
138. Coros A,, Callahan B,, Battaglioli E,, Derbyshire KM . 2008. The specialized secretory apparatus ESX-1 is essential for DNA transfer in Mycobacterium smegmatis . Mol Microbiol 69 : 794808.[PubMed]
139. Siegrist MS,, Unnikrishnan M,, McConnell MJ,, Borowsky M,, Cheng TY,, Siddiqi N,, Fortune SM,, Moody DB,, Rubin EJ . 2009. Mycobacterial Esx-3 is required for mycobactin-mediated iron acquisition. Proc Natl Acad Sci USA 106 : 1879218797.[PubMed] [CrossRef]
140. Ekiert DC,, Cox JS . 2014. Structure of a PE-PPE-EspG complex from Mycobacterium tuberculosis reveals molecular specificity of ESX protein secretion. Proc Natl Acad Sci USA 111 : 1475814763.[PubMed] [CrossRef]
141. Vance RE,, Isberg RR,, Portnoy DA . 2009. Patterns of pathogenesis: discrimination of pathogenic and nonpathogenic microbes by the innate immune system. Cell Host Microbe 6 : 1021.[PubMed] [CrossRef]
142. Wang X,, Parashar K,, Sitaram A,, Bliska JB . 2014. The GAP activity of type III effector YopE triggers killing of Yersinia in macrophages. PLoS Pathog 10 : e1004346. doi:10.1371/journal.ppat.1004346. [PubMed] [CrossRef]
143. Harder J,, Franchi L,, Munoz-Planillo R,, Park JH,, Reimer T,, Nunez G . 2009. Activation of the Nlrp3 inflammasome by Streptococcus pyogenes requires streptolysin O and NF-kappa B activation but proceeds independently of TLR signaling and P2X7 receptor. J Immunol 183 : 58235829.[PubMed] [CrossRef]
144. Osei-Owusu P,, Jessen DL,, Toosky M,, Roughead W,, Bradley DS,, Nilles ML . 2015. The N-terminus of the type III secretion needle protein YscF from Yersinia pestis functions to modulate innate immune responses. Infect Immun 83 : 15071522.[PubMed] [CrossRef]

Tables

Generic image for table
TABLE 1

Classes of bacterial protein secretion systems

Citation: Green E, Mecsas J. 2016. Bacterial Secretion Systems: An Overview, p 215-239. In Kudva I, Cornick N, Plummer P, Zhang Q, Nicholson T, Bannantine J, Bellaire B (ed),

Virulence Mechanisms of Bacterial Pathogens, Fifth Edition

. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.VMBF-0012-2015

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