Chapter 18 : Type I Secretion Systems—One Mechanism for All?

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

Preview this chapter:
Zoom in

Type I Secretion Systems—One Mechanism for All?, Page 1 of 2

| /docserver/preview/fulltext/10.1128/9781683670285/9781683670278_Chap18-1.gif /docserver/preview/fulltext/10.1128/9781683670285/9781683670278_Chap18-2.gif


Gram-negative bacteria are equipped with at least seven dedicated secretion systems that mediate the export of proteins beyond the outer membrane ( ). These are called type 1 to 6 and type 9 secretion systems (T1SS to T6SS and T9SS). Among those, T3SS, T4SS, and T6SS are even capable of delivering their cargo directly into the cytosol of the host cell. In this minireview, we place the major emphasis on the hemolysin A (HlyA) secretion system in . This is by far the most studied and illustrates very well the largely conserved, essential features of T1SS. Interestingly, however, an important mechanistic variation in the translocation of some of the unusually extended giant RTX proteins—adhesins—was discovered recently ( ) and is also discussed.

Citation: Spitz O, Erenburg I, Beer T, Kanonenberg K, Holland I, Schmitt L. 2019. Type I Secretion Systems—One Mechanism for All?, p 215-225. In Sandkvist M, Cascales E, Christie P (ed), Protein Secretion in Bacteria. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.PSIB-0003-2018
Highlighted Text: Show | Hide
Loading full text...

Full text loading...


Image of Figure 1
Figure 1

Architecture of substrates of T1SS. The primary structure of a canonical substrate of a T1SS is shown as white cylinder with the N and C termini labeled by “N” and “C,” respectively. The secretion sequence (approximately 50 to 100 amino acids depending on the substrate) at the C terminus is in red, the GG repeats forming the classic RTX domain are in blue (six GG repeats as in the case of HlyA have been chosen as an example), and the functional, N-terminal domain is in brown. However, the number and types of architectures of this functional domain have increased in recent years. HlyA-like proteins contain only one domain with dedicated activity (pore-forming activity in the case of HlyA), while, for example, CyaA-like proteins contain two domains, which possess an adenylate cyclase (light brown) and a pore-forming (brown) activity in the case of CyaA. A third class are MARTX proteins (exemplified here by a MARTX protein from ). The effector domains (yellow and separated by black vertical lines) that are autocatalytically excised after secretion are flanked by an N-terminal RTX-like domain (marked as RTX domain*) and a C-terminal RTX domain. The C-terminal domain corresponds to the canonical sequence, while the conserved aspartate is missing in the N-terminal one. Another architecture is present in LapA-like adhesins (or bacterial transglutaminase-like cysteine proteinases) that contain multiple, different domains. In the case of LapA, two different colors indicate two different domains. However, the number of different domains is not restricted to two. Additionally, the double-alanine motif in the N termini of LapA-like RTX adhesins is not shown. Finally, SiiE-like adhesins contain multiple identical domains, such as the 53 copies of the BIg domain in the case of SiiE ( ). The vertical blue line indicates that the GG repeats are integrated within the Ig-like domains and do not form a separate RTX domain. Please note that the drawing of the functional domains is not to scale.

Citation: Spitz O, Erenburg I, Beer T, Kanonenberg K, Holland I, Schmitt L. 2019. Type I Secretion Systems—One Mechanism for All?, p 215-225. In Sandkvist M, Cascales E, Christie P (ed), Protein Secretion in Bacteria. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.PSIB-0003-2018
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 2
Figure 2

Structure of GG repeats of alkaline protease (PDB entry 1KAP) from in its Ca-bound state, resulting in the classic β-roll motif. The five Ca ions are shown as blue spheres. For simplicity, only the first three GG repeats are shown in ball-and-stick representation. The carbon atoms of GG repeat one are in gray, the carbon atoms of the second GG repeat in green, and the ones of the third repeat in yellow. The interactions of repeat one with the bound Ca ion are indicated by gray dashed lines, and the interaction of the third repeat with the bound Ca ions is in yellow. As it is evident, one Ca ion is coordinated by repeat and repeat + 2. RTX domain of alkaline protease from in cartoon representation. The orientation is identical to that in panel A, and the gray and yellow dashed lines indicate the interactions.

Citation: Spitz O, Erenburg I, Beer T, Kanonenberg K, Holland I, Schmitt L. 2019. Type I Secretion Systems—One Mechanism for All?, p 215-225. In Sandkvist M, Cascales E, Christie P (ed), Protein Secretion in Bacteria. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.PSIB-0003-2018
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 3
Figure 3

Schematic summary of the classic T1SS-mediated substrate secretion and the recently discovered secretion mechanism for some RTX adhesins in which secretion stalls just before completion, creating a so-called two-step process with a pseudoperiplasmic intermediate . The ABC transporter and the MFP are shown in blue and green, respectively, and the OM protein is in maroon. The unfolded substrate is secreted with its C terminus first. At the cell surface, Ca ions (blue spheres) bind to the GG repeats and induce folding, which results in formation of the β-roll (indicated in cartoon representation). In the case of adhesins such as IBA or LapA, the N-terminal domain starts folding prior to or during secretion, which plugs the translocon (indicated by the light brown polygon) and tethers the entire substrate at the cell surface within the OM component of the translocon of the T1SS. The brown cubes and distorted ellipse represent folded domains of the substrate. This scheme clearly demonstrates that the classic T1SS disassembles only after the entire substrate is translocated, while in two-step T1SS disassembly earlier, e.g., when the N-terminal plug domain has not passed the OM. For further details, see the text. IM, inner membrane; NBD, nucleotide binding domain; TMD, transmembrane domain.

Citation: Spitz O, Erenburg I, Beer T, Kanonenberg K, Holland I, Schmitt L. 2019. Type I Secretion Systems—One Mechanism for All?, p 215-225. In Sandkvist M, Cascales E, Christie P (ed), Protein Secretion in Bacteria. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.PSIB-0003-2018
Permissions and Reprints Request Permissions
Download as Powerpoint


1. 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.[CrossRef][PubMed]
2. Veith PD,, Glew MD,, Gorasia DG,, Reynolds EC . 2017. Type IX secretion: the generation of bacterial cell surface coatings involved in virulence, gliding motility and the degradation of complex biopolymers. Mol Microbiol 106 : 35 53.[CrossRef][PubMed]
3. Smith TJ,, Font ME,, Kelly CM,, Sondermann H,, O’Toole GA . 2018. An N-terminal retention module anchors the giant adhesin LapA of Pseudomonas fluorescens at the cell surface: a novel sub-family of type I secretion systems. J Bacteriol 200 : e00734-17.[CrossRef][PubMed]
4. Linhartová I,, Bumba L,, Mašín J,, Basler M,, Osička R,, Kamanová J,, Procházková K,, Adkins I,, Hejnová-Holubová J,, Sadílková L,, Morová J,, Sebo P . 2010. RTX proteins: a highly diverse family secreted by a common mechanism. FEMS Microbiol Rev 34 : 1076 1112.[CrossRef][PubMed]
5. Felmlee T,, Welch RA . 1988. Alterations of amino acid repeats in the Escherichia coli hemolysin affect cytolytic activity and secretion. Proc Natl Acad Sci U S A 85 : 5269 5273.[CrossRef][PubMed]
6. Griessl MH,, Schmid B,, Kassler K,, Braunsmann C,, Ritter R,, Barlag B,, Stierhof YD,, Sturm KU,, Danzer C,, Wagner C,, Schäffer TE,, Sticht H,, Hensel M,, Muller YA . 2013. Structural insight into the giant Ca 2+-binding adhesin SiiE: implications for the adhesion of Salmonella enterica to polarized epithelial cells. Structure 21 : 741 752.[CrossRef][PubMed]
7. Håvarstein LS,, Diep DB,, Nes IF . 1995. A family of bacteriocin ABC transporters carry out proteolytic processing of their substrates concomitant with export. Mol Microbiol 16 : 229 240.[CrossRef][PubMed]
8. Håvarstein LS,, Holo H,, Nes IF . 1994. The leader peptide of colicin V shares consensus sequences with leader peptides that are common among peptide bacteriocins produced by gram-positive bacteria. Microbiology 140 : 2383 2389.[CrossRef][PubMed]
9. Michiels J,, Dirix G,, Vanderleyden J,, Xi C . 2001. Processing and export of peptide pheromones and bacteriocins in Gram-negative bacteria. Trends Microbiol 9 : 164 168.[CrossRef]
10. Choudhury HG,, Tong Z,, Mathavan I,, Li Y,, Iwata S,, Zirah S,, Rebuffat S,, van Veen HW,, Beis K . 2014. Structure of an antibacterial peptide ATP-binding cassette transporter in a novel outward occluded state. Proc Natl Acad Sci U S A 111 : 9145 9150.[CrossRef][PubMed]
11. Husada F,, Bountra K,, Tassis K,, de Boer M,, Romano M,, Rebuffat S,, Beis K,, Cordes T . 2018. Conformational dynamics of the ABC transporter McjD seen by single-molecule FRET. EMBO J 37 : e100056.[CrossRef][PubMed]
12. Felmlee T,, Pellett S,, Welch RA . 1985. Nucleotide sequence of an Escherichia coli chromosomal hemolysin. J Bacteriol 163 : 94 105.[PubMed]
13. Härtlein M,, Schiessl S,, Wagner W,, Rdest U,, Kreft J,, Goebel W . 1983. Transport of hemolysin by Escherichia coli. J Cell Biochem 22 : 87 97.[CrossRef][PubMed]
14. Noegel A,, Rdest U,, Springer W,, Goebel W . 1979. Plasmid cistrons controlling synthesis and excretion of the exotoxin alpha-haemolysin of Escherichia coli. Mol Gen Genet 175 : 343 350.[CrossRef][PubMed]
15. Springer W,, Goebel W . 1980. Synthesis and secretion of hemolysin by Escherichia coli. J Bacteriol 144 : 53 59.[PubMed]
16. Nicaud JM,, Mackman N,, Gray L,, Holland IB . 1985. Characterisation of HlyC and mechanism of activation and secretion of haemolysin from E. coli 2001. FEBS Lett 187 : 339 344.[CrossRef]
17. Stanley P,, Hyland C,, Koronakis V,, Hughes C . 1999. An ordered reaction mechanism for bacterial toxin acylation by the specialized acyltransferase HlyC: formation of a ternary complex with acylACP and protoxin substrates. Mol Microbiol 34 : 887 901.[CrossRef][PubMed]
18. Stanley P,, Packman LC,, Koronakis V,, Hughes C . 1994. Fatty acylation of two internal lysine residues required for the toxic activity of Escherichia coli hemolysin. Science 266 : 1992 1996.[CrossRef][PubMed]
19. Trent MS,, Worsham LM,, Ernst-Fonberg ML . 1998. The biochemistry of hemolysin toxin activation: characterization of HlyC, an internal protein acyltransferase. Biochemistry 37 : 4644 4652.[CrossRef][PubMed]
20. Issartel JP,, Koronakis V,, Hughes C . 1991. Activation of Escherichia coli prohaemolysin to the mature toxin by acyl carrier protein-dependent fatty acylation. Nature 351 : 759 761.[CrossRef][PubMed]
21. Greene NP,, Crow A,, Hughes C,, Koronakis V . 2015. Structure of a bacterial toxin-activating acyltransferase. Proc Natl Acad Sci U S A 112 : E3058 E3066.[CrossRef][PubMed]
22. Wandersman C,, Delepelaire P . 1990. TolC, an Escherichia coli outer membrane protein required for hemolysin secretion. Proc Natl Acad Sci U S A 87 : 4776 4780.[CrossRef][PubMed]
23. Chervaux C,, Sauvonnet N,, Le Clainche A,, Kenny B,, Hung AL,, Broome-Smith JK,, Holland IB . 1995. Secretion of active beta-lactamase to the medium mediated by the Escherichia coli haemolysin transport pathway. Mol Gen Genet 249 : 237 245.[CrossRef][PubMed]
24. Gentschev I,, Hess J,, Goebel W . 1990. Change in the cellular localization of alkaline phosphatase by alteration of its carboxy-terminal sequence. Mol Gen Genet 222 : 211 216.[CrossRef][PubMed]
25. Gray L,, Baker K,, Kenny B,, Mackman N,, Haigh R,, Holland IB . 1989. A novel C-terminal signal sequence targets Escherichia coli haemolysin directly to the medium. J Cell Sci Suppl 11 : 45 57.[CrossRef][PubMed]
26. Gray L,, Mackman N,, Nicaud JM,, Holland IB . 1986. The carboxy-terminal region of haemolysin 2001 is required for secretion of the toxin from Escherichia coli. Mol Gen Genet 205 : 127 133.[CrossRef][PubMed]
27. Koronakis V,, Koronakis E,, Hughes C . 1989. Isolation and analysis of the C-terminal signal directing export of Escherichia coli hemolysin protein across both bacterial membranes. EMBO J 8 : 595 605.[CrossRef][PubMed]
28. Mackman N,, Baker K,, Gray L,, Haigh R,, Nicaud JM,, Holland IB . 1987. Release of a chimeric protein into the medium from Escherichia coli using the C-terminal secretion signal of haemolysin. EMBO J 6 : 2835 2841.[CrossRef][PubMed]
29. 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 : 129 134.[CrossRef][PubMed]
30. Mackman N,, Nicaud JM,, Gray L,, Holland IB . 1985. Genetical and functional organisation of the Escherichia coli haemolysin determinant 2001. Mol Gen Genet 201 : 282 288.[CrossRef][PubMed]
31. Mackman N,, Nicaud JM,, Gray L,, Holland IB . 1985. Identification of polypeptides required for the export of haemolysin 2001 from E. coli. Mol Gen Genet 201 : 529 536.[CrossRef][PubMed]
32. Goyard S,, Sebo P,, D’Andria O,, Ladant D,, Ullmann A . 1993. Bordetella pertussis adenylate cyclase: a toxin with multiple talents. Zentralbl Bakteriol 278 : 326 333.[CrossRef]
33. Satchell KJ . 2011. Structure and function of MARTX toxins and other large repetitive RTX proteins. Annu Rev Microbiol 65 : 71 90.[CrossRef][PubMed]
34. Satchell KJF . 2015. Multifunctional-autoprocessing repeats-in-toxin (MARTX) toxins of vibrios. Microbiol Spectr 3( 3) : VE-0002-2014.[CrossRef][PubMed]
35. Kim BS,, Gavin HE,, Satchell KJ . 2015. Distinct roles of the repeat-containing regions and effector domains of the Vibrio vulnificus multifunctional-autoprocessing repeats-in-toxin (MARTX) toxin. mBio 6 : e00324-15.[CrossRef][PubMed]
36. Barlag B,, Hensel M . 2015. The giant adhesin SiiE of Salmonella enterica. Molecules 20 : 1134 1150.[CrossRef][PubMed]
37. Guo S,, Stevens CA,, Vance TDR,, Olijve LLC,, Graham LA,, Campbell RL,, Yazdi SR,, Escobedo C,, Bar-Dolev M,, Yashunsky V,, Braslavsky I,, Langelaan DN,, Smith SP,, Allingham JS,, Voets IK,, Davies PL . 2017. Structure of a 1.5-MDa adhesin that binds its Antarctic bacterium to diatoms and ice. Sci Adv 3 : e1701440.[CrossRef][PubMed]
38. Smith TJ,, Sondermann H,, O’Toole GA . 2018. Type 1 does the two-step: type 1 secretion substrates with a functional periplasmic intermediate. J Bacteriol 200 : e00168-18.[CrossRef][PubMed]
39. Peters B,, Stein J,, Klingl S,, Sander N,, Sandmann A,, Taccardi N,, Sticht H,, Gerlach RG,, Muller YA,, Hensel M . 2017. Structural and functional dissection reveals distinct roles of Ca2+-binding sites in the giant adhesin SiiE of Salmonella enterica. PLoS Pathog 13 : e1006418.[CrossRef][PubMed]
40. Wagner C,, Polke M,, Gerlach RG,, Linke D,, Stierhof YD,, Schwarz H,, Hensel M . 2011. Functional dissection of SiiE, a giant non-fimbrial adhesin of Salmonella enterica. Cell Microbiol 13 : 1286 1301.[CrossRef][PubMed]
41. Holland IB,, Peherstorfer S,, Kanonenberg K,, Lenders M,, Reimann S,, Schmitt L . 2016. Type I protein secretion—deceptively simple yet with a wide range of mechanistic variability across the family. EcoSal Plus 7 : ESP-0019-2015.[CrossRef]
42. Cao G,, Kuhn A,, Dalbey RE . 1995. The translocation of negatively charged residues across the membrane is driven by the electrochemical potential: evidence for an electrophoresis-like membrane transfer mechanism. EMBO J 14 : 866 875.[CrossRef][PubMed]
43. Baumann U,, Wu S,, Flaherty KM,, McKay DB . 1993. Three-dimensional structure of the alkaline protease of Pseudomonas aeruginosa: a two-domain protein with a calcium binding parallel beta roll motif. EMBO J 12 : 3357 3364.[CrossRef][PubMed]
44. Baumann U,, Bauer M,, Létoffé S,, Delepelaire P,, Wandersman C . 1995. Crystal structure of a complex between Serratia marcescens metallo-protease and an inhibitor from Erwinia chrysanthemi. J Mol Biol 248 : 653 661.[CrossRef][PubMed]
45. Meier R,, Drepper T,, Svensson V,, Jaeger KE,, Baumann U . 2007. A calcium-gated lid and a large beta-roll sandwich are revealed by the crystal structure of extracellular lipase from Serratia marcescens. J Biol Chem 282 : 31477 31483.[CrossRef][PubMed]
46. Ostolaza H,, Soloaga A,, Goñi FM . 1995. The binding of divalent cations to Escherichia coli alpha-haemolysin. Eur J Biochem 228 : 39 44.
47. Sánchez-Magraner L,, Viguera AR,, García-Pacios M,, Garcillán MP,, Arrondo JL,, de la Cruz F,, Goñi FM,, Ostolaza H . 2007. The calcium-binding C-terminal domain of Escherichia coli alpha-hemolysin is a major determinant in the surface-active properties of the protein. J Biol Chem 282 : 11827 11835.[CrossRef][PubMed]
48. Soloaga A,, Ramírez JM,, Goñi FM . 1998. Reversible denaturation, self-aggregation, and membrane activity of Escherichia coli alpha-hemolysin, a protein stable in 6 M urea. Biochemistry 37 : 6387 6393.[CrossRef][PubMed]
49. Thomas S,, Bakkes PJ,, Smits SH,, Schmitt L . 2014. Equilibrium folding of pro-HlyA from Escherichia coli reveals a stable calcium ion dependent folding intermediate. Biochim Biophys Acta 1844 : 1500 1510.[CrossRef][PubMed]
50. Blenner MA,, Shur O,, Szilvay GR,, Cropek DM,, Banta S . 2010. Calcium-induced folding of a beta roll motif requires C-terminal entropic stabilization. J Mol Biol 400 : 244 256.[CrossRef][PubMed]
51. Chenal A,, Guijarro JI,, Raynal B,, Delepierre M,, Ladant D . 2009. RTX calcium binding motifs are intrinsically disordered in the absence of calcium: implication for protein secretion. J Biol Chem 284 : 1781 1789.[CrossRef][PubMed]
52. Sotomayor Pérez AC,, Karst JC,, Davi M,, Guijarro JI,, Ladant D,, Chenal A . 2010. Characterization of the regions involved in the calcium-induced folding of the intrinsically disordered RTX motifs from the Bordetella pertussis adenylate cyclase toxin. J Mol Biol 397 : 534 549.[CrossRef][PubMed]
53. Zhang L,, Conway JF,, Thibodeau PH . 2012. Calcium-induced folding and stabilization of the Pseudomonas aeruginosa alkaline protease. J Biol Chem 287 : 4311 4322.[CrossRef][PubMed]
54. Jones HE,, Holland IB,, Baker HL,, Campbell AK . 1999. Slow changes in cytosolic free Ca2+ in Escherichia coli highlight two putative influx mechanisms in response to changes in extracellular calcium. Cell Calcium 25 : 265 274.[CrossRef][PubMed]
55. Bakkes PJ,, Jenewein S,, Smits SH,, Holland IB,, Schmitt L . 2010. The rate of folding dictates substrate secretion by the Escherichia coli hemolysin type 1 secretion system. J Biol Chem 285 : 40573 40580.[CrossRef][PubMed]
56. 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 : 501 510.[CrossRef][PubMed]
57. Thanabalu T,, Koronakis E,, Hughes C,, Koronakis V . 1998. Substrate-induced assembly of a contiguous channel for protein export from E. coli: reversible bridging of an inner-membrane translocase to an outer membrane exit pore. EMBO J 17 : 6487 6496.[CrossRef][PubMed]
58. Du D,, Wang Z,, James NR,, Voss JE,, Klimont E,, Ohene-Agyei T,, Venter H,, Chiu W,, Luisi BF . 2014. Structure of the AcrAB-TolC multidrug efflux pump. Nature 509 : 512 515.[CrossRef][PubMed]
59. Benabdelhak H,, Kiontke S,, Horn C,, Ernst R,, Blight MA,, Holland IB,, Schmitt L . 2003. A specific interaction between the NBD of the ABC-transporter HlyB and a C-terminal fragment of its transport substrate haemolysin A. J Mol Biol 327 : 1169 1179.[CrossRef]
60. Lenders MHH,, Weidtkamp-Peters S,, Kleinschrodt D,, Jaeger K-E,, Smits SHJ,, Schmitt L . 2015. Directionality of substrate translocation of the hemolysin A type I secretion system. Sci Rep 5 : 12470.[CrossRef][PubMed]
61. Lenders MH,, Beer T,, Smits SH,, Schmitt L . 2016. In vivo quantification of the secretion rates of the hemolysin A type I secretion system. Sci Rep 6 : 33275.[CrossRef][PubMed]
62. Bumba L,, Masin J,, Macek P,, Wald T,, Motlova L,, Bibova I,, Klimova N,, Bednarova L,, Veverka V,, Kachala M,, Svergun DI,, Barinka C,, Sebo P . 2016. Calcium-driven folding of RTX domain β-rolls ratchets translocation of RTX proteins through type I secretion ducts. Mol Cell 62 : 47 62.[CrossRef][PubMed]
63. Monds RD,, Newell PD,, Gross RH,, O’Toole GA . 2007. Phosphate-dependent modulation of c-di-GMP levels regulates Pseudomonas fluorescens Pf0-1 biofilm formation by controlling secretion of the adhesin LapA. Mol Microbiol 63 : 656 679.[CrossRef][PubMed]
64. 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.[CrossRef][PubMed]
65. 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 : 1778 1787.[CrossRef][PubMed]
66. Zaitseva J,, Jenewein S,, Jumpertz T,, Holland IB,, Schmitt L . 2005. H662 is the linchpin of ATP hydrolysis in the nucleotide-binding domain of the ABC transporter HlyB. EMBO J 24 : 1901 1910.[CrossRef][PubMed]
67. Zaitseva J,, Oswald C,, Jumpertz T,, Jenewein S,, Wiedenmann A,, Holland IB,, Schmitt L . 2006. A structural analysis of asymmetry required for catalytic activity of an ABC-ATPase domain dimer. EMBO J 25 : 3432 3443.[CrossRef][PubMed]
68. Murata D,, Okano H,, Angkawidjaja C,, Akutsu M,, Tanaka SI,, Kitahara K,, Yoshizawa T,, Matsumura H,, Kado Y,, Mizohata E,, Inoue T,, Sano S,, Koga Y,, Kanaya S,, Takano K . 2017. Structural basis for the Serratia marcescens lipase secretion system: crystal structures of the membrane fusion protein and nucleotide-binding domain. Biochemistry 56 : 6281 6291.[CrossRef][PubMed]
69. Kim JS,, Song S,, Lee M,, Lee S,, Lee K,, Ha NC . 2016. Crystal structure of a soluble fragment of the membrane fusion protein HlyD in a type i secretion system of Gram-negative bacteria. Structure 24 : 477 485.[CrossRef][PubMed]
70. Morgan JLW,, Acheson JF,, Zimmer J . 2017. Structure of a type-1 secretion system ABC transporter. Structure 25 : 522 529.[CrossRef][PubMed]
71. Gerlach RG,, Jäckel D,, Stecher B,, Wagner C,, Lupas A,, Hardt WD,, Hensel M . 2007. Salmonella pathogenicity island 4 encodes a giant non-fimbrial adhesin and the cognate type 1 secretion system. Cell Microbiol 9 : 1834 1850.[CrossRef][PubMed]

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