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

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Abstract:

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
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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
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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
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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
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