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15 Type III Secretion Systems in Animal- and Plant-Interacting Bacteria

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Abstract:

This chapter discusses the type III secretion system (TTSS) possessed by several gram-negative bacteria that live, for at least part of their life cycle, in close association with eukaryotic cells. The intestinal pathogen provides an illustrative example of the adaptation of type III gene clusters. This pathogen possesses two entirely separate TTSSs, encoded by different gene clusters, which, based on genetic evidence, apparently were acquired at different times during evolution. Secretion and assembly of the external needle only occurs once the bacterial envelope-spanning components, including the outer membrane-associated parts of the needle complex, are assembled. Another feature common to both systems is that protein secretion appears to occur by a continuous process without any detectable periplasmic protein intermediates. The proteins secreted by the TTSS interact with eukaryotic cells in several ways. In most systems studied so far, the effector proteins are translocated across the eukaryotic plasma membrane into the cytoplasm by extracellular bacteria. For and enteropathogenic (EPEC), it is thought that one function of the effector proteins is to either prevent phagocytosis or form a tight adherence between the bacterium and the target cell that induces the formation of so-called pedestal structures. Triggering apoptosis also depends on the TTSS, suggesting that, like apoptosis-inducing proteins of plant-interacting bacteria, YopJ/YopP is recognized, or its activity occurs, inside the eukaryotic cell and that this recognition or activity triggers apoptosis.

Citation: Francis M, Schesser K, Forsberg Å, Wolf-Watz H. 2004. 15 Type III Secretion Systems in Animal- and Plant-Interacting Bacteria, p 361-392. In Cossart P, Boquet P, Normark S, Rappuoli R (ed), Cellular Microbiology, Second Edition. ASM Press, Washington, DC. doi: 10.1128/9781555817633.ch15
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Figures

Image of Figure 15.1
Figure 15.1

Schematic diagram of bacterial type I to V secretion systems. Recognition sequences that target the proteins to the respective secretion complexes are indicated either in light or dark gold (for N-terminal signal sequences of type II and IV and type III systems, respectively) or grey and black (for C-terminal signal sequences of type V and type I systems, respectively). Proteins secreted by the type I and III pathways traverse the inner membrane (IM) and outer membrane (OM) in one step, whereas proteins secreted by the type II and V pathways cross the inner membrane and outer membrane in separate steps. The N-terminal signal sequences of proteins secreted by the type II and V systems are enzymatically removed upon crossing the inner membrane, in contrast to proteins secreted by the type I and III systems, which are exported intact. Although proteins secreted by the type II and V systems are similar in the mechanism by which they cross the inner membrane, differences exist in how they traverse the outer membrane. Proteins secreted by the type II system are transported across the outer membrane by a multiprotein complex, whereas those secreted by the type V system autotransport across the outer membrane by virtue of a C-terminal sequence which is enzymatically removed upon release of the protein from the outer membrane. Type IV pathways secrete either polypeptide toxins (directed against eukaryotic cells) or protein-DNA complexes between either two bacterial cells or a bacterial and eukaryotic cell. Shown in the figure is the protein-DNA complex delivered by into a plant cell that consists of a 20-kb single-stranded DNA molecule and the VirD2 (grey) and VirE2 (gold) proteins.

Citation: Francis M, Schesser K, Forsberg Å, Wolf-Watz H. 2004. 15 Type III Secretion Systems in Animal- and Plant-Interacting Bacteria, p 361-392. In Cossart P, Boquet P, Normark S, Rappuoli R (ed), Cellular Microbiology, Second Edition. ASM Press, Washington, DC. doi: 10.1128/9781555817633.ch15
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Image of Figure 15.2
Figure 15.2

The TTSS of is encoded on the virulence plasmid pIB1. The genes encoding components of the type III secretion system and those involved in plasmid replication () and plasmid partitioning () are depicted in the map as arrows showing the direction of transcription. A nonfunctional, truncated gene has no arrowhead and is indicated by an apostrophe to denote the truncation. Genes in light grey ( to , and ) encode either components of the secretion apparatus or those involved in controlling protein secretion. The genes shown in dark grey ( and ) encode proteins involved in controlling translocation of effectors into target cells. The genes encoding the secreted effector proteins (, and ) are shown in dark gold. The genes encoding the chaperones required for efficient secretion of effector Yops ( and ) are shown in light gold, and important regulatory genes are depicted in soft gold. Note that some proteins may have dual functions. For example, several proteins encoded by the operon are involved in both controlling translocation and regulating the system. Moreover, TyeA is involved in control of Yop secretion but is also required for translocation of the YopE and YopH effector molecules. The DNA sequence of pIB1 on which this map is based is unpublished data provided by Peter Cherepanov and Thomas Svensson, Department of Microbiology, FOI NBC-Defence, Umeå, Sweden.

Citation: Francis M, Schesser K, Forsberg Å, Wolf-Watz H. 2004. 15 Type III Secretion Systems in Animal- and Plant-Interacting Bacteria, p 361-392. In Cossart P, Boquet P, Normark S, Rappuoli R (ed), Cellular Microbiology, Second Edition. ASM Press, Washington, DC. doi: 10.1128/9781555817633.ch15
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Image of Figure 15.3
Figure 15.3

Structural comparison between the enteric bacterial flagellum and the needle complex. Three major components of the flagellum structure are shown: external filamentous structure, basal body, and flagellum-specific secretion apparatus. The structure of the TTSS spanning the bacterial envelope is represented like the basal body, as deduced from genetic, electron microscopic, and scanning electron microscopic studies (see the micrograph inset of a purified flagellum [plate A] and the SPI-1 needle complex [plate B]). Nevertheless, these structures are shown in black to indicate limited sequence similarity among the corresponding protein components. Conversely, some proteins of the needle complex that have extensive similarities to components of the flagellum-specific secretion apparatus, located within the bell-shaped C ring (proteins indicated in parentheses; see Table 15.2 ), are shown in light grey. Plate A is shown with copyright permission from ASM Press, and plate B is reprinted from Kubori et al., 602–605, 1998, with permission of AAAS. OM, outer membrane; P, peptidoglycan; IM, inner membrane.

Citation: Francis M, Schesser K, Forsberg Å, Wolf-Watz H. 2004. 15 Type III Secretion Systems in Animal- and Plant-Interacting Bacteria, p 361-392. In Cossart P, Boquet P, Normark S, Rappuoli R (ed), Cellular Microbiology, Second Edition. ASM Press, Washington, DC. doi: 10.1128/9781555817633.ch15
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Image of Figure 15.11
Figure 15.11

The EspA surface appendage bridges the gap between EPEC and the eukaryotic cell. This scanning electron micrograph captures the EspA filamentous structures (indicated by arrows) that promote attachment between EPEC and an infected red blood cell. The EspA filament is required for the translocation of the Tir effector into eukaryotic cells. Provided by Stuart Knutton, University of Birmingham, Birmingham, United Kingdom.

Citation: Francis M, Schesser K, Forsberg Å, Wolf-Watz H. 2004. 15 Type III Secretion Systems in Animal- and Plant-Interacting Bacteria, p 361-392. In Cossart P, Boquet P, Normark S, Rappuoli R (ed), Cellular Microbiology, Second Edition. ASM Press, Washington, DC. doi: 10.1128/9781555817633.ch15
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Image of Figure 15.4
Figure 15.4

Secretion of effector proteins occurs through the Hrp pilus of the plant pathogen . A strain of was engineered so that Hrp pilus assembly was uncoupled from effector synthesis by placing the effector gene under the control of a heterologous inducible promoter. Shown are electron microscopy images of recombinant grown in Hrp-inducing media with no induction simultaneous induction of AvrPto synthesis and AvrPto synthesis induced long after Hrp pilus assembly Arrows indicate the Hrp pili extending from the bacterial surface. Secreted AvrPto is detected by a specific immunogold labeling technique that is reflected by the appearance of black spots on the micrographs. When was coinduced with Hrp-pili, secreted effector was uniformly localized along the entire structure However, when pili were allowed to assemble prior to induction of AvrPto synthesis, secreted effector was routinely localized at the tip portion of pili This strongly supports a conduit model whereby effectors travel through a hollow pilus and are secreted at the tip. Modified from Figure 2 in Jin et al., 2556–2558, 2001, with permission of AAAS and provided by Sheng-Yang He, Michigan State University, East Lansing.

Citation: Francis M, Schesser K, Forsberg Å, Wolf-Watz H. 2004. 15 Type III Secretion Systems in Animal- and Plant-Interacting Bacteria, p 361-392. In Cossart P, Boquet P, Normark S, Rappuoli R (ed), Cellular Microbiology, Second Edition. ASM Press, Washington, DC. doi: 10.1128/9781555817633.ch15
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Image of Figure 15.5
Figure 15.5

Schematic diagram of the modular organization of effector proteins injected into eukaryotic cells by TTSSs. The YopE and YopH antiphagocytic proteins, SptP from serovar Typhimurium and ExoS from , are given as examples. The minimal N-terminal domain required for secretion of each protein is shown in grey. The secretion signal is immediately followed by a minimal region required for the proteins to be injected into eukaryotic cells (corresponding to “Translocation and chaperone binding”). These translocation domains are also overlapped by high-affinity chaperone-binding sites. The C-terminal region of YopE (amino acids 99 to 215) is essential for the cytotoxic effector function. In particular, this domain functions as a Rho GTPase-activating domain. Both the SptP and ExoS proteins also display a modular organization, having regions with extensive similarity to the cytotoxic domain of YopE. An essential arginine (Arg) finger motif defines this functional domain. SptP possesses a second effector domain with similarity to the PTPase activity domain of YopH. The cysteine (Cys) residue is essential for tyrosine dephosphorylation of host proteins. The second functional domain of ExoS located at the C terminus exhibits ADP-ribosyltransferase activity, which blocks receptor-stimulated Ras activation through a modification of Ras in vivo.

Citation: Francis M, Schesser K, Forsberg Å, Wolf-Watz H. 2004. 15 Type III Secretion Systems in Animal- and Plant-Interacting Bacteria, p 361-392. In Cossart P, Boquet P, Normark S, Rappuoli R (ed), Cellular Microbiology, Second Edition. ASM Press, Washington, DC. doi: 10.1128/9781555817633.ch15
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Image of Figure 15.8
Figure 15.8

A proposed model for interaction with target cells. Intimate association between the pathogen and its target cell is established by a receptor-ligand interaction. In phagocytic cells, the basis of this interaction is not known. In epithelial cells, however, β1-integrins bind to the bacterial surface-located protein, invasin. This target cell contact opens the TTSS, allowing Yop secretion, some of which forms a pore in the target cell plasma membrane, while others are injected through the pore into the target cell. This results in blockage of bacterial uptake and suppression of cytokine expression.

Citation: Francis M, Schesser K, Forsberg Å, Wolf-Watz H. 2004. 15 Type III Secretion Systems in Animal- and Plant-Interacting Bacteria, p 361-392. In Cossart P, Boquet P, Normark S, Rappuoli R (ed), Cellular Microbiology, Second Edition. ASM Press, Washington, DC. doi: 10.1128/9781555817633.ch15
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Image of Figure 15.9
Figure 15.9

A proposed model for invasion and intracellular survival of (arrowheads) within epithelial cells. Upon contact with the eukaryotic epithelial cell (mucosal cells or M cells), injects a number of effector proteins (Sops) into the cytosol of the target cell via the SPI-1-encoded TTSS. The injected effector proteins induce membrane ruffling (arrows) and subsequent uptake of the pathogen into a membrane-bound phagosome. After uptake into phagosomal compartments within eukaryotic cells, activates the SPI-2-encoded TTSS, including the associated effector proteins. Thereafter, the effector proteins are translocated across the phagosomal membrane into the lumen of the target cell. These effectors apparently inhibit a variety of functions such as phagosome-lysosome fusion (SpiC), vesicular trafficking, and avoidance of killing by the respiratory burst. Thus, the SPI-2-encoded TTSS supports the intracellular survival and proliferation of . Panel A was provided by Jorge Galán, Yale University School of Medicine, New Haven, Conn.

Citation: Francis M, Schesser K, Forsberg Å, Wolf-Watz H. 2004. 15 Type III Secretion Systems in Animal- and Plant-Interacting Bacteria, p 361-392. In Cossart P, Boquet P, Normark S, Rappuoli R (ed), Cellular Microbiology, Second Edition. ASM Press, Washington, DC. doi: 10.1128/9781555817633.ch15
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Image of Figure 15.10
Figure 15.10

The proposed stages in the generation of tight adherence between EPEC and its target cell. After initial interaction between EPEC and the eukaryotic cell has been established (independent of the TTSS), a type III-dependent EspA organelle that extends from the needle complex bridges the small gap between the pathogen and the eukaryotic cell surface (see Figure 15.11 ). This facilitates the secretion of EspB and EspD, which subsequently form a translocation pore in the target cell plasma membrane through which the Tir protein is translocated. Tir then integrates into the host cell plasma membrane. Tight association between EPEC and the eukaryotic cell is then established via the interaction between the bacterial outer membrane protein intimin and Tir, which in this case works as a bacterially induced “eukaryotic cell receptor.” Concomitantly, pedestal-like structures are formed as a consequence of dramatic actin rearrangements within the host cell. EPEC bacteria reside at the top of these pedestal structures. During this process the ability to visualize EspA is lost.

Citation: Francis M, Schesser K, Forsberg Å, Wolf-Watz H. 2004. 15 Type III Secretion Systems in Animal- and Plant-Interacting Bacteria, p 361-392. In Cossart P, Boquet P, Normark S, Rappuoli R (ed), Cellular Microbiology, Second Edition. ASM Press, Washington, DC. doi: 10.1128/9781555817633.ch15
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References

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24. Stebbins, C. E.,, and J. E. Galán. 2000. Modulation of host signaling by a bacterial mimic: structure of the Salmonella effector SptP bound to Rac1. Mol. Cell 6:14491460. Several bacterial proteins secreted by type III secretion systems possess domains common to eukaryotic proteins. Presented herein are X-ray crystal structures of the Salmonella effector SptP, a GAP toward the Rho family of small G proteins, complexed with a molecular target, Rac1. They provide a high-resolution glimpse at the efficiency of bacterial pathogens to evolve molecular mimics to components of host cell signal transduction cascades.
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28. Van den Ackerveken, G.,, E. Marois,, and U. Bonas. 1996. Recognition of the bacterial avirulence protein AvrBs3 occurs inside the host plant cell. Cell 87:13071316. This paper documented the finding that the product of the plant gene Bs3 specifically recognized the avirulence protein AvrBs3 from a bacterial plant pathogen, when transiently produced inside the plant cell, to elicit hypersensitive cell death. This work, coupled with observations that intact hrp (hypersensitive reaction and pathogenicity) genes are essential for recognition of the bacterium by a plant cell, led these authors to introduce the notion that plant pathogens utilize a type III secretion system composed of products of the hrp genes to directly translocate bacterial Avr proteins into plant cells.
29. Wattiau, P.,, and G. R. Cornelis. 1993. SycE, a chaperone-like protein of Yersinia enterocolitica involved in the secretion of YopE. Mol. Microbiol. 8:123131. This breakthrough report introduced the concept that specific accessory proteins (chaperones) are required for presecretory stability and/or targeting of one, or at most a few, cognate substrates to the type III secretion machinery. In this study, the SycE chaperone was shown to specifically bind to the YopE cytotoxin and promote its type III-dependent secretion in the model bacterium Y. enterocolitica. The presence of dedicated chaperones is now accepted as a defining feature of type III secretion systems.

Tables

Generic image for table
Table 1

Type III secretion systems of prominent animal- and plant-interacting bacteria

Citation: Francis M, Schesser K, Forsberg Å, Wolf-Watz H. 2004. 15 Type III Secretion Systems in Animal- and Plant-Interacting Bacteria, p 361-392. In Cossart P, Boquet P, Normark S, Rappuoli R (ed), Cellular Microbiology, Second Edition. ASM Press, Washington, DC. doi: 10.1128/9781555817633.ch15
Generic image for table
Table 15.2

Proteins common to the flagellum-specific secretion apparatus and the type III secreton

Citation: Francis M, Schesser K, Forsberg Å, Wolf-Watz H. 2004. 15 Type III Secretion Systems in Animal- and Plant-Interacting Bacteria, p 361-392. In Cossart P, Boquet P, Normark S, Rappuoli R (ed), Cellular Microbiology, Second Edition. ASM Press, Washington, DC. doi: 10.1128/9781555817633.ch15

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