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EcoSal Plus

Domain 4:

Synthesis and Processing of Macromolecules

The Type VI Secretion System in and Related Species

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  • Authors: Laure Journet1, and Eric Cascales2
  • Editors: Susan T. Lovett3, Harris D. Bernstein4
  • VIEW AFFILIATIONS HIDE AFFILIATIONS
    Affiliations: 1: Laboratoire d’Ingénierie des Systèmes Macromoléculaires (LISM), Institut de Microbiologie de la Méditerranée (IMM), Centre National de la Recherche Scientifique (CNRS) – Aix-Marseille Université, UMR 7255, 13402 Marseille Cedex 20, France; 2: Laboratoire d’Ingénierie des Systèmes Macromoléculaires (LISM), Institut de Microbiologie de la Méditerranée (IMM), Centre National de la Recherche Scientifique (CNRS) – Aix-Marseille Université, UMR 7255, 13402 Marseille Cedex 20, France; 3: Brandeis University, Waltham, MA; 4: National Institutes of Health, Bethesda, MD
  • Received 20 August 2015 Accepted 16 November 2015 Published 01 February 2016
  • Address correspondence to Eric Cascales cascales@imm.cnrs.fr
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  • Abstract:

    The type VI secretion system (T6SS) is a multiprotein complex widespread in and dedicated to the delivery of toxins into both prokaryotic and eukaryotic cells. It thus participates in interbacterial competition as well as pathogenesis. The T6SS is a contractile weapon, related to the injection apparatus of contractile tailed bacteriophages. Basically, it assembles an inner tube wrapped by a sheath-like structure and anchored to the cell envelope via a membrane complex. The energy released by the contraction of the sheath propels the inner tube through the membrane channel and toward the target cell. Although the assembly and the mechanism of action are conserved across species, the repertoire of secreted toxins and the diversity of the regulatory mechanisms and of target cells make the T6SS a highly versatile secretion system. The T6SS is particularly represented in pathotypes and serotypes. In this review we summarize the current knowledge regarding the prevalence, the assembly, the regulation, and the roles of the T6SS in , , and related species.

  • Citation: Journet L, Cascales E. 2016. The Type VI Secretion System in and Related Species, EcoSal Plus 2016; doi:10.1128/ecosalplus.ESP-0009-2015

Key Concept Ranking

Type VI Secretion System
0.43669933
Type IVB Secretion System
0.43273297
0.43669933

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/content/journal/ecosalplus/10.1128/ecosalplus.ESP-0009-2015
2016-02-01
2017-08-21

Abstract:

The type VI secretion system (T6SS) is a multiprotein complex widespread in and dedicated to the delivery of toxins into both prokaryotic and eukaryotic cells. It thus participates in interbacterial competition as well as pathogenesis. The T6SS is a contractile weapon, related to the injection apparatus of contractile tailed bacteriophages. Basically, it assembles an inner tube wrapped by a sheath-like structure and anchored to the cell envelope via a membrane complex. The energy released by the contraction of the sheath propels the inner tube through the membrane channel and toward the target cell. Although the assembly and the mechanism of action are conserved across species, the repertoire of secreted toxins and the diversity of the regulatory mechanisms and of target cells make the T6SS a highly versatile secretion system. The T6SS is particularly represented in pathotypes and serotypes. In this review we summarize the current knowledge regarding the prevalence, the assembly, the regulation, and the roles of the T6SS in , , and related species.

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Figures

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Figure 1

(A) Schematic representation of the T6SS core genes. Genes are specified by a letter corresponding to the Tss nomenclature (“A” corresponding to “TssA”) or by their vernacular, usual names (Hcp, VgrG, PAAR, and ClpV). The color code is shared with panels B and C. (B) Architecture of the T6SS. The membrane complex, composed of the TssJ lipoprotein (orange) and the TssM (blue) and TssL (red) inner membrane proteins, is indicated (OM, outer membrane; PG, cell wall; IM, inner membrane). The different regions of the tail (spike, tube, sheath, and baseplate) are shown. (C) Architecture of a contractile tailed bacteriophage. Components that are shared with the T6SS (spike, tube, sheath, and baseplate) are depicted with the same color code (LTF, long tail fibers).

Citation: Journet L, Cascales E. 2016. The Type VI Secretion System in and Related Species, EcoSal Plus 2016; doi:10.1128/ecosalplus.ESP-0009-2015
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Figure 2

Time-lapse fluorescence microscopy recordings of green fluorescent protein-labeled EAEC T6SS cells (green) in the presence of mCherry-labeled T6SS prey bacterial cells (red) in T6SS-3 inducing conditions (one image every 7.5 min). Prey cells that are killed and not present in the next frame are indicated by white arrows. Scale bar is 5 μm.

Citation: Journet L, Cascales E. 2016. The Type VI Secretion System in and Related Species, EcoSal Plus 2016; doi:10.1128/ecosalplus.ESP-0009-2015
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Figure 3

The biogenesis of the T6SS starts with the assembly of the TssJLM membrane complex (MC) and recruitment of the baseplate complex (BC) (A), which serves as a platform for polymerization of the tail tube/sheath structure (B, C). During elongation of the tail structure, effectors (red balls) can be loaded inside the inner tube lumen or attached to the VgrG spike. Following contact with a prey cell, the sheath contracts and propels the inner tube/spike toward the target, allowing penetration and delivery of the effectors (D). Once contracted, the ClpV AAA+ ATPase is recruited to the apparatus for recycling sheath subunits (E, F). The MC (and BC ?) might be reused for a new round of assembly.

Citation: Journet L, Cascales E. 2016. The Type VI Secretion System in and Related Species, EcoSal Plus 2016; doi:10.1128/ecosalplus.ESP-0009-2015
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Figure 4

T6SS gene clusters catagorize in 5 phylogenetic groups (A to E) ( 1 , 2 ). The distribution of the -associated T6SSs (T6SS-1 to 3, red) and -associated SPI T6SSs (green) is shown, as well as that of and (blue) and the model T6SSs from , , , and (black). The figure has been prepared with phylogeny.fr using the sequences of the TssF core component homologues (similar results were obtained with TssB homologues) ( 115 ).

Citation: Journet L, Cascales E. 2016. The Type VI Secretion System in and Related Species, EcoSal Plus 2016; doi:10.1128/ecosalplus.ESP-0009-2015
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Figure 5

Genes encoding the T6SS-1 (A), T6SS-2 (B), and T6SS-3 (C) in the indicated strains are shown schematically. Homologous genes are colored similarly (see box below). When predictable, putative phospholipase effector/immunity pairs (Tle1/Tli1, Tle3/Tli3, or Tle4/Tli4) or genes are indicated. Open reading frames with unknown function are shown in white. Genes into brackets are not present or not identical in all the strains listed. Genes were identified using the SecReT6 database ( 116 ).

Citation: Journet L, Cascales E. 2016. The Type VI Secretion System in and Related Species, EcoSal Plus 2016; doi:10.1128/ecosalplus.ESP-0009-2015
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Figure 6

Genes encoding the T6SS in the indicated strains are shown schematically. Homologous genes are colored similarly (see box in Fig. 5 ). When predictable, genes are indicated. The and open reading frames shown to undergo rearrangements ( 94 ) are indicated in the serotype Typhimurium SPI-6 gene cluster, as well as the Tae4/Tai4 effector/immunity pairs in serotype Typhimurium SPI-6 and . Open reading frames with unknown function are shown in white. Genes were identified using the SecReT6 database ( 116 ). Note that the transcription of the gene, interrupted by an early stop codon, is rescued by frameshifting ( 114 ).

Citation: Journet L, Cascales E. 2016. The Type VI Secretion System in and Related Species, EcoSal Plus 2016; doi:10.1128/ecosalplus.ESP-0009-2015
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Figure 7

(A) The , , and genes that encode the components of the membrane complex. (B) Schematic representation of the TssJ, -L, and -M proteins: TssJ is an outer membrane (OM)-tethered lipoprotein, whereas TssL and TssM are inner membrane (IM)-embedded proteins. In T6SS-1, the membrane complex comprises an additional protein, TagL, which binds to the peptidoglycan (PG) layer (not depicted here) ( 27 ). (C) Crystal structure of the complex between the soluble fragment of TssJ (orange) and the two C-terminal domains of the TssM periplasmic segment (light and dark blue) including the C-terminal helix that inserts into the outer membrane (in purple) from EAEC T6SS-1 (Protein Data Bank [PDB]: 4Y7O) (Reprinted from reference 26 with permission). (D) Crystal structure of the cytoplasmic domain of TssL from EAEC T6SS-1 (PDB: 3U66) ( 33 ). (E) Negative stain electron microcopy structure reconstruction of the EAEC TssJLM complex (lower panel, EMDB: 2927) (adapted from reference 26 with permission) (scale bar is 50 nm). The position of the outer (OM) and inner (IM) membranes are predicted based on the presence of detergent micelle and the putative location of the transmembrane segments of TssM, respectively. In the upper panel is shown a top view of the TssJLM complex in which crystal structures of the TssJ-M complex (panel C) are docked, highlighting the presence of two concentric layers closing the channel at the outer membrane.

Citation: Journet L, Cascales E. 2016. The Type VI Secretion System in and Related Species, EcoSal Plus 2016; doi:10.1128/ecosalplus.ESP-0009-2015
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Figure 8

(A) The , , , , , , , , , and genes that encode the components of the tail complex (blue, sheath subunits; black, inner tube subunit; green, spike subunits; pink, baseplate subunits). (B) Schematic representation of the T6SS tail complex (same color code as panel A). (C) Structural model of EAEC T6SS-1 TssE based on the bacteriophage gp25 crystal structure (PDB: 4HRZ). (D) Composite structure made with the crystal structures (from bottom to top) of the UPEC CTF073 VgrG1 protein (PDB: 2P57) ( 39 ), the O157 EDL933 VgrG β-helical prism (PDB: 3WIT) ( 40 ) and the O6 PAAR protein (PDB: 4JIW) ( 41 ). (E) Crystal structure of the EAEC T6SS-1 Hcp hexamer (left, top view; right, side view) (PDB: 4HKH) ( 42 ). (F) Cryoelectron micrograph of a contracted T6SS sheath from (left panel, scale bar is 100 nm) and atomic-resolution cryoelectron structure of the TssB-C complex (PDB: 3J9G) (adapted from reference 47 with permission).

Citation: Journet L, Cascales E. 2016. The Type VI Secretion System in and Related Species, EcoSal Plus 2016; doi:10.1128/ecosalplus.ESP-0009-2015
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Figure 9

Time-lapse fluorescence microscopy recordings of EAEC producing fluorescently labeled sheath subunits (TssB-sfGFP) in the presence of mCherry-labeled T6SS K-12 prey cells (one image every 7.5 min). The time lapse highlights the assembly and the contraction (white arrow) of the T6SS sheath, followed by the lysis of the target cell. Scale bar is 1 μm. Adapted from reference 22 with permission.

Citation: Journet L, Cascales E. 2016. The Type VI Secretion System in and Related Species, EcoSal Plus 2016; doi:10.1128/ecosalplus.ESP-0009-2015
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Figure 10

(A) Schematic representation of the promoter organization of the EAEC T6SS-1 gene cluster. The location of the −10 and −35 transcriptional elements (blue), of the Fur-binding sequences (red) and of one of the GATC sites (green) are shown. (B) Regulatory mechanism of the EAEC T6SS-1 gene cluster ( 23 ). In iron-replete conditions, a Fur dimer (red balls) represses the expression of the T6SS-1 gene cluster by binding to the Fur box, which overlaps with the −10 element (OFF). When iron is limiting, the −10 element is available for the RNA polymerase allowing expression of the T6SS-1 genes (ON). Upon replication, the GATC site is methylated (CH) and by preventing Fur binding allows Fur-independent, constitutive expression of the T6SS-1 gene cluster.

Citation: Journet L, Cascales E. 2016. The Type VI Secretion System in and Related Species, EcoSal Plus 2016; doi:10.1128/ecosalplus.ESP-0009-2015
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Tables

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Table 1

Phenotypes and effectors associated with T6SS in , , and related species

Citation: Journet L, Cascales E. 2016. The Type VI Secretion System in and Related Species, EcoSal Plus 2016; doi:10.1128/ecosalplus.ESP-0009-2015

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