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Advances in the Assembly Model of Bacterial Type IVB Secretion Systems

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Advances in the Assembly Model of Bacterial Type IVB Secretion Systems applied sciences Review Advances in the Assembly Model of Bacterial Type IVB Secretion Systems Shan Wang, Dan Wang, Dan Du, Shanshan Li * and Wei Yan Department of Environmental Science and Engineering, Xi’an Jiaotong University, Xi’an 710049, China; [email protected] (S.W.); [email protected] (D.W.); [email protected] (D.D.); [email protected] (W.Y.) * Correspondence: [email protected]; Tel.: +86-29-8266-8572 Received: 22 September 2018; Accepted: 20 November 2018; Published: 23 November 2018 Abstract: Bacterial type IV secretion systems (T4SSs) are related to not only secretion of effector proteins and virulence factors, but also to bacterial conjugation systems that promote bacterial horizontal gene transfer. The subgroup T4BSS, with a unique mosaic architecture system, consists of nearly 30 proteins that are similar to those from other secretory systems. Despite being intensively studied, the secretion mechanism of T4BSS remains unclear. This review systematically summarizes the protein composition, coding gene set, core complex, and protein interactions of T4BSS. The interactions of proteins in the core complex of the system and the operation mechanism between each element needs to be further studied. Keywords: T4BSS; core complex; mosaic architecture 1. Introduction When bacterial growth is stimulated by the external environment, some effective factors are often secreted to enhance its viability. These effectors are usually secreted into host cells or the surrounding environment using unique recognition and transmission mechanisms through a protein secretion system (a system in which the bacteria depend on a secretory pathway for transcellular membrane transport of proteins) [1]. The protein secretion systems discovered so far can be divided into nine types according to the secretion mechanism of the outer membrane (OM), namely, type I to type IX secretion systems (T1SS to T9SS). Early results indicate that the first six secretory systems are prevalent in Gram-negative bacteria and T7SS was only found in Gram-positive bacteria, although the presence of T4SS in Gram-positive bacteria was also recently reported [2]. Many reports are found in the literature on T1SS to T6SS and T8SS, whereas T7SS and T9SS are newly discovered protein secretion systems whose assembly and secretion mechanisms are still unclear. Unlike other Gram-negative bacterial secretion systems, T4SSs typically transport macromolecular substances such as nucleoprotein particles and deoxyribonucleic acid (DNA). At the same time, it can also mediate the horizontal transfer of DNA via conjugation, thereby promoting the plasticity of the bacterial genome and the transmission of resistance genes and other virulence genes [3–6]. T4SSs can be divided into different types according to different classification standards (Table1) [7–9]. Based on biochemical composition and structural characteristics, it can be divided into T4ASS (typically represented by VirB/D4 systems in Agrobacterium tumefaciens), T4BSS (typically represented as Dot/Icm systems in Legionella pneumophila), T4CSS (typically represented as GI-type T4SS-like system in Gram-positive strain Streptococcus suis)[2], and genomic island (GI) T4SS (typically represented as ICE Hin1056 in Haemophilus influenza)[10]. The most prevalent and best studied are T4ASS and T4BSS. T4ASS is comprised of proteins encoded by 12 genes, whereas T4BSS is more complex, being comprised of ~30 different proteins. Unlike T4ASS, the constituent proteins of T4BSS contain components Appl. Sci. 2018, 8, 2368; doi:10.3390/app8122368 www.mdpi.com/journal/applsci Appl. Sci. 2018, 8, 2368 2 of 13 homologous to other secretory systems (T2SS, T3SS, T4ASS, and T6SS), highlighting the special mosaic structure of T4BSS [11]. Appl. Sci. 2018, 8, x FOR PEER REVIEW 2 of 13 Table 1. Classification of T4SS. of BasisT4BSS of Classificationcontain components Subtype homologous to other secretory Example systems (T2SS, T3SS, Characteristics T4ASS, and T6SS), highlighting the special mosaic structure of T4BSS [11]. Narrow range of secretory substrates, F-subtype IncF, IncH, IncT, IncJ mainly including ssDNA. Plasmid incompatibility Table 1. Classification of T4SS. Wide range of secretory substrates, P-subtype IncP, IncN, IncW including multiple virulence effectors. Basis of Classification Subtype Example Characteristics Aid in both in liquid and solid-surface I-subtype IncI1 plasmid R64 Narrow range of secretory substrates, F-subtype IncF, IncH, IncT, IncJ mating and secrete virulence effectors. mainly including ssDNA. Plasmid Self-transmissible plasmids orWide rangeMostly of secretory present in substrates, bacteria and P-subtypeConjugal transfer IncP, IncN, IncW incompatibility transposons including multiple archaea.virulence effectors. Aid inTransport both in liqui ford virulence and solid-surface effectors in Functional classification EffectorI-subtype translocators IncI1 Pertussis plasmid toxin R64 secretion mating andGram-negative secrete virulence bacteria. effectors. Self-transmissibleComB (Helicobacter plasmids pylori or ) ConjugalDNA release/uptaketransfer Mostly present in bacteria and archaea. systemtransposons takes DNA from Similar to T2SS. systems Functional outside the cell Transport for virulence effectors in Gram- Effector translocators Pertussis toxin secretion classification negativeContains bacteria. pili, which assist in protein T4ASS VirB/D4 (A. tumefaciens) DNA release/uptake ComB (Helicobacter pylori) system secretion. Similar to T2SS. systems takes DNA from outside the cell Secretes a large number of effectors Dot/Icm (Legionella T4BSS Containsand pili, transfers which nucleic assist in acids protein to host Biochemical properties T4ASS VirB/D4 (A.pneumophila tumefaciens)) and structure secretion. cells. Secretes a large number of effectors and Biochemical properties T4BSS Dot/Icm GI-type(Legionella T4SS-like pneumophila system) Common in Gram-positive bacteria of T4CSS transfers nucleic acids to host cells. and structure (Streptococcus suis) the genus Streptococcus GI-type T4SS-like system Common in Gram-positive bacteria of the T4CSS ICE Hin1056 (Haemophilus GI-type T4SS (Streptococcus suis) genus Streptococcus influenza) GI-type T4SS ICE Hin1056 (Haemophilus influenza) 2.2. GeneGene CompositionComposition ofof T4BSST4BSS AA typicaltypical T4BSST4BSS consistsconsists of proteinsproteins encoded by ~30 genes, genes, which which are are named named dotdot (defect(defect in in organelleorganelle trafficking)trafficking) oror icmicm (intracellular(intracellular multiplication), as as shown shown in in Figure Figure 1.1. The The coding coding genes genes for for thethe Dot/Icm Dot/Icm system are mostly mostly found found in in plasmi plasmidsds except except the the genes genes for for T4BSS T4BSS in in the the genera genera LegionellaLegionella, , CoxiellaCoxiellaand andRickettsiella Rickettsiella areare inin thethe chromosomechromosome[11] [11].. The The similarity similarity of of sequen sequencece of of the the genes genes suggests suggests thatthat these these genes genes may may have have originated originated from from a a common common ancestor ancestor (for (for instance instance between between the the tra tra system system in R64in R64 and and Dot/Icm Dot/Icm system) system) [12 [12].]. The The genes genes encoding encoding thethe T4BSST4BSS proteins tend tend to to form form different different gene gene clusters:clusters: (a)(a) thethe dotDdotD--dotCdotC--dotBdotB genegene cluster;cluster; (b)(b) thethe dotMdotM//icmPicmP--dotLdotL//icmOicmO genegene cluster; cluster; and and (c) (c) the the dotIdotI//icmL--dotHdotH//icmKicmK–dotG–dotG/icmE/icmE genegene cluster cluster [11]. [11 ].Compared Compared with with other other T4SSs T4SSs (Figure (Figure 2b)2b) [1,7,13], [ 1,7,13 ], onlyonlydotL dotL ((icmOicmO),), dotGdotG ((icmEicmE),), andand dotO (icmB)) have homology homology with with the the corresponding corresponding genes genes virD4virD4, , virB10virB10and andvirB4 virB4 inin T4ASST4ASS inin sequencesequence level.level. FigureFigure 1.1. CompositionComposition of different T4SSs and homology co comparison.mparison. Blocks Blocks of of the the same same color color (green, (green, purple,purple, red, red, orange, orange, deep deep orange, orange, celadon, celadon, cyan cyan and and yellow) yellow) represent represent homologous homologous proteins; proteins; light light grey blocksgrey blocks in T4CSS in T4CSS represent represent proteins proteins of unknown of unknown function. function. Appl. Sci. 2018, 8, 2368 3 of 13 Appl. Sci. 2018, 8, x FOR PEER REVIEW 3 of 13 FigureFigure 2. 2. ProteinProtein composition composition of of T4ASS T4ASS (the (the VirB/VirD4 VirB/VirD4 system system from from AgrobacteriumAgrobacterium tumefaciens tumefaciens) )and and T4BSST4BSS (the (the Dot/Icm Dot/Icm system system from from LegionellaLegionella pneumophila pneumophila).). (a ()a )T4ASS. T4ASS. Outer Outer membrane membrane components: components: VirB7,VirB7, VirB9, VirB9, and and VirB10 VirB10;; inner inner membrane membrane components: components: VirB3, VirB3, VirB6, VirB6, and and VirB8; VirB8; pilus pilus components: components: VirB2VirB2 (major (major pilus pilus component) component) and and VirB5 VirB5 (minor (minor pilus pilus component); component); lytic lytic transglycosylase: transglycosylase: VirB1; VirB1; nucleosidenucleoside triphosphatases: triphosphatases: VirB4 VirB4 and and VirB11; VirB11; coupling coupling protein: protein: VirD4; VirD4; (b (b) )T4BSS. T4BSS.
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