Bacterial Injection Machines

The delivery of virulence factors directly into host cells is a fascinating aspect of pathogenesis. For Gram-negative bacteria to translocate virulence factors into host cells, at least three membranes must be passed (two bacterial and a host plasma membrane). Bacterial injection machines deliver virulence factors to a specific cellular location where they intersect and influence host mechanisms. This minireview focuses on the Gram-negative bacterial translocation systems that mediate type III and type IV secretion. Remarkably, although these systems are complex multiprotein structures, there is significant similarity and analogy in function, and thus a conserved mechanistic theme in pathogenicity emerges. Currently there are seven identified types of macromolecular secretion systems in Gram-negative bacterial pathogens (1Henderson I.R. Nataro J.P. Kaper J.B. Meyer T.F. Farrand S.K. Burns D.L. Finlay B.B. Trends Microbiol. 2000; 8: 352Abstract Full Text Full Text PDF Scopus (35) Google Scholar, 2Thanassi D.G. Hultgren S.J. Curr. Opin. Cell Biol. 2000; 12: 420-430Crossref PubMed Scopus (235) Google Scholar). This minireview focuses on the two systems that deliver macromolecules directly into eukaryotic cells: type III secretion system (T3SS) 1The abbreviations used are: T3SS, type III secretion system(s); T4SS, type IV secretion system(s); Ysc, Yersinia type III secretion complex; EPEC, enteropathogenic E. coli.1The abbreviations used are: T3SS, type III secretion system(s); T4SS, type IV secretion system(s); Ysc, Yersinia type III secretion complex; EPEC, enteropathogenic E. coli. and type IV secretion system (T4SS). The delivered macromolecules are referred to as effectors, as they affect and alter the host cellular process. Gram-negative bacterial effectors cross several biochemically distinct barriers, including the bacterial inner membrane, peptidoglycan layer, and outer membrane as well as the host plasma membrane, and even potentially intracellular host membranes. Plant pathogen effectors have the additional complexity of crossing the plant cell wall. The biochemistry of these delivery systems will be discussed, including what is known about how they are assembled and how they function. In the 1980s and 1990s researchers studying Yersinia, a genus that causes human diseases ranging from bubonic plague to gastrointestinal disease, found that the bacteria produced proteins that were thought to be associated with the outer membrane called Yops. Yops lacked classical signal sequences and were not secreted via a sec-dependent pathway and thus were assumed to be delivered by a new type of secretion system, which later became known as a T3SS, representing its order of discovery in secretion systems. In the last 10 years T3SS have been identified in more than 20 bacterial pathogens that infect plants and animals (Table I). Although there is a high degree of conservation among the components of the type III apparatus in different bacterial species, the pathogens often carry a distinct set of virulence factors with a variety of functions that can be translocated into either animal or plant cells. The overall theme of these T3SS is the direct delivery of proteins that alter and in effect “hijack” the infected host cell for the pathogen (reviewed in Refs. 3Alfano J.R. Collmer A. J. Bacteriol. 1997; 179: 5655-5662Crossref PubMed Google Scholar and 4Hueck C.J. Microbiol. Mol. Biol. Rev. 1998; 62: 379-433Crossref PubMed Google Scholar).Table IType III secretion systems are found in a wide variety of human, animal and plant pathogensBacterial pathogenDiseaseAnimal pathogensBordetella speciesB. pertussisWhooping cough and other respiratory diseasesB. bronchisepticaRespiratory diseasesB. parapertussisRespiratory diseasesBurkholderiapseudomalleiMeliodosis (septicaemia, pneumonia, infections)Chlamydia speciesC. trachomatisInfectious blindness, sexually transmitted diseaseC. pneumoniaeUpper respiratory tract infections, possibly artherosclerosisC. psittaciPrimarily animal pathogenPathogenic E. coliEnteropathogenic E. coliDiarrheal diseasesEnterohemorrhagic E. coliDiarrheal diseases, hemolytic uremic syndromeRabbit EPECRabbit pathogenDog EPECDog pathogenP. aeruginosaOpportunistic pathogen: cystic fibrosis, burn victimsSalmonella serovarsS. typhiTyphoid fever in humansS. typhimuriumHumans: gastroenteritis, bacteremia, enteric feverMouse: typhoid feverS. dublinCattle pathogenS. pullorumPoultry pathogenS. arizonaeReptile pathogenS. enteritidisGastroenteritis in a broad host rangeS. choleraesuisBroad host rangeShigella speciesS. dysenteriaeBacillary dysenteryS. flexneriDiarrheal diseasesYersinia speciesY. pestisBubonic plagueY. enterocoliticaGastrointestinal syndromesY. pseudotuberculosisSelf-limiting gastroenteritisPlant pathogensErwinia speciesE. amylovoraSoft rot of plantsE. chrysanthemiFire blight of rosaceous plantsP. syringaeBacterial speck diseaseRalstonia solanacearumBacterial wilt of solanaceous plantsXanthomonas campestrisBacterial spot disease of pepper and tomatoFish pathogensAeromonas salmonicidaFurunculosisEndosymbiontRhizobium speciesCultivar-specific nodulation of leguminous plantsSodalis glossinidiusIntracellular endosymbiont of the tsetse fly Open table in a new tab Over 20 proteins are proposed to form a functional T3SS (Fig. 1A) (4Hueck C.J. Microbiol. Mol. Biol. Rev. 1998; 62: 379-433Crossref PubMed Google Scholar, 5Michiels T. Vanooteghem J.-C. Lambert de Rouvroit C. China B. Gustin A. Boudry P. Cornelis G.R. J. Bacteriol. 1991; 173: 4994-5009Crossref PubMed Scopus (215) Google Scholar). YscN is thought to energize the secretion machinery, as it shares homology with the F0F1-ATPase and has an ATP-binding site. YscN from Yersinia and its homologue InvC from Salmonella typhimurium have been shown to have ATPase activity as mutations in the catalytic domain cause a loss of secretion (6Eichelberg K. Ginocchio C.C. Galan J.E. J. Bacteriol. 1994; 176: 4501-4510Crossref PubMed Google Scholar, 7Woestyn S. Allaoui A. Wattiau P. Cornelis G.R. J. Bacteriol. 1994; 176: 1561-1569Crossref PubMed Google Scholar). YscN homologues are predicted to be located in the cytoplasm where they interact with membrane-bound components of the type III secretion apparatus, thereby energizing the system (4Hueck C.J. Microbiol. Mol. Biol. Rev. 1998; 62: 379-433Crossref PubMed Google Scholar). It has been speculated that the ATPase polymerizes, by itself or with other components, to form the lower part of the T3SS, but this has not been shown. Lending support to this model, YscN has been shown to form a complex with three other cytoplasmic and/or inner membrane-associated Ysc proteins (8Jackson M.W. Plano G.V. FEMS Microbiol. Lett. 2000; 186: 85-90Crossref PubMed Google Scholar). Many of the proteins involved in forming the T3SS have been localized or are predicted to be inner membrane proteins with varying numbers of transmembrane domains. For example the Yersinia YscV (LcrD) contains eight transmembrane domains and a large cytoplasmic C-terminal domain (9Plano G.V. Barve S.S. Straley S.C. J. Bacteriol. 1991; 173: 7293-7303Crossref PubMed Google Scholar, 10Plano G.V. Straley S.C. J. Bacteriol. 1993; 175: 3536-3545Crossref PubMed Google Scholar). YscJ family members carry sec-dependent signal sequences and are lipoproteins (4Hueck C.J. Microbiol. Mol. Biol. Rev. 1998; 62: 379-433Crossref PubMed Google Scholar, 11Allaoui A. Sansonetti P.J. Parsot C. J. Bacteriol. 1992; 174: 7661-7669Crossref PubMed Scopus (125) Google Scholar). The Pseudomonas syringae homologue HrcJ is associated with both inner and outer membranes (12Deng W.L. Huang H.C. J. Bacteriol. 1999; 181: 2298-2301Crossref PubMed Google Scholar), suggesting that it spans the periplasmic space. Homologues of YscC (e.g. InvG, HrcC) are the only components of the type III apparatus that are clearly found in the outer membrane (12Deng W.L. Huang H.C. J. Bacteriol. 1999; 181: 2298-2301Crossref PubMed Google Scholar, 13Crago A.M. Koronakis V. Mol. Microbiol. 1998; 30: 47-56Crossref PubMed Scopus (137) Google Scholar, 14Koster M. Bitter W. de Cock H. Allaoui A. Cornelis G.R. Tommassen J. Mol. Microbiol. 1997; 26: 789-797Crossref PubMed Scopus (188) Google Scholar, 15Plano G.V. Straley S.C. J. Bacteriol. 1995; 177: 3843-3854Crossref PubMed Google Scholar). YscC belongs to a family of proteins (secretins) that are involved in transporting large molecules across the outer membrane probably by forming a channel (4Hueck C.J. Microbiol. Mol. Biol. Rev. 1998; 62: 379-433Crossref PubMed Google Scholar). YscC and its homologues form a ring-shaped oligomeric complex in the outer membrane with approximately a 20-nm diameter. Experimentally it has been shown that InvG has a cleavable signal sequence at residue 25, indicating that secretins are exported by the sec-dependent pathway (16Kubori T. Matsushima Y. Nakamura D. Uralil J. Lara-Tejero M. Sukhan A. Galan J.E. Aizawa S.I. Science. 1998; 280: 602-605Crossref PubMed Scopus (697) Google Scholar). It has been demonstrated that small outer membrane lipoproteins are required to increase the efficiency for the correct localization and functioning of the YscC homologues (13Crago A.M. Koronakis V. Mol. Microbiol. 1998; 30: 47-56Crossref PubMed Scopus (137) Google Scholar, 14Koster M. Bitter W. de Cock H. Allaoui A. Cornelis G.R. Tommassen J. Mol. Microbiol. 1997; 26: 789-797Crossref PubMed Scopus (188) Google Scholar, 17Daefler S. Russel M. Mol. Microbiol. 1998; 28: 1367-1380Crossref PubMed Scopus (94) Google Scholar, 18Sukhan A. Kubori T. Wilson J. Galan J.E. J. Bacteriol. 2001; 183: 1159-1167Crossref PubMed Scopus (140) Google Scholar, 19Schuch R. Maurelli A.T. J. Bacteriol. 2001; 183: 6991-6998Crossref PubMed Scopus (66) Google Scholar). Recently we have shown that correct insertion and function of enteropathogenic Escherichia coli's (EPEC) EscC secretin in the outer membrane requires cytoplasmic and inner membrane components of the type III apparatus, namely EscN and EscV (20Gauthier A. Puente J.L. Finlay B.B. Infect. Immun. 2003; 71: 3310-3319Crossref PubMed Scopus (125) Google Scholar). Electron microscopic analysis has revealed the T3SS to be an organelle that consists of a base (or syringe) that spans the bacterial membranes and peptidoglycan layer composed of two pairs of rings that are joined by a central channel, and a hollow needle-like structure that protrudes outside the bacteria and in some cases has been observed to contact the host cells (reviewed in Refs. 21Kimbrough T.G. Miller S.I. Microbes Infect. 2002; 4: 75-82Crossref PubMed Scopus (75) Google Scholar and 22Blocker A. Komoriya K. Aizawa S.-I. Proc. Natl. Acad. Sci. U. S. A. 2003; 6: 3027-3030Crossref Scopus (242) Google Scholar). There is a remarkable structural similarity to the bacterial flagellar basal bodies (see “Origin of Translocation Systems”). Mutants in the needle protein cannot secrete or translocate effectors, suggesting that either the needle keeps the pore open or that the needle extends into the “syringe.” Whereas needle proteins exist in all of the animal pathogens, a homologous protein has not been found in the plant pathogens although the pilus protein HrpA seems to play a similar functional role (23Plano G.V. Day J.B. Ferracci F. Mol. Microbiol. 2001; 40: 284-293Crossref PubMed Scopus (91) Google Scholar). Elegant immunogold electron microscopy experiments have been conducted with the plant pathogens Erwinia and P. syringae demonstrating very clearly that the effectors actually go through the needle/pilus conduit and can be visualized at the tip of the structure (24Jin Q. He S.Y. Science. 2001; 294: 2556-2558Crossref PubMed Scopus (147) Google Scholar, 25Li C.-M. Brown I. Mansfield J. Stevens C. Boureau T. Romantschuk M. Taira S. EMBO J. 2002; 21: 1909-1915Crossref PubMed Scopus (97) Google Scholar). This indicates that the type III apparatus and needle are a hollow conduit for protein delivery. All of the animal pathogen T3SS have one or more proteins that are thought to form a pore in the host cell membrane, called the “translocon” (reviewed in Ref. 26Buttner D. Bonas U. Trends Microbiol. 2002; 10: 186-192Abstract Full Text Full Text PDF PubMed Scopus (187) Google Scholar). It is important to note that although mutations in needle components result in no secretion or translocation of effectors, mutation of translocon components yields wild-type levels of secreted but not translocated effectors. Most of the translocon proteins contain one or two predicted transmembrane domains and are associated with host cell membranes. Furthermore, in EPEC the needle sheath protein EspA and the translocon EspB have been shown to interact by a number of binding assays (27Hartland E.L. Daniell S.J. Delahay R.M. Neves B.C. Wallis T. Shaw R.K. Hale C. Knutton S. Frankel G. Mol. Microbiol. 2000; 35: 1483-1492Crossref PubMed Scopus (73) Google Scholar), suggesting a continuous channel. Additionally, Yersinia and P. aeruginosa have another type of translocon protein that does not contain α-helical transmembrane domains but is required for pore formation. Translocon proteins have not been described in plant pathogens, but HrpF from Xanthomonas is a candidate as it is not needed for secretion but is required for translocation and forms pores in lipid bilayers (28Buttner D. Nennstiel D. Klusener B. Bonas U. J. Bacteriol. 2002; 184: 2389-2398Crossref PubMed Scopus (130) Google Scholar). T3SS effectors do not have an obvious signal sequence. However, there is evidence for the existence of three different kinds of secretion signals: the 5′-region of the mRNA, the N terminus of the effector, and/or the ability of a chaperone to bind the effector before secretion (reviewed in Ref. 29Aldridge P. Hughes K.T. Trends Microbiol. 2001; 9: 209-214Abstract Full Text Full Text PDF PubMed Scopus (44) Google Scholar). The minimal requirement for secretion of some effectors is the N-terminal 10–15 residues (30Sory M.P. Boland A. Lambermont I. Cornelis G.R. Proc. Natl. Acad. Sci. U. S. A. 1995; 92: 11998-12002Crossref PubMed Scopus (393) Google Scholar, 31Schesser K. Frithz-Lindsten E. Wolf-Watz H. J. Bacteriol. 1996; 178: 7227-7233Crossref PubMed Google Scholar), whereas the minimum needed for translocation is 50–75 N-terminal residues (30Sory M.P. Boland A. Lambermont I. Cornelis G.R. Proc. Natl. Acad. Sci. U. S. A. 1995; 92: 11998-12002Crossref PubMed Scopus (393) Google Scholar, 31Schesser K. Frithz-Lindsten E. Wolf-Watz H. J. Bacteriol. 1996; 178: 7227-7233Crossref PubMed Google Scholar). The so-called mRNA hypothesis is very controversial. Two groups have shown that certain effectors have a 5′-mRNA fold that directs translocation (32Anderson D.M. Schneewind O. Science. 1997; 278: 1140-1143Crossref PubMed Scopus (258) Google Scholar, 33Anderson D.M. Fouts D.E. Collmer A. Schneewind O. Proc. Natl. Acad. Sci. U. S. A. 1999; 96: 12839-12843Crossref PubMed Scopus (114) Google Scholar, 34Anderson D.M. Schneewind O. Mol. Microbiol. 1999; 31: 1139-1148Crossref PubMed Scopus (119) Google Scholar, 35Ramamurthi K.S. Schneewind O. J. Bacteriol. 2002; 184: 3321-3328Crossref PubMed Scopus (43) Google Scholar), but others have refuted these observations with equally convincing experiments showing that the N-terminal amino acids are the signal (36Lloyd S.A. Norman M. Rosqvist R. Wolf-Watz H. Mol. Microbiol. 2001; 39: 520-531Crossref PubMed Scopus (167) Google Scholar). Many functions have been attributed to T3SS chaperones, but the exact role or roles of the entire family of chaperones remain to be determined (reviewed in Refs. 29Aldridge P. Hughes K.T. Trends Microbiol. 2001; 9: 209-214Abstract Full Text Full Text PDF PubMed Scopus (44) Google Scholar and 37Page A.L. Parsot C. Mol. Microbiol. 2002; 46: 1-11Crossref PubMed Scopus (124) Google Scholar). Although most chaperones have only one cognate effector, there are exceptions with differing numbers of effectors. Deletion of a chaperone usually results in less of the cognate effector in the cytoplasm of the bacteria and less secreted/translocated. For some effectors, chaperone binding prevents degradation, whereas for others it has been suggested that chaperone binding prevents premature association. Another model suggests that chaperones escort the effector to the type III apparatus and play a role in the hierarchy of translocation (38Boyd A.P. Lambermont I. Cornelis G.R. J. Bacteriol. 2000; 182: 4811-4821Crossref PubMed Scopus (109) Google Scholar). Chaperones could maintain effectors in a secretion-competent state. The needle of the T3SS is likely too small to allow folded proteins to pass through, but recent data suggest that effectors are in a partially folded conformation (reviewed in Ref. 39Smith C.L. Hultgren S.J. Nature. 2001; 414: 29-31Crossref PubMed Scopus (4) Google Scholar). T4SS are a recent discovery in pathogenic delivery systems (reviewed in Refs. 40Burns D.L. Curr. Opin. Microbiol. 1999; 2: 25-29Crossref PubMed Scopus (91) Google Scholar and 41Christie P.J. Mol. Microbiol. 2001; 40: 294-305Crossref PubMed Scopus (255) Google Scholar). These systems deliver proteins and DNA (often complexed together), but they can also deliver only proteins. The prototype and most well studied T4SS is involved in the transfer of oncogenic DNA into plant cells by Agrobacterium tumefaciens (reviewed in Ref. 42Lai E.M. Kado C.I. Trends Microbiol. 2000; 8: 361-369Abstract Full Text Full Text PDF PubMed Scopus (91) Google Scholar). Although the function and perhaps the mechanism of the T4SS are similar to the T3SS, there is little to no conservation in the proteins that comprise the apparatus. The lack of conservation suggests the mechanism at a molecular and physical level may differ significantly between the two. Like the T3SS, the T4SS is considered “promiscuous” in terms of the variety of substrates and the diversity of target cells (43Christie P.J. Vogel J.P. Trends Microbiol. 2000; 8: 354-360Abstract Full Text Full Text PDF PubMed Scopus (383) Google Scholar) (Table II). It should be noted that although T4SS have recently been identified in a number of bacterial species, are often IV secretion systems translocate macromolecules across a variety of of of virulence and delivery to host of of of host cell and in in intracellular in intracellular in intracellular to in Open table in a new tab The involved in transfer in A. tumefaciens contains of which are as well as an additional which is involved in the of DNA (Fig. (reviewed in Ref. 41Christie P.J. Mol. Microbiol. 2001; 40: 294-305Crossref PubMed Scopus (255) Google Scholar). It is important to note that not all of the type family of bacteria have homologues of all of these and a conserved of proteins of and C. E. Mol. Microbiol. 2002; PubMed Scopus Google Scholar). The type IV apparatus components have been localized and with most of the on A. proteins are found in the inner membrane and some are membrane proteins and whereas others are associated with the inner of the inner membrane (reviewed in Ref. 40Burns D.L. Curr. Opin. Microbiol. 1999; 2: 25-29Crossref PubMed Scopus (91) Google Scholar). to both the inner and outer membranes A. Mol. Microbiol. 1998; PubMed Scopus (73) Google Scholar), and it has been suggested that these proteins in to both membranes. In is a that is important for structural of other components of the T4SS D. P.J. J. Bacteriol. 1996; 178: PubMed Google Scholar). with and results suggest that the outer membrane complex with the inner membrane proteins and to form the translocation channel A. J. Bacteriol. 2000; 182: PubMed Scopus Google Scholar). The T4SS has at least two and possibly three The may be required for the translocation to open the channel, as a or for chaperone functions (reviewed in Refs. 40Burns D.L. Curr. Opin. Microbiol. 1999; 2: 25-29Crossref PubMed Scopus (91) Google Scholar and 41Christie P.J. Mol. Microbiol. 2001; 40: 294-305Crossref PubMed Scopus (255) Google Scholar). to what has been observed for the T3SS, have demonstrated that activity is for and have binding and have ATPase activity E. V. J. P.J. J. Bacteriol. 2001; 183: PubMed Scopus Google Scholar). recent support a model there can be DNA transfer by the structure of but that it is the activity that it an system B. P.J. Mol. Microbiol. 1999; PubMed Scopus Google Scholar). ATPase homologues from T4SS in and have been shown by electron microscopy to form a structure with a and a central channel S. M. W. R. E. Proc. Natl. Acad. Sci. U. S. A. 2000; PubMed Scopus Google Scholar). The structure of the H. ATPase to has been and suggests that this family of may function as chaperones similar to E. G. Mol. 2000; 6: Full Text Full Text PDF PubMed Scopus Google Scholar). In A. tumefaciens the to be in and have a Science. 1996; PubMed Scopus Google Scholar), and it is of which is a small protein E.M. Kado C.I. J. Bacteriol. 1998; PubMed Google Scholar, A.L. E.M. K. Kado C.I. J. Bacteriol. 1996; 178: PubMed Google Scholar), a structure of the T3SS it has been suggested that may the components to the of the translocation U. G. S. C. Proc. Natl. Acad. Sci. U. S. A. 2002; PubMed Scopus Google Scholar). has been suggested to the translocon or function of the T4SS it forms large and the of DNA F. M. P. P. B. Proc. Natl. Acad. Sci. U. S. A. 2001; PubMed Scopus Google Scholar). Chaperones are involved in the of both DNA and proteins by the There is evidence for the chaperone and W. S. M.P. Mol. Microbiol. 1999; 31: PubMed Scopus Google Scholar), suggesting a function in premature as has been suggested for the T3SS It has been suggested that proteins the family by and T4SS substrates (reviewed in Ref. P.J. Vogel J.P. Trends Microbiol. 2000; 8: 354-360Abstract Full Text Full Text PDF PubMed Scopus (383) Google Scholar). seems to be an in the T4SS substrates there are periplasmic (reviewed in Ref. 40Burns D.L. Curr. Opin. Microbiol. 1999; 2: 25-29Crossref PubMed Scopus (91) Google Scholar). the sec-dependent secretion pathway for to the and the T4SS for secretion of the Additionally, the system is the other T4SS in that it functions of host contact of the ability of the to itself into the host cell than on T4SS delivery. Although periplasmic of effectors have not been found in the T3SS, recent in the T4SS suggest that the translocation are not and M. Y. Mol. Microbiol. 2002; PubMed Scopus Google Scholar) have demonstrated that T4SS substrates in A. tumefaciens that lack a signal form a complex in the with another and interact with components of the This suggests a model for type IV secretion in which effectors are exported via different into the and translocated across the outer membrane and host cell membrane via the Many but not all of the proteins the T3SS of pathogenic bacteria have homologues that are known to be involved in flagellar are complex cell that in The a hollow in a and a basal least are involved in a Ref. Hughes K.T. Microbiol. Mol. Biol. Rev. 2000; PubMed Scopus Google Scholar). T3SS needle are not although these secretion systems are both involved in different which to form a cell In T3SS needle bacterial basal bodies by electron microscopy (16Kubori T. Matsushima Y. Nakamura D. Uralil J. Lara-Tejero M. Sukhan A. Galan J.E. Aizawa S.I. Science. 1998; 280: 602-605Crossref PubMed Scopus (697) Google Scholar, K. M. T. K. C. A. Proc. Natl. Acad. Sci. U. S. A. 2001; PubMed Scopus Google Scholar, A. E. P. F. Parsot C. Sansonetti P. Allaoui A. Mol. Microbiol. 2001; 39: PubMed Scopus Google Scholar). that form these basal bodies are some of the most conserved components in all T3SS and are homologous to specific flagellar proteins. example is YscJ its homologues in all which are lipoproteins that sequence similarity with from the flagellar secretion This family of proteins is involved in forming an oligomeric is how have these secretion systems with similar It is that in the of a bacterial other proteins became to the flagellar apparatus and were This hypothesis is to but there is some evidence to suggest that this is the In Yersinia it has been shown that a small specific number of virulence substrates are secreted through the flagellar pathway Miller Proc. Natl. Acad. Sci. U. S. A. 1999; 96: PubMed Scopus Google Scholar). complex functional secretion system for a cell organelle has been in to the of lower bacteria have likely been cells for of Bacterial pathogens have to infect the eukaryotic cell types the T3SS The components of T3SS that directly contact the host cell the needle and translocon are not as conserved among bacteria with the basal components T.G. Miller S.I. Microbes Infect. 2002; 4: 75-82Crossref PubMed Scopus (75) Google Scholar, S.-I. FEMS Microbiol. Lett. 2001; PubMed Google Scholar). the structural needle proteins do not to sequence homology with proteins. it is that in the flagellar secretion systems and T3SS of the basal components an apparatus, and the components have been by about by the or the some of the components involved in the secretion of virulence substrates via the T4SS are similar to required for the transfer of DNA by bacterial All components of the are homologous to components of the A. tumefaciens T4SS, and components of the system homology to the T4SS C. E. Mol. Microbiol. 2002; PubMed Scopus Google Scholar). These a family of secretion and proteins as and to It is that bacterial is a process. In it has been demonstrated that the DNA transfer pathway can mediate the translocation of a protein between E. cells A.T. Mol. Microbiol. 2000; PubMed Scopus Google Scholar). B. A. de P.J. Science. 2000; PubMed Scopus Google Scholar) demonstrated that the system proteins as well as these that a system for the transfer of one of (e.g. could be by a different type of (e.g. effector This where an translocation system is for a virulence is also to have for the flagellar secretion pathway and T3SS Miller Proc. Natl. Acad. Sci. U. S. A. 1999; 96: PubMed Scopus Google Scholar). It has also been proposed that T4SS were for with other and later to virulence with 2001; PubMed Scopus Google Scholar). type III and type IV translocation machines are in to the of how to bacterial proteins across the Gram-negative as well as into target cells. The T3SS is and it is that it will be how this system is assembled and functions to deliver proteins directly into host cells. The most recent in the T4SS suggesting a transfer with a periplasmic suggest that more are to The of a hierarchy of is more in the T3SS and likely also in Although the of both these systems is not the from flagellar to type III secretion and bacterial to type IV secretion may not be a in the of

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