Bacterial type IV secretion systems (T4SS) perform two fundamental functions related to pathogenesis: the delivery of effector molecules to eukaryotic target cells, and genetic exchange. Two T4SSs have been identified in Burkholderia cenocepacia K56-2, a representative of the ET12 lineage of the B. cepacia complex (Bcc). The plant tissue watersoaking (Ptw) T4SS encoded on a resident 92 kb plasmid is a chimera composed of VirB/D4 and F-specific subunits, and is responsible for the translocation of effector(s) that have been linked to the Ptw phenotype. The bc-VirB/D4 system located on chromosome II displays homology to the VirB/D4 T4SS of Agrobacterium tumefaciens. In contrast to the Ptw T4SS, the bc-VirB/D4 T4SS was found to be dispensable for Ptw effector(s) secretion, but was found to be involved in plasmid mobilization. The fertility inhibitor Osa did not affect the secretion of Ptw effector(s) via the Ptw system, but did disrupt the mobilization of a RSF1010 derivative plasmid.
AbdallahA. M.,
Gey van PittiusN. C.,
ChampionP. A.,
CoxJ.,
LuirinkJ.,
Vandenbroucke-GraulsC. M.,
AppelmelkB. J.,
BitterW.2007; Type VII secretion – mycobacteria show the way. Nat Rev Microbiol 5:883–891
AtmakuriK.,
DingZ.,
ChristieP. J.2003; VirE2, a type IV secretion substrate, interacts with the VirD4 transfer protein at cell poles of Agrobacterium tumefaciens
. Mol Microbiol 49:1699–1713
BarrettA. R.,
KangY.,
InamasuK. S.,
SonM. S.,
VukovichJ. M.,
HoangT. T.2008; Genetic tools for allelic replacement in Burkholderia species. Appl Environ Microbiol 74:4498–4508
CabezonE.,
LankaE.,
de la CruzF.1994; Requirements for mobilization of plasmids RSF1010 and ColE1 by the IncW plasmid R388: trwB and RP4 traG are interchangeable. J Bacteriol 176:4455–4458
ChenL.,
ChenY.,
WoodD. W.,
NesterE. W.2002; A new type IV secretion system promotes conjugal transfer in Agrobacterium tumefaciens
. J Bacteriol 184:4838–4845
ChristieP. J.2001; Type IV secretion: intercellular transfer of macromolecules by systems ancestrally related to conjugation machines. Mol Microbiol 40:294–305
ChristieP. J.,
AtmakuriK.,
KrishnamoorthyV.,
JakubowskiS.,
CascalesE.2005; Biogenesis, architecture, and function of bacterial type IV secretion systems. Annu Rev Microbiol 59:451–485
DharS. K.,
SoniR. K.,
DasB. K.,
MukhopadhyayG.2003; Molecular mechanism of action of major Helicobacter pylori virulence factors. Mol Cell Biochem 253:207–215
EngledowA. S.,
MedranoE. G.,
MahenthiralingamE.,
LiPumaJ. J.,
GonzalezC. F.2004; Involvement of a plasmid-encoded type IV secretion system in the plant tissue watersoaking phenotype of Burkholderia cenocepacia
. J Bacteriol 186:6015–6024
FlannaganR. S.,
LinnT.,
ValvanoM. A.2008; A system for the construction of targeted unmarked gene deletions in the genus Burkholderia
. Environ Microbiol 10:1652–1660
FongS. T.,
StanisichV. A.1989; Location and characterization of two functions on RP1 that inhibit the fertility of the IncW plasmid R388. J Gen Microbiol 135:499–502
GonzalezC. F.,
PettitE. A.,
ValadezV. A.,
ProvinE. M.1997; Mobilization, cloning, and sequence determination of a plasmid-encoded polygalacturonase from a phytopathogenic Burkholderia ( Pseudomonas) cepacia
. Mol Plant Microbe Interact 10:840–851
GuoM.,
JinS.,
SunD.,
HewC. L.,
PanS. Q.2007; Recruitment of conjugative DNA transfer substrate to Agrobacterium type IV secretion apparatus. Proc Natl Acad Sci U S A 104:20019–20024
HamiltonC. M.,
LeeH.,
LiP. L.,
CookD. M.,
PiperK. R.,
von BodmanS. B.,
LankaE.,
ReamW.,
FarrandS. K.2000; TraG from RP4 and TraG and VirD4 from Ti plasmids confer relaxosome specificity to the conjugal transfer system of pTiC58. J Bacteriol 182:1541–1548
HansenJ. B.,
OlsenR. H.1978; Isolation of large bacterial plasmids and characterization of the P2 incompatibility group plasmids pMG1 and pMG5. J Bacteriol 135:227–238
HoangT. T.,
Karkhoff-SchweizerR. R.,
KutchmaA. J.,
SchweizerH. P.1998; A broad-host-range Flp-FRT recombination system for site-specific excision of chromosomally-located DNA sequences: application for isolation of unmarked Pseudomonas aeruginosa mutants. Gene 212:77–86
HoldenM. T.,
Seth-SmithH. M.,
CrossmanL. C.,
SebaihiaM.,
BentleyS. D.,
Cerdeño-TárragaA. M.,
ThomsonN. R.,
BasonN.,
QuailM. A.other authors2009; The genome of Burkholderia cenocepacia J2315, an epidemic pathogen of cystic fibrosis patients. J Bacteriol 191:261–277
JonesK. M.,
LloretJ.,
DanieleJ. R.,
WalkerG. C.2007; The type IV secretion system of Sinorhizobium meliloti strain 1021 is required for conjugation but not for intracellular symbiosis. J Bacteriol 189:2133–2138
JuhasM.,
CrookD. W.,
DimopoulouI. D.,
LunterG.,
HardingR. M.,
FergusonD. J. P.,
HoodD. W.2007; Novel type IV secretion system involved in propagation of genomic islands. J Bacteriol 189:761–771
KostakiotiM.,
NewmanC. L.,
ThanassiD. G.,
StathopoulosC.2005; Mechanisms of protein export across the bacterial outer membrane. J Bacteriol 187:4306–4314
LabesM.,
PuhlerA.,
SimonR.1990; A new family of RSF1010-derived expression and lac-fusion broad-host-range vectors for Gram-negative bacteria. Gene 89:37–46
LeeL. Y.,
GelvinS. B.2004; Osa protein constitutes a strong oncogenic suppression system that can block vir-dependent transfer of IncQ plasmids between Agrobacterium cells and the establishment of IncQ plasmids in plant cells. J Bacteriol 186:7254–7261
LiP. L.,
EverhartD. M.,
FarrandS. K.1998; Genetic and sequence analysis of the pTiC58 trb locus, encoding a mating-pair formation system related to members of the type IV secretion family. J Bacteriol 180:6164–6172
LiP. L.,
HwangI.,
MiyagiH.,
TrueH.,
FarrandS. K.1999; Essential components of the Ti plasmid trb system, a type IV macromolecular transporter. J Bacteriol 181:5033–5041
LlosaM.,
ZunzuneguiS.,
de la CruzF.2003; Conjugative coupling proteins interact with cognate and heterologous VirB10-like proteins while exhibiting specificity for cognate relaxosomes. Proc Natl Acad Sci U S A 100:10465–10470
MahenthiralingamE.,
CoenyeT.,
ChungJ. W.,
SpeertD. P.,
GovanJ. R.,
TaylorP.,
VandammeP.2000; Diagnostically and experimentally useful panel of strains from the Burkholderia cepacia complex. J Clin Microbiol 38:910–913
NagaiH.,
CambronneE. D.,
KaganJ. C.,
AmorJ. C.,
KahnR. A.,
RoyC. R.2005; A C-terminal translocation signal required for Dot/Icm-dependent delivery of the Legionella RalF protein to host cells. Proc Natl Acad Sci U S A 102:826–831
O'CallaghanD.,
CazevieilleC.,
Allardet-ServentA.,
BoschiroliM. L.,
BourgG.,
FoulongneV.,
FrutosP.,
KulakovY.,
RamuzM.1999; A homologue of the Agrobacterium tumefaciens VirB and Bordetella pertussis Ptl type IV secretion systems is essential for intracellular survival of Brucella suis
. Mol Microbiol 33:1210–1220
SajjanS. U.,
CarmodyL. A.,
GonzalezC. F.,
LiPumaJ. J.2008; A type IV secretion system contributes to intracellular survival and replication of Burkholderia cenocepacia
. Infect Immun 76:5447–5455
SchellM. A.,
UlrichR. L.,
RibotW. J.,
BrueggemannE. E.,
HinesH. B.,
ChenD.,
LipscombL.,
KimH. S.,
MrázekJ.other authors 2007; Type VI secretion is a major virulence determinant in Burkholderia mallei
. Mol Microbiol 64:1466–1485
SchröderG.,
LankaE.2005; The mating pair formation system of conjugative plasmids – a versatile secretion machinery for transfer of proteins and DNA. Plasmid 54:1–25
SchuleinR.,
DehioC.2002; The VirB/VirD4 type IV secretion system of Bartonella is essential for establishing intraerythrocytic infection. Mol Microbiol 46:1053–1067
SchuleinR.,
GuyeP.,
RhombergT. A.,
SchmidM. C.,
SchroderG.,
VergunstA. C.,
CarenaI.,
DehioC.2005; A bipartite signal mediates the transfer of type IV secretion substrates of Bartonella henselae into human cells. Proc Natl Acad Sci U S A 102:856–861
SegalG.,
ShumanH. A.1998; Intracellular multiplication and human macrophage killing by Legionella pneumophila are inhibited by conjugal components of IncQ plasmid RSF1010. Mol Microbiol 30:197–208
SegalG.,
PurcellM.,
ShumanH. A.1998; Host cell killing and bacterial conjugation require overlapping sets of genes within a 22-kb region of the Legionella pneumophila genome. Proc Natl Acad Sci U S A 95:1669–1674
SegalG.,
RussoJ. J.,
ShumanH. A.1999; Relationships between a new type IV secretion system and the icm/ dot virulence system of Legionella pneumophila
. Mol Microbiol 34:799–809
SimoneM.,
McCullenC. A.,
StahlL. E.,
BinnsA. N.2001; The carboxy-terminus of VirE2 from Agrobacterium tumefaciens is required for its transport to host cells by the virB-encoded type IV transport system. Mol Microbiol 41:1283–1293
SokolP. A.,
DarlingP.,
WoodsD. E.,
MahenthiralingamE.,
KooiC.1999; Role of ornibactin biosynthesis in the virulence of Burkholderia cepacia: characterization of pvdA, the gene encoding l-ornithine N(5)-oxygenase. Infect Immun 67:4443–4455
VanlaereE.,
CoenyeT.,
SamynE.,
Van den PlasC.,
GovanJ.,
De BaetsF.,
De BoeckK.,
KnoopC.,
VandammeP.2005; A novel strategy for the isolation and identification of environmental Burkholderia cepacia complex bacteria. FEMS Microbiol Lett 249:303–307
VergunstA. C.,
van LierM. C.,
den Dulk-RasA.,
StuveT. A.,
OuwehandA.,
HooykaasP. J.2005; Positive charge is an important feature of the C-terminal transport signal of the VirB/D4-translocated proteins of Agrobacterium
. Proc Natl Acad Sci U S A 102:832–837
WalkerJ. E.,
SarasteM.,
RunswickM. J.,
GayN. J.1982; Distantly related sequences in the alpha- and beta-subunits of ATP synthase, myosin, kinases and other ATP-requiring enzymes and a common nucleotide binding fold. EMBO J 1:945–951