Conjugative type IV secretion systems in Gram-positive bacteria

Abajy, 2007, A type IV-secretion-like system is required for conjugative DNA transport of broad-host-range plasmid pIP501 in Gram-positive bacteria, J. Bacteriol., 189, 2487, 10.1128/JB.01491-06 Alvarez-Martinez, 2009, Biological diversity of prokaryotic type IV secretion systems, Microbiol. Mol. Biol. Rev., 73, 775, 10.1128/MMBR.00023-09 Arends, 2013, TraG encoded by the pIP501 type IV secretion system is a two domain peptidoglycan degrading enzyme essential for conjugative transfer, J. Bacteriol., 195, 4436, 10.1128/JB.02263-12 Auchtung, 2005, Regulation of a Bacillus subtilis mobile genetic element by intercellular signaling and the global DNA damage response, Proc. Natl. Acad. Sci. USA, 102, 12554, 10.1073/pnas.0505835102 Babic, 2011, Efficient gene transfer in bacterial cell chains, mBio., 2, e00027-11, 10.1128/mBio.00027-11 Bailey, 2006, Agrobacterium tumefaciens VirB8 structure reveals potential protein–protein interaction sites, Proc. Natl. Acad. Sci. USA, 103, 2582, 10.1073/pnas.0511216103 Bannam, 2006, Functional identification of conjugation and replication regions of the tetracycline resistance plasmid pCW3 from Clostridium perfringens, J. Bacteriol., 188, 4942, 10.1128/JB.00298-06 Bantwal, 2012, The peptidoglycan hydrolase TcpG is required for efficient conjugative transfer of pCW3 in Clostridium perfringens, Plasmid, 67, 139, 10.1016/j.plasmid.2011.12.016 Bauer, 2011, Localization pattern of conjugation machinery in a Gram-positive bacterium, J. Bacteriol., 193, 6244, 10.1128/JB.00175-11 Bentley, 2004, SCP1, a 356,023 bp linear plasmid adapted to the ecology and developmental biology of its host, Streptomyces coelicolor A3(2), Mol. Microbiol., 51, 1615, 10.1111/j.1365-2958.2003.03949.x Bey, 2000, The homologous terminal sequence of the Streptomyces lividans chromosome and SLP2 plasmid, Microbiology, 146, 911, 10.1099/00221287-146-4-911 Bhatty, 2013, The expanding bacterial type IV secretion lexicon, Res. Microbiol., 164, 620, 10.1016/j.resmic.2013.03.012 Bordeleau, 2012, Diversity of integrating conjugative elements in actinobacteria: coexistence of two mechanistically different DNA-translocation systems, Mob. Genet. Elements, 2, 119, 10.4161/mge.20498 Bose, 2011, Regulation of horizontal gene transfer in Bacillus subtilis by activation of a conserved site-specific protease, J. Bacteriol., 193, 22, 10.1128/JB.01143-10 Brolle, 1993, Analysis of the transfer region of the Streptomyces plasmid SCP2∗, Mol. Microbiol., 10, 157, 10.1111/j.1365-2958.1993.tb00912.x Brynestad, 2001, Enterotoxin plasmid from Clostridium perfringens is conjugative, Infect. Immun., 69, 3483, 10.1128/IAI.69.5.3483-3487.2001 Burrus, 2002, Conjugative transposons: the tip of the iceberg, Mol. Microbiol., 46, 601, 10.1046/j.1365-2958.2002.03191.x Burrus, 2004, Shaping bacterial genomes with integrative and conjugative elements, Res. Microbiol., 155, 376, 10.1016/j.resmic.2004.01.012 Cascales, 2004, Definition of a bacterial type IV secretion pathway for a DNA substrate, Science, 304, 1170, 10.1126/science.1095211 Chandran, 2009, Structure of the outer membrane complex of a type IV secretion system, Nature, 462, 1011, 10.1038/nature08588 Chen, 1996, Complications and implications of linear bacterial chromosomes, Trends Genet., 12, 192, 10.1016/0168-9525(96)30014-0 Chen, 2008, Enterococcus faecalis PcfC, a spatially localized substrate receptor for type IV secretion of the pCF10 transfer intermediate, J. Bacteriol., 190, 3632, 10.1128/JB.01999-07 Clewell, 2007, Properties of Enterococcus faecalis plasmid pAD1, a member of a widely disseminated family of pheromone-responding, conjugative, virulence elements encoding cytolysin, Plasmid, 58, 205, 10.1016/j.plasmid.2007.05.001 Coros, 2008, The specialized secretory apparatus ESX-1 is essential for DNA transfer in Mycobacterium smegmatis, Mol. Microbiol., 69, 794 Dang, 1999, Dimerization of the Agrobacterium tumefaciens VirB4 ATPase and the effect of ATP-binding cassette mutations on the assembly and function of the T-DNA transporter, Mol. Microbiol., 32, 1239, 10.1046/j.1365-2958.1999.01436.x Dawson, 2010, Sortase transpeptidases: insights into mechanism, substrate specificity, and inhibition, Biopolymers, 94, 385, 10.1002/bip.21472 de la Cruz, 2010, Conjugative DNA metabolism in Gram-negative bacteria, FEMS Microbiol. Rev., 34, 18, 10.1111/j.1574-6976.2009.00195.x Dubarry, 2010, Multiple regions along the Escherichia coli FtsK protein are implicated in cell division, Mol. Microbiol., 78, 1088, 10.1111/j.1365-2958.2010.07412.x Dunny, 2007, The peptide pheromone-inducible conjugation system of Enterococcus faecalis plasmid pCF10: cell–cell signalling, gene transfer, complexity and evolution, Philos. Trans. R. Soc. Lond. B Biol. Sci., 362, 1185, 10.1098/rstb.2007.2043 Durand, 2011, Structural insights into the membrane-extracted dimeric form of the ATPase TraB from the Escherichia coli pKM101 conjugation system, BMC Struct. Biol., 11, 4, 10.1186/1472-6807-11-4 Francia, 2004, A classification scheme for mobilization regions of bacterial plasmids, FEMS Microbiol. Rev., 28, 79, 10.1016/j.femsre.2003.09.001 Franco, 2003, Direct repeat sequences are essential for function of the cis-acting locus of transfer (clt) of Streptomyces phaeochromogenes plasmid pJV1, Plasmid, 50, 242, 10.1016/S0147-619X(03)00063-5 Fronzes, 2009, The structural biology of type IV secretion systems, Nat. Rev. Microbiol., 7, 703, 10.1038/nrmicro2218 Frost, 2005, Mobile genetic elements: the agents of open source evolution, Nat. Rev. Microbiol., 3, 722, 10.1038/nrmicro1235 Goessweiner-Mohr, 2013, The 2.5Å structure of the Enterococcus conjugation protein TraM resembles VirB8 type IV secretion proteins, J. Biol. Chem., 288, 2018, 10.1074/jbc.M112.428847 Gomis-Rüth, 2001, Conjugative plasmid protein TrwB, an integral membrane type IV secretion system coupling protein, J. Biol. Chem., 277, 7556, 10.1074/jbc.M110462200 Gomis-Rüth, 2004, Coupling factors in macromolecular type-IV secretion machineries, Curr. Pharm. Des., 10, 1551, 10.2174/1381612043384817 Grohmann, 2003, Conjugative plasmid transfer in Gram-positive bacteria, Microbiol. Mol. Biol. Rev., 67, 277, 10.1128/MMBR.67.2.277-301.2003 Guglielmini, 2013, Evolution of conjugation and type IV secretion systems, Mol. Biol. Evol., 30, 315, 10.1093/molbev/mss221 Haft, 2007, In vivo oligomerization of the F conjugative coupling protein TraD, J. Bacteriol., 189, 6626, 10.1128/JB.00513-07 Hendrickx, 2009, LPxTG surface proteins of enterococci, Trends Microbiol., 17, 423, 10.1016/j.tim.2009.06.004 Heuer, 2012, Plasmids foster diversification and adaptation of bacterial populations in soil, FEMS Microbiol. Rev., 36, 1083, 10.1111/j.1574-6976.2012.00337.x Hirt, 2005, Characterization of the pheromone response of the Enterococcus faecalis conjugative plasmid pCF10: complete sequence and comparative analysis of the transcriptional and phenotypic responses of pCF10-containing cells to pheromone induction, J. Bacteriol., 187, 1044, 10.1128/JB.187.3.1044-1054.2005 Hopwood, 1993, Conjugative plasmids of Streptomyces, 293 Horodniceanu, 1979, Conjugative R plasmids in Streptococcus agalactiae (group B), Plasmid, 2, 197, 10.1016/0147-619X(79)90038-6 Huang, 2003, Linear plasmid SLP2 of Streptomyces lividans is a composite replicon, Mol. Microbiol., 47, 1563, 10.1046/j.1365-2958.2003.03403.x Itaya, 2006, Conjugational transfer kinetics of pLS20 between Bacillus subtilis in liquid medium, Biosci. Biotechnol. Biochem., 70, 740, 10.1271/bbb.70.740 Jakubowski, 2005, Agrobacterium tumefaciens VirB9, an outer-membrane-associated component of a type IV secretion system, regulates substrate selection and T-Pilus biogenesis, J. Bacteriol., 187, 3486, 10.1128/JB.187.10.3486-3495.2005 Jakubowski, 2004, Agrobacterium tumefaciens VirB6 domains direct the ordered export of a DNA substrate through a type IV secretion system, J. Mol. Biol., 341, 961, 10.1016/j.jmb.2004.06.052 Judd, 2005, Spatial location and requirements for the assembly of the Agrobacterium tumefaciens type IV secretion apparatus, Proc. Natl. Acad. Sci. USA, 102, 11498, 10.1073/pnas.0505290102 Judd, 2005, Molecular characterization of the Agrobacterium tumefaciens DNA transfer protein VirB6, Microbiology, 151, 3483, 10.1099/mic.0.28337-0 Kataoka, 1994, Complete nucleotide sequence of the Streptomyces nigrifaciens plasmid, pSN22: genetic organization and correlation with genetic properties, Plasmid, 32, 55, 10.1006/plas.1994.1044 Kieser, 1982, PIJ101, a multi-copy broad host-range Streptomyces plasmid: functional analysis and development of DNA cloning vectors, Mol. Gen. Genet., 185, 223, 10.1007/BF00330791 Kopec, 2005, TraA and its N-terminal relaxase domain of the Gram-positive plasmid pIP501 show specific oriT binding and behave as dimers in solution, Biochem. J., 387, 401, 10.1042/BJ20041178 Kosono, 1996, The TraB protein, which mediates the intermycelial transfer of the Streptomyces plasmid pSN22, has functional NTP-binding motifs and is localized to the cytoplasmic membrane, Mol. Microbiol., 19, 397, 10.1046/j.1365-2958.1996.379909.x Kozlowicz, 2006, Molecular basis for control of conjugation by bacterial pheromone and inhibitor peptides, Mol. Microbiol., 62, 958, 10.1111/j.1365-2958.2006.05434.x Krishnan, 2011, Crystallography of Gram-positive bacterial adhesins, Adv. Exp. Med. Biol., 715, 175, 10.1007/978-94-007-0940-9_11 Kurenbach, 2003, Intergeneric transfer of the Enterococcus faecalis plasmid pIP501 to Escherichia coli and Streptomyces lividans and sequence analysis of its tra region, Plasmid, 50, 86, 10.1016/S0147-619X(03)00044-1 Kurenbach, 2002, The tra region of the conjugative plasmid pIP501 is organized in an operon with the first gene encoding the relaxase, J. Bacteriol., 184, 1801, 10.1128/JB.184.6.1801-1805.2002 Kurenbach, 2006, The TraA relaxase autoregulates the putative type IV secretion-like system encoded by the broad-host-range Streptococcus agalactiae plasmid pIP501, Microbiology, 152, 637, 10.1099/mic.0.28468-0 Lee, 2007, Identification and characterization of int (integrase), xis (excisionase) and chromosomal attachment sites of the integrative and conjugative element ICEBs1 of Bacillus subtilis, Mol. Microbiol., 66, 1356 Lee, 2010, Autonomous plasmid-like replication of a conjugative transposon, Mol. Microbiol., 75, 268, 10.1111/j.1365-2958.2009.06985.x Lee, 2012, The Bacillus subtilis conjugative transposon ICEBs1 mobilizes plasmids lacking dedicated mobilization functions, J. Bacteriol., 194, 3165, 10.1128/JB.00301-12 Li, 2012, Enterococcus faecalis PrgJ, a VirB4-Like ATPase, mediates pCF10 conjugative transfer through substrate binding, J. Bacteriol., 194, 4041, 10.1128/JB.00648-12 Li, 2013, Toxin plasmids of Clostridium perfringens, Microbiol. Mol. Biol. Rev., 77, 208, 10.1128/MMBR.00062-12 Li, 2011, GI-type T4SS-mediated horizontal transfer of the 89K pathogenicity island in epidemic Streptococcus suis serotype 2, Mol. Microbiol., 79, 1670, 10.1111/j.1365-2958.2011.07553.x Liu, 2013, Biology of the staphylococcal conjugative multiresistance plasmid pSK41, Plasmid, 70, 42, 10.1016/j.plasmid.2013.02.001 Menard, 2013, Selective pressures to maintain attachment site specificity of integrative and conjugative elements, PLoS Genet., 9, e1003623, 10.1371/journal.pgen.1003623 Navarre, 1999, Surface proteins of Gram-positive bacteria and mechanisms of their targeting to the cell wall envelope, Microbiol. Mol. Biol. Rev., 63, 74, 10.1128/MMBR.63.1.174-229.1999 Ochman, 2000, Lateral gene transfer and the nature of bacterial innovation, Nature, 405, 299, 10.1038/35012500 Olmsted, 1993, High-resolution visualization by field emission scanning electron microscopy of Enterococcus faecalis surface proteins encoded by the pheromone-inducible conjugative plasmid pCF10, J. Bacteriol., 175, 6229, 10.1128/jb.175.19.6229-6237.1993 Olmsted, 1991, Role of the pheromone-inducible surface protein AsclO in mating aggregate formation and conjugal transfer of the Enterococcus faecalis plasmid pCF10, J. Bacteriol., 173, 7665, 10.1128/jb.173.23.7665-7672.1991 Parsons, 2007, TcpA, an FtsK/SpoIIIE homolog, is essential for transfer of the conjugative plasmid pCW3 in Clostridium perfringens, J. Bacteriol., 189, 7782, 10.1128/JB.00783-07 Parsons, 1998, Conjugal transfer of chromosomal DNA in Mycobacterium smegmatis, Mol. Microbiol., 28, 571, 10.1046/j.1365-2958.1998.00818.x Pena, 2012, The hexameric structure of a conjugative VirB4 protein ATPase provides new insights for a functional and phylogenetic relationship with DNA translocases, J. Biol. Chem., 287, 39925, 10.1074/jbc.M112.413849 Pettis, 1996, Plasmid transfer and expression of the transfer (tra) gene product of plasmid pIJ101 are temporally regulated during the Streptomyces lividans life cycle, Mol. Microbiol., 19, 1127, 10.1046/j.1365-2958.1996.493986.x Picardeau, 1998, Mycobacterial linear plasmids have an invertron-like structure related to other linear replicons in actinomycetes, Microbiology, 144, 1981, 10.1099/00221287-144-7-1981 Popowska, 2013, Broad-host-range IncP-1 plasmids and their resistance potential, Front. Microbiol., 4, 10.3389/fmicb.2013.00044 Porter, 2012, The conjugation protein TcpC from Clostridium perfringens is structurally related to the type IV secretion system protein VirB8 from Gram-negative bacteria, Mol. Microbiol., 83, 275, 10.1111/j.1365-2958.2011.07930.x Possoz, 2001, The integrative element pSAM2 from Streptomyces: kinetics and mode of conjugal transfer, Mol. Microbiol., 42, 159, 10.1046/j.1365-2958.2001.02618.x Rabello, 2012, First description of natural and experimental conjugation between mycobacteria mediated by a linear plasmid, PLoS One, 7, e29884, 10.1371/journal.pone.0029884 Ragonese, 2007, The F plasmid-encoded TraM protein stimulates relaxosome-mediated cleavage at oriT through an interaction with TraI, Mol. Microbiol., 63, 1173, 10.1111/j.1365-2958.2006.05576.x Reuther, 2006, Unique conjugation mechanism in mycelial streptomycetes: a DNA-binding ATPase translocates unprocessed plasmid DNA at the hyphal tip, Mol. Microbiol., 61, 436, 10.1111/j.1365-2958.2006.05258.x Reuther, 2006, Modular architecture of the conjugative plasmid pSVH1 from Streptomyces venezuelae, Plasmid, 55, 201, 10.1016/j.plasmid.2005.11.007 Roberts, 2009, A modular master on the move: the Tn916 family of mobile genetic elements, Trends Microbiol., 17, 251, 10.1016/j.tim.2009.03.002 Sepulveda, 2011, A septal chromosome segregator protein evolved into a conjugative DNA-translocator protein, Mob. Genet. Elements, 1, 225, 10.4161/mge.1.3.18066 Servin-Gonzalez, 1995, Sequence and functional analysis of the Streptomyces phaeochromogenes plasmid pJV1 reveals a modular organization of Streptomyces plasmids that replicate by rolling circle, Microbiology, 141, 2499, 10.1099/13500872-141-10-2499 Smits, 2010, The transcriptional regulator Rok binds A+T-rich DNA and is involved in repression of a mobile genetic element in Bacillus subtilis, PLoS Genet., 6, e1001207, 10.1371/journal.pgen.1001207 Staddon, 2006, Genetic characterization of the conjugative DNA processing system of enterococcal plasmid pCF10, Plasmid, 56, 102, 10.1016/j.plasmid.2006.05.001 Steen, 2009, The putative coupling protein TcpA interacts with other pCW3-encoded proteins to form an essential part of the conjugation complex, J. Bacteriol., 191, 2926, 10.1128/JB.00032-09 Tanaka, 1977, Isolation and characterization of four types of plasmids from Bacillus subtilis (natto), J. Bacteriol., 131, 699, 10.1128/JB.131.2.699-701.1977 Teng, 2008, Functional characterization and localization of the TcpH conjugation protein from Clostridium perfringens, J. Bacteriol., 190, 5075, 10.1128/JB.00386-08 Terradot, 2005, Structures of two core subunits of the bacterial type IV secretion system, VirB8 from Brucella suis and ComB10 from Helicobacter pylori, Proc. Natl. Acad. Sci. USA, 102, 4596, 10.1073/pnas.0408927102 Thoma, 2012, Conjugative DNA transfer in Streptomyces, FEMS Microbiol. Lett., 337, 81, 10.1111/1574-6968.12031 Thomas, 2005, Mechanisms of, and barriers to, horizontal gene transfer between bacteria, Nat. Rev. Microbiol., 3, 711, 10.1038/nrmicro1234 Tiffert, 2007, Conjugative DNA transfer in Streptomyces: SpdB2 involved in the intramycelial spreading of plasmid pSVH1 is an oligomeric integral membrane protein that binds to dsDNA, Microbiology, 153, 2976, 10.1099/mic.0.2006/005413-0 Tripathi, 2012, Conjugal transfer of a virulence plasmid in the opportunistic intracellular actinomycete Rhodococcus equi, J. Bacteriol., 194, 6790, 10.1128/JB.01210-12 Tusnady, 2001, The HMMTOP transmembrane topology prediction server, Bioinformatics, 17, 849, 10.1093/bioinformatics/17.9.849 van der Auwera, 2005, Conjugative plasmid pAW63 brings new insights into the genesis of the Bacillus anthracis virulence plasmid pXO2 and of the Bacillus thuringiensis plasmid pBT9727, BMC Genomics, 6, 103, 10.1186/1471-2164-6-103 van der Auwera, 2008, Transcriptional analysis of the conjugative plasmid pAW63 from Bacillus thuringiensis, Plasmid, 60, 190, 10.1016/j.plasmid.2008.07.003 Vecino, 2011, Membrane insertion stabilizes the structure of TrwB, the R388 conjugative plasmid coupling protein, Biochim. Biophys. Acta, Biomembr., 1808, 1032, 10.1016/j.bbamem.2010.12.025 Villamil Giraldo, 2012, Type IV secretion system core component VirB8 from Brucella binds to the globular domain of VirB5 and to a periplasmic domain of VirB6, Biochemistry, 51, 3881, 10.1021/bi300298v Vogelmann, 2011, Conjugal plasmid transfer in Streptomyces resembles bacterial chromosome segregation by FtsK/SpoIIIE, EMBO J., 30, 2246, 10.1038/emboj.2011.121 Wallden, 2010, Microreview: type IV secretion systems: versatility and diversity in function, Cell. Microbiol., 12, 1203, 10.1111/j.1462-5822.2010.01499.x Wallden, 2012, Structure of the VirB4 ATPase, alone and bound to the core complex of a type IV secretion system, Proc. Natl. Acad. Sci. USA, 109, 11348, 10.1073/pnas.1201428109 Wang, 2004, Plasmid DNA transfer in Mycobacterium smegmatis involves novel DNA rearrangements in the recipient, which can be exploited for molecular genetic studies, Mol. Microbiol., 53, 1233, 10.1111/j.1365-2958.2004.04201.x Wang, 2005, Chromosomal DNA transfer in Mycobacterium smegmatis is mechanistically different from classical Hfr chromosomal DNA transfer, Mol. Microbiol., 58, 280, 10.1111/j.1365-2958.2005.04824.x Wang, 2003, Unconventional conjugal DNA transfer in mycobacteria, Nat. Genet., 34, 80, 10.1038/ng1139 Wang, 2010, The tra locus of streptomycete plasmid pIJ101 mediates efficient transfer of a circular but not a linear version of the same replicon, Microbiology, 156, 2723, 10.1099/mic.0.036467-0 Waters, 2001, Analysis of functional domains of the Enterococcus faecalis pheromone-induced surface protein aggregation substance, J. Bacteriol., 183, 5659, 10.1128/JB.183.19.5659-5667.2001 Waters, 2003, The aggregation domain of aggregation substance, not the RGD motifs, is critical for efficient internalization by HT-29 enterocytes, Infect. Immun., 71, 5682, 10.1128/IAI.71.10.5682-5689.2003 Wozniak, 2010, Integrative and conjugative elements: mosaic mobile genetic elements enabling dynamic lateral gene flow, Nat. Rev. Microbiol., 8, 552, 10.1038/nrmicro2382 Xu, 2006, Characterization of the essential gene components for conjugal transfer of Streptomyces lividans linear plasmid SLP2, Prog. Biochem. Biophys., 33, 986 Yang, 2007, TraA is required for megaplasmid conjugation in Rhodococcus erythropolis AN12, Plasmid, 57, 55, 10.1016/j.plasmid.2006.08.002 Zechner, 2012, Assembly and mechanisms of bacterial type IV secretion machines, Philos. Trans. R. Soc. Lond. B Biol. Sci., 367, 1073, 10.1098/rstb.2011.0207 Zhang, 2012, Type-IVC secretion system: a novel subclass of type IV secretion system (T4SS) common existing in Gram-positive genus Streptococcus, PLoS One, 7, e46390, 10.1371/journal.pone.0046390