Advertisement

Mechanisms of Conjugative Transfer and Type IV Secretion-Mediated Effector Transport in Gram-Positive Bacteria

  • Elisabeth Grohmann
  • Walter Keller
  • Günther Muth
Chapter
Part of the Current Topics in Microbiology and Immunology book series (CT MICROBIOLOGY, volume 413)

Abstract

Conjugative DNA transfer is the most important means to transfer antibiotic resistance genes and virulence determinants encoded by plasmids, integrative conjugative elements (ICE), and pathogenicity islands among bacteria. In gram-positive bacteria, there exist two types of conjugative systems, (i) type IV secretion system (T4SS)-dependent ones, like those encoded by the Enterococcus, Streptococcus, Staphylococcus, Bacillus, and Clostridia mobile genetic elements and (ii) T4SS-independent ones, as those found on Streptomyces plasmids. Interestingly, very recently, on the Streptococcus suis genome, the first gram-positive T4SS not only involved in conjugative DNA transfer but also in effector translocation to the host was detected. Although no T4SS core complex structure from gram-positive bacteria is available, several structures from T4SS protein key factors from Enterococcus and Clostridia plasmids have been solved. In this chapter, we summarize the current knowledge on the molecular mechanisms and structure–function relationships of the diverse conjugation machineries and emerging research needs focused on combatting infections and spread of multiple resistant gram-positive pathogens.

Keywords

Conjugative type IV secretion Plasmid Integrative conjugative element Pathogenicity island Antibiotic resistance 

Notes

Acknowledgements

E. G. thanks the German Aerospace Center (DLR) for funding (grant 50WB1466). G. M. thanks the DFG (SFB-766) for financial support. Funding by the Austrian Science Foundation (FWF) under project number P27383 to W. K. is acknowledged. We apologize that not all valuable contributions of our colleagues to the topic could be included due to limitations of space.

References

  1. Abajy MY, Kopeć J, Schiwon K, Burzynski M, Döring M, Bohn C, Grohmann E (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(6):2487–2496CrossRefGoogle Scholar
  2. Alvarez-Martinez CE, Christie PJ (2009) Biological diversity of prokaryotic type IV secretion systems. Microbiol Mol Biol Rev 73:775–808CrossRefGoogle Scholar
  3. Arends K (2010) Entwicklung von gfp-basierten Monitoring Tools zur Verfolgung von horizontalem Gentransfer und Studien zum T4SLS des konjugativen Plasmids pIP501 aus Enterococcus faecalis. PhD thesis, Technical University Berlin, GermanyGoogle Scholar
  4. Arends K, Celik EK, Probst I, Goessweiner-Mohr N, Fercher C, Grumet L, Soellue C, Abajy MY, Sakinc T, Broszat M, Schiwon K, Koraimann G, Keller W, Grohmann E (2013) TraG encoded by the pIP501 type IV secretion system is a two-domain peptidoglycan-degrading enzyme essential for conjugative transfer. J Bacteriol 195(19):4436–4444.  https://doi.org/10.1128/JB.02263-12CrossRefPubMedPubMedCentralGoogle Scholar
  5. Auchtung JM, Lee CA, Monson RE, Lehman AP, Grossman AD (2005) Regulation of a Bacillus subtilis mobile genetic element by intercellular signaling and the global DNA damage response. Proc Natl Acad Sci U S A 102(35):12554–12559CrossRefGoogle Scholar
  6. Auchtung JM, Lee CA, Garrison KL, Grossman AD (2007) Identification and characterization of the immunity repressor (ImmR) that controls the mobile genetic element ICEBs1 of Bacillus subtilis. Mol Microbiol 64(6):1515–1528CrossRefGoogle Scholar
  7. Auchtung JM, Aleksanyan N, Bulku A, Berkmen MB (2016) Biology of ICEBs1, an integrative and conjugative element in Bacillus subtilis. Plasmid 86:14–25.  https://doi.org/10.1016/j.plasmid.2016.07.001CrossRefPubMedPubMedCentralGoogle Scholar
  8. Bailey S, Ward D, Middleton R, Grossmann JG, Zambryski PC (2006) Agrobacterium tumefaciens VirB8 structure reveals potential protein-protein interaction sites. Proc Natl Acad Sci U S A 103:2582–2587.  https://doi.org/10.1073/pnas.0511216103CrossRefGoogle Scholar
  9. Bannam TL, Teng WL, Bulach D, Lyras D, Rood JI (2006) Functional identification of conjugation and replication regions of the tetracycline resistance plasmid pCW3 from Clostridium perfringens. J Bacteriol 188(13):4942–4951.  https://doi.org/10.1128/JB.00298-06CrossRefPubMedPubMedCentralGoogle Scholar
  10. Bantwal R, Bannam TL, Porter CJ, Quinsey NS, Lyras D, Adams V, Rood JI (2012) The peptidoglycan hydrolase TcpG is required for efficient conjugative transfer of pCW3 in Clostridium perfringens. Plasmid 67(2):139–147.  https://doi.org/10.1016/j.plasmid.2011.12.016CrossRefPubMedGoogle Scholar
  11. Baron C (2006) VirB8: a conserved type IV secretion system assembly factor and drug target. Biochem Cell Biol 84:890–899.  https://doi.org/10.1139/o06-148
  12. Bauer T, Rösch T, Itaya M, Graumann PL (2011) Localization pattern of conjugation machinery in a Gram-positive bacterium. J Bacteriol 193(22):6244–6256.  https://doi.org/10.1128/JB.00175-11CrossRefPubMedPubMedCentralGoogle Scholar
  13. Berger BR, Christie PJ (1993) The Agrobacterium tumefaciens virB4 gene product is an essential virulence protein requiring an intact nucleoside triphosphate-binding domain. J Bacteriol 175(6):1723–1734CrossRefGoogle Scholar
  14. Berkmen MB, Lee CA, Loveday EK, Grossman AD (2010) Polar positioning of a conjugation protein from the integrative and conjugative element ICEBs1 of Bacillus subtilis. J Bacteriol 192(1):38–45.  https://doi.org/10.1128/JB.00860-09CrossRefPubMedGoogle Scholar
  15. Bhatty M, Laverde Gomez JA, Christie PJ (2013) The expanding bacterial type IV secretion lexicon. Res Microbiol 164(6):620–639.  https://doi.org/10.1016/j.resmic.2013.03.012CrossRefPubMedGoogle Scholar
  16. Bhatty M, Cruz MR, Frank KL, Gomez JA, Andrade F, Garsin DA, Dunny GM, Kaplan HB, Christie PJ (2015) Enterococcus faecalis pCF10-encoded surface proteins PrgA, PrgB (aggregation substance) and PrgC contribute to plasmid transfer, biofilm formation and virulence. Mol Microbiol 95:660–677CrossRefGoogle Scholar
  17. Bibb MJ, Hopwood DA (1981) Genetic studies of the fertility plasmid SCP2 and its SCP2* variants in Streptomyces coelicolor A3(2). J Gen Microbiol 126:427–442Google Scholar
  18. Bibb MJ, Ward JM, Hopwood DA (1978) Transformation of plasmid DNA into Streptomyces at high frequency. Nature 274:398–400CrossRefGoogle Scholar
  19. Bibb MJ, Ward JM, Kieser T, Cohen SN, Hopwood DA (1981) Excision of chromosomal DNA sequences from Streptomyces coelicolor forms a novel family of plasmids detectable in Streptomyces lividans. Mol Gen Genet 184:230–240PubMedGoogle Scholar
  20. Bose B, Auchtung JM, Lee CA, Grossman AD (2008) A conserved anti-repressor controls horizontal gene transfer by proteolysis. Mol Microbiol 70(3):570–582.  https://doi.org/10.1111/j.1365-2958.2008.06414CrossRefPubMedPubMedCentralGoogle Scholar
  21. Bottacini F, O’Connell Motherway M, Casey E, McDonnell B, Mahony J, Ventura M, van Sinderen D (2015) Discovery of a conjugative megaplasmid in Bifidobacterium breve. Appl Environ Microbiol 81:166–176CrossRefGoogle Scholar
  22. Chandran V, Fronzes R, Duquerroy S, Cronin N, Navaza J, Waksman G (2009) Structure of the outer membrane complex of a type IV secretion system. Nature 462(7276):1011–1015.  https://doi.org/10.1038/nature08588CrossRefPubMedPubMedCentralGoogle Scholar
  23. Chen CW, Yu T-W, Lin Y-S, Kieser HM, Hopwood DA (1993) The conjugative plasmid SLP2 of Streptomyces lividans is a 50 kb linear molecule. Mol Microbiol 7(6):925–932.  https://doi.org/10.1111/j.1365-2958.1993.tb01183.xCrossRefPubMedGoogle Scholar
  24. Chen Y, Zhang X, Manias D, Yeo HJ, Dunny GM, Christie PJ (2008) Enterococcus faecalis PcfC, a spatially localized substrate receptor for type IV secretion of the pCF10 transfer intermediate. J Bacteriol 190(10):3632–3645CrossRefGoogle Scholar
  25. Chen Y, Bandyopadhyay A, Kozlowicz BK, Haemig HAH, Tai A, Hu WS, Dunny GM (2017) Mechanisms of peptide sex pheromone regulation of conjugation in Enterococcus faecalis. MicrobiologyOpen 6(4):e00492.  https://doi.org/10.1002/mbo3.492CrossRefPubMedCentralGoogle Scholar
  26. De-Donatis G, Zhao Z, Wang S, Huang LP, Schwartz C, Tsodikov OV, Zhang H, Haque F, Guo P (2014) Finding of widespread viral and bacterial revolution dsDNA translocation motors distinct from rotation motors by channel chirality and size. Cell Bioscience 4(1):30.  https://doi.org/10.1186/2045-3701-4-30CrossRefPubMedPubMedCentralGoogle Scholar
  27. Derbyshire KM, Gray TA (2014) Distributive conjugal transfer: new insights into horizontal gene transfer and genetic exchange in mycobacteria. Microbiology Spectrum 2(1).  https://doi.org/10.1128/microbiolspec.mgm2-0022-2013
  28. DeWitt T, Grossman AD (2014) The bifunctional cell wall hydrolase CwlT is needed for conjugation of the integrative and conjugative ICEBs1 in Bacillus subtilis and B. anthracis. J Bacteriol 196(8):1588–1596.  https://doi.org/10.1128/JB.00012-14CrossRefPubMedPubMedCentralGoogle Scholar
  29. Ducote MJ, Pettis GS (2006) An in vivo assay for conjugation-mediated recombination yields novel results for Streptomyces plasmid pIJ101. Plasmid 55(3):242–248.  https://doi.org/10.1016/j.plasmid.2005.11.002CrossRefPubMedGoogle Scholar
  30. Dunny GM, Berntsson RP (2016) Enterococcal sex pheromones: evolutionary pathways to complex, two-signal systems. J Bacteriol 198(11):1556–1562.  https://doi.org/10.1128/JB.00128-16CrossRefPubMedPubMedCentralGoogle Scholar
  31. Fercher C, Keller W, Zangger K, Meyer NH (2016a) 1H, 15N and 13C chemical shift assignment of the Gram-positive conjugative transfer protein TraHpIP501. Biomol NMR Assign 10(1):163–166.  https://doi.org/10.1007/s12104-015-9658-3CrossRefPubMedGoogle Scholar
  32. Fercher C, Probst I, Kohler V, Goessweiner-Mohr N, Arends K, Grohmann E, Zangger K, Meyer NH, Keller W (2016b) VirB8-like protein TraH is crucial for DNA transfer in Enterococcus faecalis. Sci Rep 624643.  https://doi.org/10.1038/srep24643
  33. Flärdh K (2010) Cell polarity and the control of apical growth in Streptomyces. Curr Opin Microbiol 13(6):758–765.  https://doi.org/10.1016/j.mib.2010.10.002CrossRefPubMedGoogle Scholar
  34. Fronzes R, Schafer E, Wang L, Saibil HR, Orlova EV, Waksman G (2009) Structure of a type IV secretion system core complex. Science 323(5911):266–268.  https://doi.org/10.1126/science.1166101CrossRefPubMedGoogle Scholar
  35. Fullner KJ, Lara JC, Nester EW (1996) Pilus assembly by Agrobacterium T-DNA transfer genes. Science 273(5278):1107–1109CrossRefGoogle Scholar
  36. Ghinet MG, Bordeleau E, Beaudin J, Brzezinski R, Roy S, Burrus V (2011) Uncovering the prevalence and diversity of integrating conjugative elements in actinobacteria. PLoS ONE 6(11):e27846.  https://doi.org/10.1371/journal.pone.0027846CrossRefPubMedPubMedCentralGoogle Scholar
  37. Goessweiner-Mohr N, Fercher C, Abajy MY, Grohmann E, Keller W (2012) Crystallization and first data collection of the putative transfer protein TraN from the Gram-positive conjugative plasmid pIP501. Acta Crystallogr, Sect F: Struct Biol Cryst Commun 68(11):1402–1405.  https://doi.org/10.1107/S174430911204184XCrossRefGoogle Scholar
  38. Goessweiner-Mohr N, Arends K, Keller W, Grohmann E (2013a) Conjugative type IV secretion in Gram-positive bacteria. Plasmid 70(3):289–302CrossRefGoogle Scholar
  39. Goessweiner-Mohr N, Grumet L, Arends K, Pavkov-Keller T, Gruber C, Birner-Gruenberger R, Kropec-Huebner A, Huebner J, Grohmann E, Keller W (2013b) The 2.5 Å structure of the Enterococcus conjugation protein TraM resembles VirB8 type IV secretion proteins. J Biol Chem 288(3):2018–2028CrossRefGoogle Scholar
  40. Goessweiner-Mohr N, Arends K, Keller W, Grohmann E (2014a) Conjugation in Gram-positive bacteria. Microbiol Spectrum 2(4):PLAS-0004-2013.  https://doi.org/10.1128/microbiolspec
  41. Goessweiner-Mohr N, Eder M, Hofer G, Fercher C, Arends K, Birner-Gruenberger R, Grohmann E, Keller W (2014b) Structure of the double-stranded DNA-binding type IV secretion protein TraN from Enterococcus. Acta Crystallogr D Biol Crystallogr 70(Pt 9):2376–2389.  https://doi.org/10.1107/S1399004714014187CrossRefPubMedGoogle Scholar
  42. Goessweiner-Mohr N, Fercher C, Arends K, Birner-Gruenberger D, Laverde-Gomez D, Huebner J, Grohmann E, Keller W (2014c) The type IV secretion protein TraK from the Enterococcus conjugative plasmid pIP501 exhibits a novel fold. Acta Cryst Section D 70(4):1124–1135.  https://doi.org/10.1107/S1399004714001606CrossRefGoogle Scholar
  43. Gomis-Rüth FX, Moncalián G, Pérez-Luque R, González A, Cabezón E, de la Cruz F, Coll M (2001) The bacterial conjugation protein TrwB resembles ring helicases and F1-ATPase. Nature 409(6820):637–641.  https://doi.org/10.1038/35054586CrossRefPubMedGoogle Scholar
  44. Gonzalez-Rivera C, Bhatty M, Christie PJ (2016) Mechanism and function of type IV secretion during infection of the human host. Microbiol Spectr 4(3).  https://doi.org/10.1128/microbiolspec.vmbf-0024-2015
  45. Goranov AI, Kuester-Schoeck E, Wang JD, Grossman AD (2006) Characterization of the global transcriptional responses to different types of DNA damage and disruption of replication in Bacillus subtilis. J Bacteriol 188(15):5595–5605CrossRefGoogle Scholar
  46. Gray TA, Clark RR, Boucher N, Lapierre P, Smith C, Derbyshire KM (2016) Intercellular communication and conjugation are mediated by ESX secretion systems in mycobacteria. Science 354(6310):347–350.  https://doi.org/10.1126/science.aag0828CrossRefPubMedPubMedCentralGoogle Scholar
  47. Grohmann E, Muth G, Espinosa M (2003) Conjugative plasmid transfer in gram-positive bacteria. Microbiol Mol Biol Rev 67:277–301CrossRefGoogle Scholar
  48. Grohmann E, Goessweiner-Mohr N, Brantl S (2016) DNA-binding proteins regulating pIP501 transfer and replication. Front Mol Biosci 11(8):2016.  https://doi.org/10.3389/fmolb.2016.00042CrossRefGoogle Scholar
  49. Grohmann E, Christie PJ, Waksman G, Backert S (2018) Type IV secretion in Gram-negative and Gram-positive bacteria. Mol Microbiol 107:455–471  https://doi.org/10.1111/mmi.13896CrossRefPubMedPubMedCentralGoogle Scholar
  50. Guo P, Noji H, Yengo CM, Zhao Z, Grainge I (2016) Biological nanomotors with a revolution, linear, or rotation motion mechanism. Microbiol Mol Biol Rev 80(1):161–186.  https://doi.org/10.1128/MMBR.00056-15CrossRefPubMedPubMedCentralGoogle Scholar
  51. Hagège J, Pernodet JL, Sezonov G, Gerbaud C, Friedmann A, Guérineau M (1993) Transfer functions of the conjugative integrating element pSAM2 from Streptomyces ambofaciens: characterization of a kil-kor system associated with transfer. J Bacteriol 175(17):5529–5538.  https://doi.org/10.1128/jb.175.17.5529-5538.1993CrossRefPubMedPubMedCentralGoogle Scholar
  52. Haug I, Weissenborn A, Brolle D, Bentley S, Kieser T, Altenbuchner J (2003) Streptomyces coelicolor A3(2) plasmid SCP2*: deductions from the complete sequence. Microbiology 149(2):505–513.  https://doi.org/10.1099/mic.0.25751-0CrossRefPubMedGoogle Scholar
  53. Hopwood DA, Kieser T (1993) Conjugative plasmids of Streptomyces. In: Clewell DB (ed) Bacterial conjugation. Plenum Press, New York, pp 293–311CrossRefGoogle Scholar
  54. Ilangovan A, Connery S, Waksman G (2015) Structural biology of the Gram-negative bacterial conjugation systems. Trends Microbiol 23(5):301–310.  https://doi.org/10.1016/j.tim.2015.02.01CrossRefPubMedGoogle Scholar
  55. Jiang X, Yang Y, Zhou J, Zhu L, Gu Y, Zhang X, Li X, Fang W (2016) Roles of the putative type IV-like secretion system key component VirD4 and PrsA in pathogenesis of Streptococcus suis type 2. Front Cell Infect Microbiol 6:172PubMedPubMedCentralGoogle Scholar
  56. Johnson CM, Grossman AD (2015) Integrative and conjugative elements (ICEs): what they do and how they work. Annu Rev Genet 49:577–601.  https://doi.org/10.1146/annurev-genet-112414-055018CrossRefPubMedPubMedCentralGoogle Scholar
  57. Johnson CM, Grossman AD (2016) The composition of the cell envelope affects conjugation in Bacillus subtilis. J Bacteriol 198(8):1241–1249.  https://doi.org/10.1128/JB.01044-15CrossRefPubMedPubMedCentralGoogle Scholar
  58. Jung CM, Crocker FH, Eberly JO, Indest KJ (2011) Horizontal gene transfer (HGT) as a mechanism of disseminating RDX-degrading activity among Actinomycete bacteria. J Appl Microbiol 110(6):1449–1459.  https://doi.org/10.1111/j.1365-2672.2011.04995.xCrossRefPubMedGoogle Scholar
  59. Kataoka M, Seki T, Yoshida T (1991) Five genes involved in self-transmission of pSN22, a Streptomyces plasmid. J Bacteriol 173(13):4220–4228.  https://doi.org/10.1128/jb.173.13.4220-4228.1991CrossRefPubMedPubMedCentralGoogle Scholar
  60. Kendall KJ, Cohen SN (1987) Plasmid transfer in Streptomyces lividans: identification of a kil-kor system associated with the transfer region of pIJ101. J Bacteriol 169(9):4177–4183.  https://doi.org/10.1128/jb.169.9.4177-4183.1987CrossRefPubMedPubMedCentralGoogle Scholar
  61. Kieser T, Hopwood DA, Wright HM, Thompson CJ (1982) pIJ101, a multi-copy broad host-range Streptomyces plasmid: functional analysis and development of DNA cloning vectors. Mol Gen Genet 185(2):223–238.  https://doi.org/10.1007/bf00330791CrossRefPubMedGoogle Scholar
  62. Kinashi H, Shimaji M, Sakai A (1987) Giant linear plasmids in Streptomyces which code for antibiotic biosynthesis genes. Nature 328(6129):454–456.  https://doi.org/10.1038/328454a0CrossRefPubMedGoogle Scholar
  63. Kohler V, Probst I, Aufschnaiter A, Büttner S, Schaden L, Rechberger GN, Koraimann G, Grohmann E, Keller W (2017) Conjugative type IV secretion in Gram-positive pathogens: TraG, a lytic transglycosylase and endopeptidase, interacts with translocation channel protein TraM. Plasmid 91:9–18.  https://doi.org/10.1016/j.plasmid.2017.02.002CrossRefPubMedGoogle Scholar
  64. Kopeć J, Bergmann A, Fritz G, Grohmann E, Keller W (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(2):401–409CrossRefGoogle Scholar
  65. Kosono S, Kataoka M, Seki T, Yoshida T (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(2):397–405.  https://doi.org/10.1046/j.1365-2958.1996.379909.xCrossRefPubMedGoogle Scholar
  66. Kumar RB, Xie YH, Das A (2000) Subcellular localization of the Agrobacterium tumefaciens T-DNA transport pore proteins: VirB8 is essential for the assembly of the transport pore. Mol Microbiol 36:608–617.  https://doi.org/10.1046/j.1365-2958.2000.01876.x CrossRefGoogle Scholar
  67. Kurenbach B, Bohn C, Prabhu J, Abudukerim M, Grohmann E (2003) Intergeneric transfer of the Enterococcus faecalis plasmid pIP501 to Escherichia coli and Streptomyces lividans and sequence analysis of its tra region. Plasmid 50:86–93CrossRefGoogle Scholar
  68. Kurenbach B, Kopec J, Magdefrau M, Andreas K, Keller W, Bohn C, Abajy MY, Grohmann E (2006) The TraA relaxase autoregulates the putative type IV secretion-like system encoded by the broad-host-range Streptococcus agalactiae plasmid pIP501. Microbiology 152(3):637–645.  https://doi.org/10.1099/mic.0.28468-0CrossRefPubMedGoogle Scholar
  69. Laverde Gomez JA, Bhatty M, Christie PJ (2014) PrgK, a multidomain peptidoglycan hydrolase, is essential for conjugative transfer of the pheromone-responsive plasmid pCF10. J Bacteriol 196:527–539CrossRefGoogle Scholar
  70. Laverde D, Probst I, Romero-Saavedra F, Kropec A, Wobser D, Keller W, Grohmann E, Huebner J (2017) Targeting type IV secretion system proteins to combat multiresistant Gram-positive pathogens. J Infect Dis 215:1836–1845CrossRefGoogle Scholar
  71. Lederberg J, Tatum EL (1946) Gene recombination in Escherichia coli. Nature 158:558CrossRefGoogle Scholar
  72. Lee CA, Auchtung JM, Monson RE, Grossman AD (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(6):1356–1369PubMedGoogle Scholar
  73. Lee CA, Thomas J, Grossman AD (2012) The Bacillus subtilis conjugative transposon ICEBs1 mobilizes plasmids lacking dedicated mobilization functions. J Bacteriol 194(12):3165–3172.  https://doi.org/10.1128/JB.00301-12CrossRefPubMedPubMedCentralGoogle Scholar
  74. Leonetti CT, Hamada MA, Laurer SJ, Broulidakis MP, Swerdlow KJ, Lee CA, Grossman AD, Berkmen MB (2015) Critical components of the conjugation machinery of the integrative and conjugative element ICEBs1 of Bacillus subtilis. J Bacteriol 197(15):2558–2567.  https://doi.org/10.1128/JB.00142-15CrossRefPubMedPubMedCentralGoogle Scholar
  75. Li M, Shen X, Yan J, Han H, Zheng B, Liu D, Cheng H, Zhao Y, Rao X, Wang C, Tang J, Hu F, Gao GF (2011) GI-type T4SS-mediated horizontal transfer of the 89 K pathogenicity island in epidemic Streptococcus suis serotype 2. Mol Microbiol 79(6):1670–1683.  https://doi.org/10.1111/j.1365-2958.2011.07553.xCrossRefPubMedPubMedCentralGoogle Scholar
  76. Li F, Alvarez-Martinez C, Chen Y, Choi KJ, Yeo HJ, Christie PJ (2012) Enterococcus faecalis PrgJ, a VirB4-like ATPase, mediates pCF10 conjugative transfer through substrate binding. J Bacteriol 194(15):4041–4051.  https://doi.org/10.1128/JB.00648-12CrossRefPubMedPubMedCentralGoogle Scholar
  77. Liu MA, Kwong SM, Jensen SO, Brzoska AJ, Firth N (2013) Biology of the staphylococcal conjugative multiresistance plasmid pSK41. Plasmid 70(1):42–51.  https://doi.org/10.1016/j.plasmid.2013.02.001CrossRefPubMedGoogle Scholar
  78. Low HH, Gubellini F, Rivera-Calzada A, Braun N, Connery S, Dujeancourt A, Lu F, Redzej A, Fronzes R, Orlova EV, Waksman G (2014) Structure of a type IV secretion system. Nature 508(7497):550–553.  https://doi.org/10.1038/nature13081CrossRefPubMedPubMedCentralGoogle Scholar
  79. Massey TH, Mercogliano CP, Yates J, Sherratt DJ, Lowe J (2006) Double-stranded DNA translocation: structure and mechanism of hexameric FtsK. Mol Cell 23(4):457–469.  https://doi.org/10.1016/j.molcel.2006.06.019CrossRefPubMedGoogle Scholar
  80. Menard KL, Grossman AD (2013) Selective pressures to maintain attachment site specificity of integrative and conjugative elements. PLoS Genet 9(7):e1003623.  https://doi.org/10.1371/journal.pgen.1003623CrossRefPubMedPubMedCentralGoogle Scholar
  81. Pena A, Matilla I, Martin-Benito J, Valpuesta JM, Carrascosa JL, de la Cruz F, Cabezon E, Arechaga I (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(47):39925–39932.  https://doi.org/10.1074/jbc.M112.413849CrossRefPubMedPubMedCentralGoogle Scholar
  82. Pernodet J-L, Simonet J-M, Guérineau M (1984) Plasmids in different strains of Streptomyces ambofaciens: free and integrated form of plasmid pSAM2. Mol Gen Genet 198(1):35–41.  https://doi.org/10.1007/bf00328697CrossRefPubMedGoogle Scholar
  83. Pettis GS, Cohen SN (1994) Transfer of the plJ101 plasmid in Streptomyces lividans requires a cis-acting function dispensable for chromosomal gene transfer. Mol Microbiol 13(6):955–964.  https://doi.org/10.1111/j.1365-2958.1994.tb00487.xCrossRefPubMedGoogle Scholar
  84. Porter CJ, Bantwal R, Bannam TL, Rosado CJ, Pearce MC, Adams V, Lyras D, Whisstock JC, Rood JI (2012) The conjugation protein TcpC from Clostridium perfringens is structurally related to the type IV secretion system protein VirB8 from Gram-negative bacteria. 83(2):275–288.  https://doi.org/10.1111/j.1365-2958.2011.07930.x
  85. Possoz C, Ribard C, Gagnat J, Pernodet J-L, Guérineau M (2001) The integrative element pSAM2 from Streptomyces: kinetics and mode of conjugal transfer. Mol Microbiol 42(1):159–166.  https://doi.org/10.1046/j.1365-2958.2001.02618.xCrossRefPubMedGoogle Scholar
  86. Ramachandran G, Singh PK, Luque-Ortega JR, Yuste L, Alfonso C, Rojo F, Wu LJ, Meijer WJ (2014) A complex genetic switch involving overlapping divergent promoters and DNA looping regulates expression of conjugation genes of a gram-positive plasmid. PLoS Genet 10(10):e1004733.  https://doi.org/10.1371/journal.pgen.1004733CrossRefPubMedPubMedCentralGoogle Scholar
  87. Ramsay JP, Kwong SM, Murphy RJ, Yui Eto K, Price KJ, Nguyen QT, O’Brien FG, Grubb WB, Coombs GW, Firth N (2016) An updated view of plasmid conjugation and mobilization in Staphylococcus. Mob Genet Elements 6(4):e1208317.  https://doi.org/10.1080/2159256X.2016.1208317CrossRefPubMedPubMedCentralGoogle Scholar
  88. Reimmann C, Haas D (1993) Mobilization of chromosomes and nonconjugative plasmids by cointegrative mechanisms. In: Clewell D (ed) Bacterial conjugation. Plenum Press, New York, pp 137–188CrossRefGoogle Scholar
  89. Reuther J, Gekeler C, Tiffert Y, Wohlleben W, Muth G (2006a) Unique conjugation mechanism in mycelial streptomycetes: a DNA-binding ATPase translocates unprocessed plasmid DNA at the hyphal tip. Mol Microbiol 61(2):436–446.  https://doi.org/10.1111/j.1365-2958.2006.05258.xCrossRefPubMedGoogle Scholar
  90. Reuther J, Wohlleben W, Muth G (2006b) Modular architecture of the conjugative plasmid pSVH1 from Streptomyces venezuelae. Plasmid 55(3):201–209.  https://doi.org/10.1016/j.plasmid.2005.11.007CrossRefPubMedGoogle Scholar
  91. Rösch TC, Graumann PL (2015) Induction of plasmid conjugation in Bacillus subtilis is bistable and driven by a direct interaction of a Rap/Phr Quorum-sensing system with a master repressor. J Biol Chem 290(33):20221–20232.  https://doi.org/10.1074/jbc.M115.664110CrossRefPubMedPubMedCentralGoogle Scholar
  92. Rösch TC, Golman W, Hucklesby L, Gonzalez-Pastor JE, Graumann PL (2014) The presence of conjugative plasmid pLS20 affects global transcription of its Bacillus subtilis host and confers beneficial stress resistance to cells. Appl Environ Microbiol 80(4):1349–1358.  https://doi.org/10.1128/AEM.03154-13CrossRefPubMedPubMedCentralGoogle Scholar
  93. Schlievert PM, Gahr PJ, Assimacopoulos AP, Dinges MM, Stoehr JA, Harmala JW, Hirt H, Dunny GM (1998) Aggregation and binding substances enhance pathogenicity in rabbit models of Enterococcus faecalis endocarditis. Infect Immun 66:218–223PubMedPubMedCentralGoogle Scholar
  94. Sepulveda E, Vogelmann J, Muth G (2011) A septal chromosome segregator protein evolved into a conjugative DNA-translocator protein. Mobile Genetic Elements 1(3):225–229.  https://doi.org/10.4161/mge.1.3.18066CrossRefPubMedPubMedCentralGoogle Scholar
  95. Sermonti G, Spada-Sermonti I (1955) Genetic recombination in Streptomyces. Nature 176(4472):121.  https://doi.org/10.1038/176121a0CrossRefPubMedGoogle Scholar
  96. Servín-González L (1996) Identification and properties of a novel clt locus in the Streptomyces phaeochromogenes plasmid pJV1. J Bacteriol 178(14):4323–4326.  https://doi.org/10.1128/jb.178.14.4323-4326.1996CrossRefPubMedPubMedCentralGoogle Scholar
  97. Servin-Gonzalez L, Sampieri A, Cabello J, Galvan L, Juarez V, Castro C (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(10):2499–2510.  https://doi.org/10.1099/13500872-141-10-2499CrossRefPubMedGoogle Scholar
  98. Singh PK, Meijer WJ (2014) Diverse regulatory circuits for transfer of conjugative elements. FEMS Microbiol Lett 358(2):119–128.  https://doi.org/10.1111/1574-6968.12526CrossRefPubMedGoogle Scholar
  99. Singh PK, Ramachandran G, Ramos-Ruiz R, Peiró-Pastor R, Abia D, Wu LJ, Meijer WJ (2013) Mobility of the native conjugative plasmid pLS20 is regulated by intercellular signaling. PLoS Genet 9(10):e1003892.  https://doi.org/10.1371/journal.pgen.1003892CrossRefPubMedPubMedCentralGoogle Scholar
  100. Tauch A, Götker S, Pühler A, Kalinowski J, Thierbach G (2002) The 27.8-kb R-plasmid pTET3 from Corynebacterium glutamicum encodes the aminoglycoside adenyltransferase gene cassette aadA9 and the regulated tetracycline efflux system Tet 33 flanked by active copies of the widespread insertion sequence IS6100. Plasmid 48(2):117–129.  https://doi.org/10.1016/s0147-619x(02)00120-8CrossRefPubMedGoogle Scholar
  101. Tauch A, Bischoff N, Brune I, Kalinowski J (2003) Insights into the genetic organization of the Corynebacterium diphtheriae erythromycin resistance plasmid pNG2 deduced from its complete nucleotide sequence. Plasmid 49(1):63–74.  https://doi.org/10.1016/s0147-619x(02)00115-4CrossRefPubMedGoogle Scholar
  102. Teng WL, Bannam TL, Parsons JA, Rood JI (2008) Functional characterization and localization of the TcpH conjugation protein from Clostridium perfringens. J Bacteriol 190(14):5075–5086CrossRefGoogle Scholar
  103. Terradot L, Bayliss R, Oomen C, Leonard GA, Baron C, Waksman G (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 U S A 102:4596–4601.  https://doi.org/10.1073/pnas.0408927102CrossRefGoogle Scholar
  104. te Poele EM, Bolhuis H, Dijkhuizen L (2008) Actinomycete integrative and conjugative elements. Antonie Van Leeuwenhoek 94(1):127–143.  https://doi.org/10.1007/s10482-008-9255-xCrossRefGoogle Scholar
  105. Thoma L, Muth G (2015) The conjugative DNA-transfer apparatus of Streptomyces. Int J Med Microbiol 305(2):224–229.  https://doi.org/10.1016/j.ijmm.2014.12.020CrossRefPubMedGoogle Scholar
  106. Thoma L, Dobrowinski H, Finger C, Guezguez J, Linke D, Sepulveda E, Muth G (2015) A multi-protein DNA-translocation complex directs intramycelial plasmid spreading during Streptomyces conjugation. mBio 6(3):e02559–e02514.  https://doi.org/10.1128/mbio.02559-14CrossRefGoogle Scholar
  107. Thoma L, Vollmer B, Muth G (2015b) Fluorescence microscopy of Streptomyces conjugation suggests DNA-transfer at the lateral walls and reveals the spreading of the plasmid in the recipient mycelium. Environ Microbiol 18(2):598–608.  https://doi.org/10.1111/1462-2920.13027CrossRefPubMedGoogle Scholar
  108. Tripathi VN, Harding WC, Willingham-Lane JM, Hondalus MK (2012) Conjugal transfer of a virulence plasmid in the opportunistic intracellular actinomycete Rhodococcus equi. J Bacteriol 194(24):6790–6801.  https://doi.org/10.1128/jb.01210-12CrossRefPubMedPubMedCentralGoogle Scholar
  109. Trokter M, Felisberto-Rodrigues C, Christie PJ, Waksman G (2014) Recent advances in the structural and molecular biology of type IV secretion systems. Curr Opin Struct Biol 2716–2723.  https://doi.org/10.1016/j.sbi.2014.02.006
  110. Ummels R, Abdallah AM, Kuiper V, Aajoud A, Sparrius M, Naeem R, Spaink HP, van Soolingen D, Pain A, Bitter W (2014) Identification of a novel conjugative plasmid in mycobacteria that requires both type IV and type VII secretion. mBio 5(5):e01744-01714.  https://doi.org/10.1128/mbio.01744-14CrossRefGoogle Scholar
  111. Vogelmann J, Ammelburg M, Finger C, Guezguez J, Linke D, Flötenmeyer M, Stierhof Y-D, Wohlleben W, Muth G (2011) Conjugal plasmid transfer in Streptomyces resembles bacterial chromosome segregation by FtsK/SpoIIIE. EMBO J 30(11):2246–2254.  https://doi.org/10.1038/emboj.2011.121CrossRefPubMedPubMedCentralGoogle Scholar
  112. Wallden K, Rivera-Calzada A, Waksman G (2010) Type IV secretion systems: versatility and diversity in function. Cell Microbiol 12(9):1203–1212.  https://doi.org/10.1111/j.1462-5822.2010.01499.xCrossRefPubMedPubMedCentralGoogle Scholar
  113. Wallden K, Williams R, Yan J, Lian PW, Wang L, Thalassinos K, Orlova EV, Waksman G (2012) Structure of the VirB4 ATPase, alone and bound to the core complex of a type IV secretion system. Proc Natl Acad Sci U S A 109(28):11348–11353.  https://doi.org/10.1073/pnas.1201428109CrossRefPubMedPubMedCentralGoogle Scholar
  114. Wang J, Feng Y, Wang C, Srinivas S, Chen C, Liao H, He E, Jiang S, Tang J (2017) Pathogenic Streptococcus strains employ novel escape strategy to inhibit bacteriostatic effect mediated by mammalian peptidoglycan recognition protein. Cell Microbiol 19(7).  https://doi.org/10.1111/cmi.12724CrossRefGoogle Scholar
  115. Watarai M, Makino S, Shirahata T (2002) An essential virulence protein of Brucella abortus, VirB4, requires an intact nucleoside-triphosphate-binding domain. Microbiology 148(5):1439–1446.  https://doi.org/10.1099/00221287-148-5-1439CrossRefPubMedGoogle Scholar
  116. Wisniewski JA, Rood JI (2017) The Tcp conjugation system of Clostridium perfringens. Plasmid 91:28–36.  https://doi.org/10.1016/j.plasmid.2017.03.001CrossRefPubMedGoogle Scholar
  117. Wisniewski JA, Traore DA, Bannam TL, Lyras D, Whisstock JC, Rood JI (2016) TcpM: a novel relaxase that mediates transfer of large conjugative plasmids from Clostridium perfringens. Mol Microbiol 99(5):884–896.  https://doi.org/10.1111/mmi.13270CrossRefPubMedGoogle Scholar
  118. Yang JC, Lessard PA, Sengupta N, Windsor SD, O’Brien XM, Bramucci M, Tomb J-F, Nagarajan V, Sinskey AJ (2007) TraA is required for megaplasmid conjugation in Rhodococcus erythropolis AN12. Plasmid 57(1):55–70.  https://doi.org/10.1016/j.plasmid.2006.08.00CrossRefPubMedGoogle Scholar
  119. Yin S, Li M, Rao X, Yao X, Zhong Q, Wang M, Wang J, Peng Y, Tang J, Hu F, Zhao Y (2016) Subtilisin-like protease-1 secreted through type IV secretion system contributes to high virulence of Streptococcus suis 2. Sci Rep 6:27369.  https://doi.org/10.1038/srep27369CrossRefPubMedPubMedCentralGoogle Scholar
  120. Zechner EL, Pruger H, Grohmann E, Espinosa M, Hogenauer G (1997) Specific cleavage of chromosomal and plasmid DNA strands in gram-positive and gram-negative bacteria can be detected with nucleotide resolution. Proc Natl Acad Sci USA 94(14):7435–7440.  https://doi.org/10.1073/pnas.94.14.7435CrossRefPubMedPubMedCentralGoogle Scholar
  121. Zhang W, Rong C, Chen C, Gao GF (2012) Type-IVC secretion system: a novel subclass of type IV secretion system (T4SS) common existing in Gram-positive genus Streptococcus. PLoS ONE 7:e46390CrossRefGoogle Scholar
  122. Zhao Y, Liu G, Li S, Wang M, Song J, Wang J, Tang J, Li M, Hu F (2011) Role of a type IV-like secretion system of Streptococcus suis 2 in the development of streptococcal toxic shock syndrome. J Infect Dis 204(2):274–281.  https://doi.org/10.1093/infdis/jir261CrossRefPubMedGoogle Scholar
  123. Zhao L, Zhong L, Qin Z (2014) Two distinct conjugal transfer systems on Streptomyces plasmid pZL1. Acta Biochim Biophys Sin 46(12):1084–1086.  https://doi.org/10.1093/abbs/gmu095CrossRefPubMedGoogle Scholar

Copyright information

© Springer International Publishing AG 2017

Authors and Affiliations

  • Elisabeth Grohmann
    • 1
  • Walter Keller
    • 2
  • Günther Muth
    • 3
  1. 1.Beuth University of Applied Sciences Berlin, Life Sciences and TechnologyBerlinGermany
  2. 2.Institute of Molecular Biosciences, BioTechMed, University of GrazGrazAustria
  3. 3.Interfaculty Institute of Microbiology and Infection Medicine Tübingen, University TübingenTübingenGermany

Personalised recommendations