The all-alpha domains of coupling proteins from the Agrobacterium tumefaciens VirB/VirD4 and Enterococcus faecalis pCF10-encoded type IV secretion systems confer specificity to binding of cognate DNA substrates

Journal of Bacteriology

Volumn 197, Issue 14, 2015, Pages 2335-2349

  Whitaker, Neal ^a   Chen, Yuqing ^a,d   Jakubowski, Simon J ^b   Sarkar, Mayukh K ^c   Li, Feng ^a   Christie, Peter J ^a  

^a UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF HOUSTON DOWNTOWN   (United States)

^c UNIVERSITY OF TEXAS MEDICAL BRANCH   (United States)

^d UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL DNA; BACTERIAL PROTEIN; CHIMERIC PROTEIN; PROTEIN BINDING;

AGROBACTERIUM TUMEFACIENS; ALGORITHM; AMINO ACID SEQUENCE; ARTICLE; CELL NUCLEUS; CHIMERA; DNA BINDING; DNA SEQUENCE; DNA TRANSFER; ENTEROCOCCUS FAECALIS; GENE DELETION; GENE TARGETING; IN VITRO STUDY; INTERACTIONS WITH DNA; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DNA BINDING; PROTEIN DOMAIN; PROTEIN INTERACTION; PROTEIN PROCESSING; PROTEIN PURIFICATION; PROTEIN SYNTHESIS; STEADY STATE; TYPE IV SECRETION SYSTEM; WILD TYPE; GENETICS; METABOLISM; MOLECULAR GENETICS; MOLECULAR MODEL; PROTEIN CONFORMATION; PROTEIN TERTIARY STRUCTURE;

AGROBACTERIUM TUMEFACIENS; BACTERIA (MICROORGANISMS); ENTEROCOCCUS FAECALIS;

AGROBACTERIUM TUMEFACIENS; AMINO ACID SEQUENCE; BACTERIAL PROTEINS; DNA, BACTERIAL; ENTEROCOCCUS FAECALIS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN STRUCTURE, TERTIARY;

EID: 84932098482     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.00189-15     Document Type: Article

References (78)

1. Christie PJ, Whitaker N, Gonzalez-Rivera C. 2014. Mechanism and structure of the bacterial type IV secretion systems. Biochim Biophys Acta 1843:1578-1591. http://dx.doi.org/10.1016/j.bbamcr.2013.12.019.
2. Bhatty M, Laverde Gomez JA, Christie PJ. 2013. The expanding bacterial type IV secretion lexicon. Res Microbiol 164:620-639. http://dx.doi.org/10.1016/j.resmic.2013.03.012.
3. Goessweiner-Mohr N, Arends K, Keller W, Grohmann E. 2013. Conjugative type IV secretion systems in Gram-positive bacteria. Plasmid 70: 289-302. http://dx.doi.org/10.1016/j.plasmid.2013.09.005.
4. Zechner EL, Lang S, Schildbach JF. 2012. Assembly and mechanisms of bacterial type IV secretion machines. Philos Trans R Soc Lond B Biol Sci 367:1073-1087. http://dx.doi.org/10.1098/rstb.2011.0207.
5. Cabezon E, Ripoll-Rozada J, Pena A, de la Cruz F, Arechaga I. 2015. Towards an integrated model of bacterial conjugation. FEMS Microbiol Rev 39:81-95. http://dx.doi.org/10.1111/1574-6976.12085.
6. Cascales E, Christie PJ. 2003. The versatile bacterial type IV secretion systems. Nat Rev Microbiol 1:137-150. http://dx.doi.org/10.1038/nrmicro753.
7. Voth DE, Broederdorf LJ, Graham JG. 2012. Bacterial type IV secretion systems: versatile virulence machines. Future Microbiol 7:241-257. http://dx.doi.org/10.2217/fmb.11.150.
8. Alvarez-Martinez CE, Christie PJ. 2009. Biological diversity of prokaryotic type IV secretion systems. Microbiol Mol Biol Rev 73:775-808. http://dx.doi.org/10.1128/MMBR.00023-09.
9. Trokter M, Felisberto-Rodriguez C, Christie PJ, Waksman G. 2014. Recent advances in structural and molecular biology of type IV secretion systems. Curr Opin Struct Biol 27:16-23. http://dx.doi.org/10.1016/j.sbi.2014.02.006.
10. Fronzes R, Schafer E, Wang L, Saibil HR, Orlova EV, Waksman G. 2009. Structure of a type IV secretion system core complex. Science 323: 266-268. http://dx.doi.org/10.1126/science.1166101.
11. 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 462:1011-1015. http://dx.doi.org/10.1038/nature08588.
12. Fronzes R, Christie PJ, Waksman G. 2009. The structural biology of type IV secretion systems. Nat Rev Microbiol 7:703-714. http://dx.doi.org/10.1038/nrmicro2218.
13. Low HH, Gubellinin F, Rivera-Calzada A, Connery S, Dujeancourt A, Lu F, Fronzes R, Orlova EV, Waksman G. 2014. Structure of a type IV secretion system. Nature 508:550-553. http://dx.doi.org/10.1038/nature13081.
14. Llosa M, Zunzunegui S, de la Cruz F. 2003. Conjugative coupling proteins interact with cognate and heterologous VirB10-like proteins while exhibiting specificity for cognate relaxosomes. Proc Natl Acad Sci USA 100:10465-10470. http://dx.doi.org/10.1073/pnas.1830264100.
15. Cascales E, Atmakuri K, Sarkar MK, Christie PJ. 2013. DNA substrateinduced activation of the Agrobacterium VirB/VirD4 type IV secretion system. J Bacteriol 195:2691-2704. http://dx.doi.org/10.1128/JB.00114-13.
16. Garza I, Christie PJ. 2013. A putative transmembrane leucine zipper of Agrobacterium VirB10 is essential for T-pilus biogenesis but not type IV secretion. J Bacteriol 195:3022-3034. http://dx.doi.org/10.1128/JB.00287-13.
17. Segura RL, Aguila-Arcos S, Ugarte-Uribe B, Vecino AJ, de la Cruz F, Goni FM, Alkorta I. 2013. The transmembrane domain of the T4SS coupling protein TrwB and its role in protein-protein interactions. Biochim Biophys Acta 1828:2015-2025. http://dx.doi.org/10.1016/j.bbamem.2013.05.022.
18. Gomis-Ruth FX, Moncalian G, Perez-Luque R, Gonzalez A, Cabezon E, de la Cruz F, Coll M. 2001. The bacterial conjugation protein TrwB resembles ring helicases and F1-ATPase. Nature 409:637-641. http://dx.doi.org/10.1038/35054586.
19. Hormaeche I, Alkorta I, Moro F, Valpuesta JM, Goni FM, De La Cruz F. 2002. Purification and properties of TrwB, a hexameric, ATP-binding integral membrane protein essential for R388 plasmid conjugation. J Biol Chem 277:46456-46462. http://dx.doi.org/10.1074/jbc.M207250200.
20. Gomis-Ruth FX, de la Cruz F, Coll M. 2002. Structure and role of coupling proteins in conjugal DNA transfer. Res Microbiol 153:199-204. http://dx.doi.org/10.1016/S0923-2508(02)01313-X.
21. Gomis-Ruth FX, Sola M, de la Cruz F, Coll M. 2004. Coupling factors in macromolecular type-IV secretion machineries. Curr Pharm Des 10: 1551-1565. http://dx.doi.org/10.2174/1381612043384817.
22. Cao Y, Hallet B, Sherratt DJ, Hayes F. 1997. Structure-function correlations in the XerD site-specific recombinase revealed by pentapeptide scanning mutagenesis. J Mol Biol 274:39-53. http://dx.doi.org/10.1006/jmbi.1997.1380.
23. Ferreira H, Sherratt D, Arciszewska L. 2001. Switching catalytic activity in the XerCD site-specific recombination machine. J Mol Biol 312:45-57. http://dx.doi.org/10.1006/jmbi.2001.4940.
24. Llosa M, Gomis-Ruth FX, Coll M, Cruz FDL. 2002. Bacterial conjugation: a two-step mechanism for DNA transport. Mol Microbiol 45:1-8. http://dx.doi.org/10.1046/j.1365-2958.2002.03014.x.
25. Cascales E, Christie PJ. 2004. Definition of a bacterial type IV secretion pathway for a DNA substrate. Science 304:1170-1173. http://dx.doi.org/10.1126/science.1095211.
26. Atmakuri K, Cascales E, Christie PJ. 2004. Energetic components VirD4, VirB11 and VirB4 mediate early DNA transfer reactions required for bacterial type IV secretion. Mol Microbiol 54:1199-1211. http://dx.doi.org/10.1111/j.1365-2958.2004.04345.x.
27. Schroder G, Krause S, Zechner EL, Traxler B, Yeo HJ, Lurz R, Waksman G, Lanka E. 2002. TraG-like proteins of DNA transfer systems and of the Helicobacter pylori type IV secretion system: inner membrane gate for exported substrates?. J Bacteriol 184:2767-2779. http://dx.doi.org/10.1128/JB.184.10.2767-2779.2002.
28. Christie PJ, Atmakuri K, Krishnamoorthy V, Jakubowski S, Cascales E. 2005. Biogenesis, architecture, and function of bacterial type IV secretion systems. Annu Rev Microbiol 59:451-485. http://dx.doi.org/10.1146/annurev.micro.58.030603.123630.
29. Atmakuri K, Cascales E, Burton OT, Banta LM, Christie PJ. 2007. Agrobacterium ParA/MinD-like VirC1 spatially coordinates early conjugative DNA transfer reactions. EMBO J 26:2540-2551. http://dx.doi.org/10.1038/sj.emboj.7601696.
30. 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 190:3632-3645. http://dx.doi.org/10.1128/JB.01999-07.
31. Yanofsky MF, Porter SG, Young C, Albright LM, Gordon MP, Nester EW. 1986. The virD operon of Agrobacterium tumefaciens encodes a sitespecific endonuclease. Cell 47:471-477. http://dx.doi.org/10.1016/0092-8674(86)90604-5.
32. Albright LM, Yanofsky MF, Leroux B, Ma DQ, Nester EW. 1987. Processing of the T-DNA of Agrobacterium tumefaciens generates border nicks and linear, single-stranded T-DNA. J Bacteriol 169:1046-1055.
33. Toro N, Datta A, Carmi OA, Young C, Prusti RK, Nester EW. 1989. The Agrobacterium tumefaciens virC1 gene product binds to overdrive, a TDNA transfer enhancer. J Bacteriol 171:6845-6849.
34. Guo M, Jin S, Sun D, Hew CL, Pan SQ. 2007. Recruitment of conjugative DNA transfer substrate to Agrobacterium type IV secretion apparatus. Proc Natl Acad Sci USA 104:20019-20024. http://dx.doi.org/10.1073/pnas.0701738104.
35. Padavannil A, Jobichen C, Qinghua Y, Seetharaman J, Velazquez-Campoy A, Yang L, Pan SQ, Sivaraman J. 2014. Dimerization of VirD2 binding protein is essential for Agrobacterium induced tumor formation in plants. PLoS Pathog 10:e1003948. http://dx.doi.org/10.1371/journal.ppat.1003948.
36. Chen Y, Staddon JH, Dunny GM. 2007. Specificity determinants of conjugative DNA processing in the Enterococcus faecalis plasmid pCF10 and the Lactococcus lactis plasmid pRS01. Mol Microbiol 63:1549-1564. http://dx.doi.org/10.1111/j.1365-2958.2007.05610.x.
37. Sciaky D, Montoya AL, Chilton MD. 1978. Fingerprints of Agrobacterium Ti plasmids. Plasmid 1:238-253. http://dx.doi.org/10.1016/0147-619X(78)90042-2.
38. Zhu J, Oger PM, Schrammeijer B, Hooykaas PJ, Farrand SK, Winans SC. 2000. The bases of crown gall tumorigenesis. J Bacteriol 182:3885-3895. http://dx.doi.org/10.1128/JB.182.14.3885-3895.2000.
39. Van Larebeke N, Genetello C, Schell J, Schilperoort RA, Hermans AK, Van Montagu M, Hernalsteens JP. 1975. Acquisition of tumourinducing ability by non-oncogenic agrobacteria as a result of plasmid transfer. Nature 255:742-743. http://dx.doi.org/10.1038/255742a0.
40. Ooms G, Hooykaas PJJ, Van Veen RJM, Van Beelen P, Regensburg-Tunik R, Schilperoort RA. 1982. Octopine Ti-plasmid deletion mutants of Agrobacterium tumefaciens with emphasis on the right side of the T-region. Plasmid 7:15-19. http://dx.doi.org/10.1016/0147-619X(82)90023-3.
41. Fullner KJ. 1998. Role of Agrobacterium virB genes in transfer of T complexes and RSF1010. J Bacteriol 180:430-434.
42. Zhou X-R, Christie PJ. 1999. Mutagenesis of Agrobacterium VirE2 singlestranded DNA-binding protein identifies regions required for selfassociation and interaction with VirE1 and a permissive site for hybrid protein construction. J Bacteriol 181:4342-4352.
43. Dunny GM, Brown BL, Clewell DB. 1978. Induced cell aggregation and mating in Streptococcus faecalis: evidence for a bacterial sex pheromone. Proc Natl Acad Sci USA 75:3479-3483. http://dx.doi.org/10.1073/pnas.75.7.3479.
44. Staddon JH, Bryan EM, Manias DA, Chen Y, Dunny GM. 2006. Genetic characterization of the conjugative DNA processing system of enterococcal plasmid pCF10. Plasmid 56:102-111. http://dx.doi.org/10.1016/j.plasmid.2006.05.001.
45. Jakubowski SJ, Krishnamoorthy V, Christie PJ. 2003. Agrobacterium tumefaciens VirB6 protein participates in formation of VirB7 and VirB9 complexes required for type IV secretion. J Bacteriol 185:2867-2878. http://dx.doi.org/10.1128/JB.185.9.2867-2878.2003.
46. Kovach ME, Phillips RW, Elzer PH, Roop RM, II, Peterson KM. 1994. pBBR1MCS: a broad-host-range cloning vector. Biotechniques 16:800-802.
47. Bryan EM, Bae T, Kleerebezem M, Dunny GM. 2000. Improved vectors for nisin-controlled expression in gram-positive bacteria. Plasmid 44: 183-190. http://dx.doi.org/10.1006/plas.2000.1484.
48. Berger BR, Christie PJ. 1994. Genetic complementation analysis of the Agrobacterium tumefaciens virB operon: virB2 through virB11 are essential virulence genes. J Bacteriol 176:3646-3660.
49. Otten L, De Greve H, Leemans J, Hain R, Hooykaas P, Schell J. 1984. Restoration of virulence of vir region mutants of Agrobacterium tumefaciens strain B6S3 by coinfection with normal and mutant Agrobacterium strains. Mol Gen Genet 195:159-163. http://dx.doi.org/10.1007/BF00332739.
50. 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 194:4041-4051. http://dx.doi.org/10.1128/JB.00648-12.
51. Kelley LA, Sternberg MJ. 2009. Protein structure prediction on the Web: a case study using the Phyre server. Nat Protoc 4:363-371. http://dx.doi.org/10.1038/nprot.2009.2.
52. Gelvin SB. 2012. Traversing the cell: Agrobacterium T-DNA's journey to the host genome. Front Plant Sci 3:52. http://dx.doi.org/10.3389/fpls.2012.00052.
53. Simone M, McCullen CA, Stahl LE, Binns AN. 2001. The carboxyterminus 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. http://dx.doi.org/10.1046/j.1365-2958.2001.02582.x.
54. Vergunst AC, van Lier MC, den Dulk-Ras A, Grosse Stuve TA, Ouwehand A, Hooykaas PJ. 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 USA 102:832-837. http://dx.doi.org/10.1073/pnas.0406241102.
55. van Kregten M, Lindhout BI, Hooykaas PJ, van der Zaal BJ. 2009. Agrobacterium-mediated T-DNA transfer and integration by minimal VirD2 consisting of the relaxase domain and a type IV secretion system translocation signal. MPMI 22:1356-1365. http://dx.doi.org/10.1094/MPMI-22-11-1356.
56. Lee MH, Kosuk N, Bailey J, Traxler B, Manoil C. 1999. Analysis of F factor TraD membrane topology by use of gene fusions and trypsinsensitive insertions. J Bacteriol 181:6108-6113.
57. de Paz HD, Larrea D, Zunzunegui S, Dehio C, de la Cruz F, Llosa M. 2010. Functional dissection of the conjugative coupling protein TrwB. J Bacteriol 192:2655-2669. http://dx.doi.org/10.1128/JB.01692-09.
58. Tato I, Zunzunegui S, de la Cruz F, Cabezon E. 2005. TrwB, the coupling protein involved inDNAtransport during bacterial conjugation, is aDNA dependent ATPase. Proc Natl Acad Sci USA 102:8156-8161. http://dx.doi.org/10.1073/pnas.0503402102.
59. Matilla I, Alfonso C, Rivas G, Bolt EL, de la Cruz F, Cabezon E. 2010. The conjugative DNA translocase TrwB is a structure-specific DNAbinding protein. J Biol Chem 285:17537-17544. http://dx.doi.org/10.1074/jbc.M109.084137.
60. Cascales E, Christie PJ. 2004. Agrobacterium VirB10, an ATP energy sensor required for type IV secretion. Proc Natl Acad Sci USA 101:17228-17233. http://dx.doi.org/10.1073/pnas.0405843101.
61. de la Cruz F, Frost LS, Meyer RJ, Zechner EL. 2010. Conjugative DNA metabolism in Gram-negative bacteria. FEMS Microbiol Rev 34:18-40. http://dx.doi.org/10.1111/j.1574-6976.2009.00195.x.
62. Hirt H, Manias DA, Bryan EM, Klein JR, Marklund JK, Staddon JH, Paustian ML, Kapur V, Dunny GM. 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 187:1044-1054. http://dx.doi.org/10.1128/JB.187.3.1044-1054.2005.
63. Nagai H, Cambronne ED, Kagan JC, Amor JC, Kahn RA, Roy CR. 2005. A C-terminal translocation signal required for Dot/Icm-dependent delivery of the Legionella RalF protein to host cells. Proc Natl Acad Sci USA 102:826-831. http://dx.doi.org/10.1073/pnas.0406239101.
64. Atmakuri K, Ding Z, Christie PJ. 2003. VirE2, a type IV secretion substrate, interacts with the VirD4 transfer protein at cell poles of Agrobacterium tumefaciens. Mol Microbiol 49:1699-1713. http://dx.doi.org/10.1046/j.1365-2958.2003.03669.x.
65. Hormaeche I, Iloro I, Arrondo JL, Goni FM, de la Cruz F, Alkorta I. 2004. Role of the transmembrane domain in the stability of TrwB, an integral protein involved in bacterial conjugation. J Biol Chem 279: 10955-10961. http://dx.doi.org/10.1074/jbc.M310422200.
66. Hormaeche I, Segura RL, Vecino AJ, Goni FM, de la Cruz F, Alkorta I. 2006. The transmembrane domain provides nucleotide binding specificity to the bacterial conjugation protein TrwB. FEBS Lett 580:3075-3082. http://dx.doi.org/10.1016/j.febslet.2006.04.059.
67. Segura RL, Aguila-Arcos S, Ugarte-Uribe B, Vecino AJ, de la Cruz F, Goni FM, Alkorta I. 2014. Subcellular location of the coupling protein TrwB and the role of its transmembrane domain. Biochim Biophys Acta 1838:223-230. http://dx.doi.org/10.1016/j.bbamem.2013.08.016.
68. Wong JJ, Lu J, Edwards RA, Frost LS, Glover JN. 2011. Structural basis of cooperativeDNArecognition by the plasmid conjugation factor, TraM. Nucleic Acids Res 39:6775-6788. http://dx.doi.org/10.1093/nar/gkr296.
69. Wong JJ, Lu J, Glover JN. 2012. Relaxosome function and conjugation regulation in F-like plasmids: a structural biology perspective. Mol Microbiol 85:602-617. http://dx.doi.org/10.1111/j.1365-2958.2012.08131.x.
70. Parker C, Meyer RJ. 2007. The R1162 relaxase/primase contains two type IV transport signals that require the small plasmid proteinMobB.MolMicrobiol 66:252-261. http://dx.doi.org/10.1111/j.1365-2958.2007.05925.x.
71. Lang S, Gruber K, Mihajlovic S, Arnold R, Gruber CJ, Steinlechner S, Jehl MA, Rattei T, Frohlich KU, Zechner EL. 2010. Molecular recognition determinants for type IV secretion of diverse families of conjugative relaxases. Mol Microbiol 78:1539-1555. http://dx.doi.org/10.1111/j.1365-2958.2010.07423.x.
72. Alperi A, Larrea D, Fernandez-Gonzalez E, Dehio C, Zechner EL, Llosa M. 2013. A translocation motif in relaxase TrwC specifically affects recruitment by its conjugative type IV secretion system. J Bacteriol 195: 4999-5006. http://dx.doi.org/10.1128/JB.00367-13.
73. Redzej A, Ilangovan A, Lang S, Gruber CJ, Topf M, Zangger K, Zechner EL, Waksman G. 2013. Structure of a translocation signal domain mediating conjugative transfer by type IV secretion systems. Mol Microbiol 89:324-333. http://dx.doi.org/10.1111/mmi.12275.
74. Rashkova S, Spudich GM, Christie PJ. 1997. Characterization of membrane and protein interaction determinants of the Agrobacterium tumefaciens VirB11 ATPase. J Bacteriol 179:583-591.
75. Burgess RR, Arthur TM, Pietz BC. 2000. Mapping protein-protein interaction domains using ordered fragment ladder far-western analysis of hexahistidine-tagged fusion proteins. Methods Enzymol 328:141-157. http://dx.doi.org/10.1016/S0076-6879(00)28396-1.
76. Stahl LE, Jacobs A, Binns AN. 1998. The conjugal intermediate of plasmid RSF1010 inhibits Agrobacterium tumefaciens virulence and VirBdependent export of VirE2. J Bacteriol 180:3933-3939.
77. Zhou XR, Christie PJ. 1997. Suppression of mutant phenotypes of the Agrobacterium tumefaciens VirB11 ATPase by overproduction of VirB proteins. J Bacteriol 179:5835-5842.
78. Kristich CJ, Manias DA, Dunny GM. 2005. Development of a method for markerless genetic exchange in Enterococcus faecalis and its use in construction of a srtA mutant. Appl Environ Microbiol 71:5837-5849. http://dx.doi.org/10.1128/AEM.71.10.5837-5849.2005.