MobC of conjugative RA3 plasmid from IncU group autoregulates the expression of bicistronic mobC-nic operon and stimulates conjugative transfer

BMC Microbiology

Volumn 14, Issue 1, 2014, Pages

  Godziszewska, Jolanta ^a   Kuliñska, Anna ^a,b   Jagura Burdzy, Grazyna ^a  

^a INSTITUTE OF BIOCHEMISTRY AND BIOPHYSICS   (Poland)

^b WARSAW UNIVERSITY OF TECHNOLOGY   (Poland)

Author keywords

Broad host range plasmid; Conjugative transfer; IncU; MobC; Transfer auxiliary protein

Indexed keywords

BACTERIAL PROTEIN; CARRIER PROTEIN; PROTEIN MOBC; UNCLASSIFIED DRUG; TRANSCRIPTION FACTOR;

AMINO ACID SEQUENCE; ARTICLE; BACTERIAL GENE; BACTERIAL STRAIN; BACTERIUM CONJUGATION; CONTROLLED STUDY; GENE EXPRESSION; IN VITRO STUDY; MOBC GENE; MOLECULAR BIOLOGY; NIC GENE; NONHUMAN; NUCLEOTIDE SEQUENCE; OPERON; PLASMID; PROMOTER REGION; PROTEIN DNA BINDING; PROTEIN FUNCTION; PROTEIN STRUCTURE; BACTERIUM; CLUSTER ANALYSIS; GENE EXPRESSION REGULATION; GENETICS; HORIZONTAL GENE TRANSFER; METABOLISM; PHYLOGENY; PROTEIN MOTIF; PROTEIN MULTIMERIZATION; SEQUENCE HOMOLOGY;

AMINO ACID MOTIFS; BACTERIA; CLUSTER ANALYSIS; CONJUGATION, GENETIC; GENE EXPRESSION REGULATION, BACTERIAL; GENE TRANSFER, HORIZONTAL; OPERON; PHYLOGENY; PLASMIDS; PROTEIN MULTIMERIZATION; SEQUENCE HOMOLOGY, AMINO ACID; TRANSCRIPTION FACTORS;

EID: 84908221751     PISSN: None     EISSN: 14712180     Source Type: Journal    
DOI: 10.1186/s12866-014-0235-1     Document Type: Article

References (51)

1. Christie PJ, Cascales E: Structural and dynamic properties of bacterial Type IV secretion systems. Mol Membr Biol 2005, 22:51-61.
2. Schröder G, Lanka E: The mating pair formation system of conjugative plasmids-A versatile secretion machinery for transfer of proteins and DNA. Plasmid 2005, 54:1-25.
3. Zechner E, de la Cruz F, Eisenbrandt R, Grahn A, Koraimann G, Lanka E, Muth G, Pansegrau W, Thomas C, Wilkins B, Zatyka M: Conjugative-DNA Transfer Processes. In The Horizontal Gene Pool, Bacterial Plasmids and Gene Spread. Edited by Thomas CM. Amsterdam: Harwood Academic Publishers; 2000:87-174.
4. Guasch A, Lucas M, Moncalian G, Cabezas M, Perez-Luque R, Gomis-Ruth FX, de la Cruz F, Coll M: Recognition and processing of the origin of transfer DNA by conjugative relaxase TrwC. Nat Struct Mol Biol 2003, 10:1002-1010.
5. De la Cruz F, Frost LS, Meyer RJ, Zechner EL: Conjugative DNA metabolism in Gram-negative bacteria. FEMS Microbiol Rev 2010, 34:18-40.
6. Trokter M, Felisberto-Rodrigues C, Christie P, Waksman G: Recent advances in the structural and molecular biology of type IV secretion systems. Curr Opin Struct Biol 2014, 27:16-23.
7. Bhatty M, Laverde Gomez JA, Christie PJ: The expanding bacterial type IV secretion lexicon. Res Microbiol 2013, 164:620-639.
8. Fekete RA, Frost LS: Characterizing the DNA contacts and cooperative binding of F plasmid TraM to its cognate sites at oriT. J Biol Chem 2002, 277:16705-16711.
9. Pansegrau W, Ziegelin G, Lanka E: Covalent association of the traI gene product of plasmid RP4 with the 5′-terminal nucleotide at the relaxation nick site. J Biol Chem 1990, 265:10637-10644.
10. Ragonese H, Haisch D, Villareal E, Choi J-H, Matson SW: The F plasmid-encoded TraM protein stimulates relaxosome-mediated cleavage at oriT through an interaction with TraI. Mol Microbiol 2007, 63:1173-1184.
11. Ziegelin G, Fürste JP, Lanka E: TraJ protein of plasmid RP4 binds to a 19-base pair invert sequence repetition within the transfer origin. J Biol Chem 1989, 264:11989-11994.
12. Ziegelin G, Pansegrau W, Lurz R, Lanka E: TraK protein of conjugative plasmid RP4 forms a specialized nucleoprotein complex with the transfer origin. J Biol Chem 1992, 267:17279-17286.
13. Varsaki A, Moncalian G, del Pilar Garcillan-Barcia M, Drainas C, de la Cruz F: Analysis of ColE1 MbeC unveils an extended ribbon-helix-helix family of nicking accessory proteins. J Bacteriol 2009, 191:1446-1455.
14. Tato I, Matilla I, Arechaga I, Zunzunegui S, de la Cruz F, Cabezon E: The ATPase activity of the DNA transporter TrwB is modulated by protein TrwA: implications for common assembly mechanism of DNA translocating motor. J Biol Chem 2007, 282:25569-25576.
15. Zatyka M, Jagura-Burdzy G, Thomas CM: Transcriptional and translational control of the genes for the mating pair formation apparatus of promiscuous IncP plasmids. J Bacteriol 1997, 179: 7201-7209.
16. Silverman PM, Sholl A: Effect of traY amber mutations on F-plasmid traY promoter activity in vivo. J Bacteriol 1996, 178:5787-5789.
17. Penfold SS, Simon J, Frost LS: Regulation of the expression of the traM gene of the F sex factor of Escherichia coli. Mol Microbiol 1996, 20:549-558.
18. Fu YH, Tsai MM, Luo YN, Deonier RC: Deletion analysis of the F plasmid oriT locus. J Bacteriol 1991, 173:1012-1020.
19. Moncalián G, Grandoso G, Llosa M, de la Cruz F: OriT-processing and regulatory roles of TrwA protein in plasmid R388 conjugation. J Mol Biol 1997, 270:188-200.
20. Aoki T, Mitoma Y, Crosa JH: The characterization of a conjugative Rplasmid isolated from Aeromonas salmonicida. Plasmid 1986, 16:213-218.
21. Kulinska A, Czeredys M, Hayes F, Jagura-Burdzy G: Genomic and functional characterization of the modular broad-host-range RA3 plasmid, the archetype of the IncU group. Appl Environ Microbiol 2008, 74:4119-4132.
22. Rhodes G, Parkhill J, Bird C, Ambrose K, Jones MC, Huys G, Swings J, Pickup RW: Complete nucleotide sequence of the conjugative tetracycline resistance plasmid pFBAOT6, a member of a group of IncU plasmids with global ubiquity. Appl Environ Microbiol 2004, 70: 7497-7510.
23. Yanisch-Perron C, Vieira J, Messing J: Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors. Gene 1985, 33:103-119.
24. Brown CJ, Sen D, Yano H, Bauer ML, Rogers LM, Van der Auwera GA, Top EM: Diverse broad-host-range plasmids from freshwater carry few accessory genes. Appl Environ Microbiol 2013, 79:7684-7695.
25. Van der Auwera G, Król J, Suzuki H, Foster B, Van Houdt R, Brown C, Mergeay M, Top E: Plasmids captured in C. metallidurans CH34: defining the PromA family of broad-host-range plasmids. Antonie Van Leeuwenhoek 2009, 96:193-204.
26. Fürste JP, Pansegrau W, Ziegelin G, Kröger M, Lanka E: Conjugative transfer of promiscuous IncP plasmids: interaction of plasmid-encoded products with the transfer origin. Proc Natl Acad Sci 1989, 86:1771-1775.
27. Bowie JU, Sauer RT: TraY proteins of F and related episomes are members of the Arc and Mnt repressor family. J Mol Biol 1990, 211:5-6.
28. Moncalián G, de la Cruz F: DNA binding properties of protein TrwA, a possible structural variant of the Arc repressor superfamily. Biochim Biophys Acta 2004, 1701:15-23.
29. Guiney DG, Deiss C, Simnad V, Yee L, Pansegrau W, Lanka E: Mutagenesis of the Tra1 core region of RK2 by using Tn5: identification of plasmid-specific transfer genes. J Bacteriol 1989, 171:4100-4103.
30. Varsaki A, Lamb HK, Eleftheriadou O, Vandera E, Thompson P, Moncalián G, de la Cruz F, Hawkins AR, Drainas C: Interaction between relaxase MbeA and accessory protein MbeC of the conjugally mobilizable plasmid ColE1. FEBS Lett 2012, 586:675-679.
31. Karimova G, Pidoux J, Ullmann A, Ladant D: A bacterial two-hybrid system based on a reconstituted signal transduction pathway. Proc Natl Acad Sci 1998, 95:5752-5756.
32. Kahn MR, Kolter R, Thomas CM, Figurski D, Meyer R, Remault E, Helinski DR: Plasmid cloning vehicles derived from plasmids ColE1, F, R6K, and RK2. Methods Enzymol 1979, 68:268-280.
33. Sambrook J, Fritsch EF, Maniatis T: Molecular Cloning, a Laboratory Manual. 2nd edition. Cold Spring Harbor, NY: Cold Spring Harbor Press; 1989.
34. Mullis K, Faloona F, Scharf S, Saiki R, Horn G, Erlich H: Specific enzymatic amplification of DNA in vitro: the polymerase chain reaction. Cold Spring Harb Symp Quant Biol 1986, 51:263-273.
35. Jagura-Burdzy G, Ibbotson JP, Thomas CM: The korF region of broad-hostrange plasmid RK2 encodes two polypeptides with transcriptional repressor activity. J Bacteriol 1991, 173:826-833.
36. Kovach ME, Phillips RW, Elzer PH, Roop RM, Peterson KM: pBBR1MCS: a broad-host-range cloning vector. Biotechniques 1994, 16:800-802.
37. Zukowski MM, Gaffney DF, Speck D, Kauffmann M, Findeli A, Wisecup A, Lecocq JP: Chromogenic identification of genetic regulatory signals in Bacillus subtilis based on expression of a cloned Pseudomonas gene. Proc Natl Acad Sci 1983, 80:1101-1105.
38. Bradford MM: A rapid and sensitive method for the quantitation of microgram 486 quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 1976, 72:248-254.
39. Jagura-Burdzy G, Thomas CM: Purification of KorA protein from broad host range plasmid RK2: definition of a hierarchy of KorA operators. J Mol Biol 1995, 253:39-50.
40. Bartosik AA, Lasocki K, Mierzejewska J, Thomas CM, Jagura-Burdzy G: ParB of Pseudomonas aeruginosa: Interactions with its partner ParA and its target parS and specific effects on bacterial growth. J Bacteriol 2004, 186:6983-6998.
41. Spratt BG, Hedge PJ, te Heesen S, Edelman A, Broome-Smith JK: Kanamycin-resistant vectors that are analogues of plasmids pUC8, pUC9, pEMBL8 and pEMBL9. Gene 1986, 41:337-342.
42. Bartosik AA, Markowska A, Szarlak J, Kuliñska A, Jagura-Burdzy G: Novel broad-host-range vehicles for cloning and shuffling of gene cassettes. J Microbiol Methods 2012, 88:53-62.
43. Kulinska A, Cao Y, Macioszek M, Hayes F, Jagura-Burdzy G: The centromere site of the segregation cassette of broad-host-range plasmid RA3 is located at the border of the maintenance and conjugative transfer modules. Appl Environ Microbiol 2011, 77:2414-2427.
44. Tauch A, Schneiker S, Selbitschka W, Pühler A, van Overbeek LS, Smalla K, Thomas CM, Bailey MJ, Forney LJ, Weightman A, Ceglowski P, Pembroke T, Tietze E, Schröder G, Lanka E, van Elsas JD: The complete nucleotide sequence and environmental distribution of the cryptic, conjugative, broad-host-range plasmid pIPO2 isolated from bacteria of the wheat rhizosphere. Microbiology 2002, 148:1637-1653.
45. Marques MV, da Silva AM, Gomes SL: Genetic organization of plasmid pXF51 from the plant pathogen Xylella fastidiosa. Plasmid 2001, 45:184-199.
46. Schneiker S, Keller M, Dröge M, Lanka E, Pühler A, Selbitschka W: The genetic organization and evolution of the broad host range mercury resistance plasmid pSB102 isolated from a microbial population residing in the rhizosphere of alfalfa. Nucleic Acids Res 2001, 29:5169-5181.
47. Schreiter ER, Drennan CL: Ribbon-helix-helix transcription factors: variations on a theme. Nat Rev Microbiol 2007, 5:710-720.
48. Lum PL, Schildbach JF: Specific DNA recognition by F factor TraY involves β-Sheet residues. J Biol Chem 1999, 274:19644-19648.
49. Yoshida H, Furuya N, Lin Y-J, Güntert P, Komano T, Kainosho M: Structural basis of the role of the NikA ribbon-helix-helix domain in initiating bacterial conjugation. J Mol Biol 2008, 384:690-701.
50. Macartney DP, Williams DR, Stafford T, Thomas CM: Divergence and conservation of the partitioning and global regulation functions in the central control region of the IncP plasmids RK2 and R751. Microbiology 1997, 143:2167-2177.
51. Ludwiczak M, Dolowy P, Markowska A, Szarlak J, Kulinska A, Jagura-Burdzy G: Global transcriptional regulator KorC coordinates expression of three backbone modules of the broad-host-range RA3 plasmid from IncU incompatibility group. Plasmid 2013, 70:131-145.