Fluorescence microscopy of Streptomyces conjugation suggests DNA-transfer at the lateral walls and reveals the spreading of the plasmid in the recipient mycelium

Environmental Microbiology

Volumn 18, Issue 2, 2016, Pages 598-608

  Thoma, Lina ^a   Vollmer, Bernd ^a   Muth, Günther ^a  

^a UNIVERSITY OF TÜBINGEN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ENHANCED GREEN FLUORESCENT PROTEIN; FUNGAL DNA; GREEN FLUORESCENT PROTEIN; PHOTOPROTEIN; RED FLUORESCENT PROTEIN;

BACTERIUM CONJUGATION; FLUORESCENCE MICROSCOPY; FUNGUS HYPHAE; GENETICS; METABOLISM; PHYSIOLOGY; PLASMID; STREPTOMYCES LIVIDANS;

CONJUGATION, GENETIC; DNA, FUNGAL; GREEN FLUORESCENT PROTEINS; HYPHAE; LUMINESCENT PROTEINS; MICROSCOPY, FLUORESCENCE; PLASMIDS; STREPTOMYCES LIVIDANS;

EID: 84959512810     PISSN: 14622912     EISSN: 14622920     Source Type: Journal    
DOI: 10.1111/1462-2920.13027     Document Type: Article

References (41)

1. Bibb, M.J., Ward, J.M., Kieser, T., Cohen, S.N., and Hopwood, D.A. (1981) Excision of chromosomal DNA sequences from Streptomyces coelicolor forms a novel family of plasmids detectable in Streptomyces lividans. Mol Gen Genet 184: 230-240.
2. Chen, C.W., Yu, T.-W., Lin, Y.-S., Kieser, H.M., and Hopwood, D.A. (1993) The conjugative plasmid SLP2 of Streptomyces lividans is a 50kb linear molecule. Mol Microbiol 7: 925-932.
3. Christie, P.J., Whitaker, N., and Gonzalez-Rivera, C. (2014) Mechanism and structure of the bacterial type IV secretion systems. Biochim Biophys Acta 1843: 1578-1591. doi:10.1016/j.bbamcr.2013.12.019.
4. Flärdh, K., Richards, D.M., Hempel, A.M., Howard, M., and Buttner, M.J. (2012) Regulation of apical growth and hyphal branching in Streptomyces. Curr Opin Microbiol 15: 737-743.
5. Gerdes, K., Howard, M., and Szardenings, F. (2010) Pushing and pulling in prokaryotic DNA segregation. Cell 141: 927-942.
6. Grohmann, E., Muth, G., and Espinosa, M. (2003) Conjugative plasmid transfer in gram-positive bacteria. Microbiol Mol Biol Rev 67: 277-301.
7. Gumpert, J. (1976) Ultrastructure and modifiability of the cell envelope in Streptomyces hygroscopicus. In International Symposium on Nocardia and Streptomyces. Mordarski, M., Kurylowicz, W., and Jeljaszewicz, J. (eds). Warsaw, Poland: Gustav Fischer Verlag, pp. 221-233.
8. Gust, B., Chandra, G., Jakimowicz, D., Yuqing, T., Bruton, C.J., and Chater, K.F. (2004) Lambda red-mediated genetic manipulation of antibiotic-producing Streptomyces. Adv Appl Microbiol 54: 107-128.
9. Hopwood, D.A. (2006) Soil to genomics: the Streptomyces chromosome. Annu Rev Genet 40: 1-23.
10. Hopwood, D.A., and Kieser, T. (1993) Conjugative Plasmids of Streptomyces. In Bacterial Conjugation. Clewell, D.B. (ed.). New York, NY, USA: Plenum Press, pp. 293-311.
11. Jakimowicz, D., and van Wezel, G.P. (2012) Cell division and DNA segregation in Streptomyces: how to build a septum in the middle of nowhere? Mol Microbiol 85: 393-404.
12. Jyothikumar, V., Tilley, E.J., Wali, R., and Herron, P.R. (2008) Time-lapse microscopy of Streptomyces coelicolor growth and sporulation. Appl Environ Microbiol 74: 6774-6781.
13. Karimova, G., Pidoux, J., Ullmann, A., and Ladant, D. (1998) A bacterial two-hybrid system based on a reconstituted signal transduction pathway. Proc Natl Acad Sci USA 95: 5752-5756.
14. Kataoka, M., Seki, T., and Yoshida, T. (1991) Five genes involved in self-transmission of pSN22, a Streptomyces plasmid. J Bacteriol 173: 4220-4228.
15. Kendall, K.J., and Cohen, S.N. (1987) Plasmid transfer in Streptomyces lividans: identification of a kil-kor system associated with the transfer region of pIJ101. J Bacteriol 169: 4177-4183.
16. Kendall, K.J., and Cohen, S.N. (1988) Complete nucleotide sequence of the Streptomyces lividans plasmid pIJ101 and correlation of the sequence with genetic properties. J Bacteriol 170: 4634-4651.
17. Kieser, T., Hopwood, D.A., Wright, H.M., and Thompson, C.J. (1982) pIJ101, a multi-copy broad host-range Streptomyces plasmid: functional analysis and development of DNA cloning vectors. Mol Gen Genet 185: 223-238.
18. Kieser, T., Bibb, M.J., Buttner, M.J., Chater, K.F., and Hopwood, D.A. (2000) Practical Streptomyces Genetics. Norwich, UK: The John Innes Foundation.
19. Kosono, S., Kataoka, M., Seki, T., and 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: 397-405.
20. Lanka, E., and Wilkins, B.M. (1995) DNA processing reactions in bacterial conjugation. Annu Rev Biochem 64: 141-169.
21. Lovdok, L., Bentele, K., Vladimirov, N., Muller, A., Pop, F.S., Lebiedz, D., etal. (2009) Role of translational coupling in robustness of bacterial chemotaxis pathway. PLoS Biol 7: e1000171.
22. Pettis, G.S., and Cohen, S.N. (1994) Transfer of the pIJ101 plasmid in Streptomyces lividans requires a cis-acting function dispensable for chromosomal gene transfer. Mol Microbiol 13: 955-964.
23. Pettis, G.S., and Cohen, S.N. (1996) Plasmid transfer and expression of the transfer (tra) gene product of plasmid plJ101 are temporally regulated during the Streptomyces lividans life cycle. Mol Microbiol 19: 1127-1135.
24. Pettis, G.S., and Cohen, S.N. (2000) Mutational analysis of the tra locus of the broad-host-range Streptomyces plasmid pIJ101. J Bacteriol 182: 4500-4504.
25. Pettis, G.S., Ward, N., and Schully, K.L. (2001) Expression characteristics of the transfer-related kilB gene product of Streptomyces plasmid pIJ101: implications for the plasmid spread function. J Bacteriol 183: 1339-1345.
26. Possoz, C., Ribard, C., Gagnat, J., Pernodet, J.L., and Guerineau, M. (2001) The integrative element pSAM2 from Streptomyces: kinetics and mode of conjugal transfer. Mol Microbiol 42: 159-166.
27. Read, N.D., Lichius, A., Shoji, J.Y., and Goryachev, A.B. (2009) Self-signalling and self-fusion in filamentous fungi. Curr Opin Microbiol 12: 608-615.
28. Reuther, J., Gekeler, C., Tiffert, Y., Wohlleben, W., and Muth, G. (2006) Unique conjugation mechanism in mycelial streptomycetes: a DNA-binding ATPase translocates unprocessed plasmid DNA at the hyphal tip. Mol Microbiol 61: 436-446.
29. Sambrook, J., and Russel, D.W. (2001) Molecular Cloning: A Laboratory Manual. New York, USA: Cold Spring Harbor Laboratory Press.
30. Schindelin, J., Arganda-Carreras, I., Frise, E., Kaynig, V., Longair, M., Pietzsch, T., etal. (2012) Fiji: an open-source platform for biological-image analysis. Nat Methods 9: 676-682.
31. Servín-González, L. (1996) Identification and properties of a novel clt locus in the Streptomyces phaeochromogenes plasmid pJV1. J Bacteriol 178: 4323-4326.
32. Servín-González, L., Sampieri, A., Cabello, J., Galván, L., Juárez, V., and 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: 2499-2510.
33. Stein, D.S., Kendall, K.J., and Cohen, S.N. (1989) Identification and analysis of transcriptional regulatory signals for the kil and kor loci of Streptomyces plasmid pIJ101. J Bacteriol 171: 5768-5775.
34. Thoma, L., and Muth, G. (2012) Conjugative DNA transfer in Streptomyces by TraB: is one protein enough? FEMS Microbiol Lett 337: 81-88.
35. Thoma, L., and Muth, G. (2015) The conjugative DNA-transfer apparatus of Streptomyces. Int J Med Microbiol 305: 224-229.
36. Thoma, L., Sepulveda, E., Latus, A., and Muth, G. (2014) The stability region of the Streptomyces lividans plasmid pIJ101 encodes a DNA-binding protein recognizing a highly conserved short palindromic sequence motif. Front Microbiol 5: 499.
37. Thoma, L., Dobrowinski, H., Finger, C., Guezguez, L., Linke, D., Sepulveda, E., and Muth, G. (2015) A multi-protein DNA-translocation complex directs intramycelial plasmid spreading during Streptomyces conjugation. MBio 6: e02559-14. doi:10.1128/mBio.02559-14.
38. Tiffert, Y., Götz, B., Reuther, J., Wohlleben, W., and Muth, G. (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: 2976-2983.
39. Vogelmann, J., Ammelburg, M., Finger, C., Guezguez, J., Linke, D., Flotenmeyer, M., etal. (2011) Conjugal plasmid transfer in Streptomyces resembles bacterial chromosome segregation by FtsK/SpoIIIE. EMBO J 30: 2246-2254.
40. Wickham, H. (2009) ggplot2: Elegant Graphics for Data Analysis. New York, NY, USA: Springer.
41. Zechner, E.L., de la Cruz, F., Eisenbrandt, R., Grahn, A.M., Koraimann, G., Lanka, E., etal. (2000) Conjugative-DNA transfer processes. In The Horizontal Gene Pool. Thomas, C.M. (ed.). Amsterdam, Netherlands: Harwood Academic Publishers, pp. 87-175.