Roles of bacillus subtilis Dpra and Ssba in RecA-mediated genetic recombination

Journal of Biological Chemistry

Volumn 289, Issue 40, 2014, Pages 27640-27652

  Yadav, Tribhuwan ^a,b   Carrasco, Begoña ^a   Serrano, Ester ^a   Alonso, Juan C ^a  

^a CENTRO NACIONAL DE BIOTECNOLOGÍA   (Spain)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACILLUS SUBTILIS; GENETIC RECOMBINATIONS;

ADENOSINE TRIPHOSPHATE; BACTERIAL PROTEIN; DPRA PROTEIN; MICROORGANISM PROTEIN; RECA PROTEIN; SSBA PROTEIN; SSBB PROTEIN; UNCLASSIFIED DRUG; BACTERIAL DNA; DNA BINDING PROTEIN; DPRA PROTEIN, BACTERIA; MEMBRANE PROTEIN; SINGLE STRANDED DNA;

ARTICLE; BACILLUS SUBTILIS; BINDING AFFINITY; BINDING SITE; CATALYSIS; CONTROLLED STUDY; DNA RECOMBINATION; DNA STRAND; MOLECULAR DYNAMICS; NONHUMAN; PROTEIN DETERMINATION; PROTEIN DNA BINDING; PROTEIN FUNCTION; PROTEIN HYDROLYSIS; PROTEIN PROTEIN INTERACTION; ENZYMOLOGY; GENETIC RECOMBINATION; GENETICS; METABOLISM;

BACILLUS SUBTILIS; BACTERIAL PROTEINS; DNA, BACTERIAL; DNA, SINGLE-STRANDED; DNA-BINDING PROTEINS; MEMBRANE PROTEINS; REC A RECOMBINASES; RECOMBINATION, GENETIC;

EID: 84907494678     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.577924     Document Type: Article

References (42)

1. Takeuchi, N., Kaneko, K., and Koonin, E. V. (2014) Horizontal gene transfer can rescue prokaryotes from Muller's ratchet: benefit of DNA from dead cells and population subdivision. G3 (Bethesda) 4, 325-339
2. Chen, I., Christie, P. J., and Dubnau, D. (2005) The ins and outs of DNA transfer in bacteria. Science 310,1456-1460
3. Claverys, J. P., Martin, R, and Polar d, P. (2009) The genetic transformation machinery: composition, localization, and mechanism. FEMS Microbiol. Rev. 33, 643-656
4. Kidane, D., Ayora, S., Sweasy, J. B., Graumann, P. L., and Alonso, J. C. (2012) The cell pole: the site of cross talk between the DNA uptake and genetic recombination machinery. Crit. Rev. Biochem. Mol. Biol. 47, 531-555
5. Kramer, N., Hahn, J., and Dubnau, D. (2007) Multiple interactions among the competence proteins of Bacillus subtilis. Mol. Microbiol. 65,454-464
6. Yadav, T., Carrasco, B., Myers, A. R., George, N. P., Keck, J. L., and Alonso, J. C. (2012) Genetic recombination in Bacillus subtilis: a division of labor between two single-strand DNA-binding proteins. Nucleic Acids Res. 40, 5546-5559
7. Yadav, T., Carrasco, B., Hejna, J., Suzuki, Y., Takeyasu, K., and Alonso, J. C. (2013) Bacillus subtilis DprA recruits RecA onto single-stranded DNA and mediates annealing of complementary strands coated by SsbB and SsbA.J. Biol. Chem. 288, 22437-22450
8. Mortier-Barrière, I., Velten, M., Dupaigne, P., Mirouze, N., Piètrement, O., McGovern, S., Fichant, G., Martin, B., Noirot, P., Le Cam, E., Polard, P., and Claverys, J. P. (2007) A key presynaptic role in transformation for a widespread bacterial protein: DprA conveys incoming ssDNA to RecA. Cell 130, 824-836
9. Attaiech, L., Olivier, A., Mortier-Barrière, L, Soulet, A. L., Granadel, C., Martin, B., Polard, P., and Claverys, J. P. (2011) Role of the single-stranded DNA-binding protein SsbB in pneumococcal transformation: maintenance of a reservoir for genetic plasticity. PLoS Genet. 7, el002156
10. Manfredi, C., Carrasco, B., Ayora, S., and Alonso, J. C. (2008) Bacillus subtilis RecO nucleates RecA onto SsbA-coated single-stranded DNA. /. Biol. Chem. 283, 24837-24847
11. Lovett, C. M., Jr., and Roberts, J. W. (1985) Purification of a RecA protein analogue from Bacillus subtilis.J. Biol. Chem. 260, 3305-3313
12. Steffen, S. E., Katz, F. S., and Bryant, F. R. (2002) Complete inhibition of Streptococcus pneumoniae RecA protein-catalyzed ATP hydrolysis by single-stranded DNA-binding protein (SSB protein): implications for the mechanism of SSB protein-stimulated DNA strand exchange. /. Biol. Chem. 277,14493-14500
13. Grove, D. E., Anne, G., Hedayati, M. A., and Bryant, F. R. (2012) Stimulation of the Streptococcus pneumoniae RecA protein-promoted threestrand exchange reaction by the competence-specific SsbB protein. Biochem. Biophys. Res. Comm. 424, 40-44
14. Carrasco, B., Manfredi, C., Ayora, S., and Alonso, J. C. (2008) Bacillus subtilis SsbA and dATP regulate RecA nucleation onto single-stranded DNA. DNA Repair (Amst.) 7, 990-996
15. Bazemore, L. R., Takahashi, M., and Radding, C. M. (1997) Kinetic analysis of pairing and strand exchange catalyzed by RecA. Detection by fluorescence energy transfer.J. Biol. Chem. 272,14672-14682
16. Yancey-Wrona, J. E., and Camerini-Otero, R. D. (1995) The search for DNA homology does not limit stable homologous pairing promoted by RecA protein. Curr. Biol. 5, 1149-1158
17. Voloshin, O. N., and Camerini-Otero, R. D. (2004) Synaptic complex revisited; a homologous recombinase flips and switches bases. Mol. Cell 15, 846-847
18. Cox, M. M. (2007) Motoring along with the bacterial RecA protein. Nat. Rev. Mol. Cell Biol. 8,127-138
19. Bennett, B. D., Kimball, E. H., Gao, M., Osterhout, R., Van Dien, S. J., and Rabinowitz, J. D. (2009) Absolute metabolite concentrations and implied enzyme active site occupancy in Escherichia coli. Nat. Chem. Biol. 5, 593-599
20. Lioy, V. S., Machon, C, Tabone, M., Gonzalez-Pastor, J. E., Daugelavicius, R., Ayora, S., and Alonso, J. C. (2012) The ζ toxin induces a set of protective responses and dormancy. PLoS One 7, e30282
21. Steffen, S. E., and Bryant, F. R. (1999) Reevaluation of the nucleotide cofactor specificity of the RecA protein from Bacillus subtilis. J. Biol. Chem. 274, 25990-25994
22. Ayora, S., Missich, R., Mesa, P., Lurz, R., Yang, S., Egelman, E. H., and Alonso, J. C. (2002) Homologous-pairing activity of the Bacillus subtilis bacteriophage SPP1 replication protein G35P. J. Biol. Chem. 277, 35969-35979
23. Carrasco, B., Ayora, S., Lurz, R., and Alonso, J. C. (2005) Bacillus subtilis RecU Holliday-junction resolvase modulates RecA activities. Nucleic Acids Res. 33, 3942-3952
24. Hobbs, M. D., Sakai, A., and Cox, M. M. (2007) SSB protein limits RecOR binding onto single-stranded DNA.J. Biol. Chem. 282,11058-11067
25. Chiesa, M., Cardenas, P. P., Otón, F., Martinez, J., Mas-Torrent, M., Garcia, F., Alonso, J. C., Rovira, C, and Garcia, R. (2012) Detection of the early stage of recombinational DNA repair by silicon nanowire transistors. Nano Lett. 12,1275-1281
26. Vlašić, L, Mertens, R., Seco, E. M., Carrasco, B., Ayora, S., Reitz, G., Commichau, F. M., Alonso, J. C., and Moeller, R. (2014) Bacillus subtilis RecA and its accessory factors, RecF, RecO, RecR and RecX, are required for spore resistance to DNA double-strand break. Nucleic Acids Res. 42, 2295-2307
27. Shereda, R. D., Kozlov, A. G., Lohman, T. M., Cox, M. M., and Keck, J. L. (2008) SSB as an organizer/mobilizer of genome maintenance complexes. Crit. Rev. Biochem. Mol. Biol. 43, 289 -318
28. Ha, T., Kozlov, A. G., and Lohman, T. M. (2012) Single-molecule views of protein movement on single-stranded DNA. Annu. Rev. Biophys. 41, 295-319
29. Chen, Z., Yang, H., and Pavletich, N. P. (2008) Mechanism of homologous recombination from the RecA-ssDNA/dsDNA structures. Nature 453, 489-494
30. Ayora, S., Piruat, J. L, Luna, R., Reiss, B., Russo, V. E., Aguilera, A., and Alonso, J. C. (2002) Characterization of two highly similar Rad51 homologs of Physcomitrellapatens. J. Mol. Biol. 316, 35-49
31. Radding, C. M. (1991) Helical interactions in homologous pairing and strand exchange driven by RecA protein.J. Biol. Chem. 266, 5355-5358
32. Kowalczykowski, S. C., and Eggleston, A. K. (1994) Homologous pairing and DNA strand-exchange proteins. Annu. Rev. Biochem. 63, 991-1043
33. Ngo, K. V., Molzberger, E. T., Chitteni-Pattu, S., and Cox, M. M. (2013) Regulation of Deinococcus radiodurans RecA protein function via modulation of active and inactive nucleoprotein filament states. J. Biol. Chem. 288,21351-21366
34. Kowalczykowski, S. C., Dixon, D. A., Eggleston, A. K., Lauder, S. D., and Rehrauer, W. M. (1994) Biochemistry of homologous recombination in Escherichia coli. Microbiol Rev. 58, 401-465
35. Traut, T. W. (1994) Physiological concentrations of purines and pyrimidines. Mol. Cell Biochem. 140,1-22
36. Bergé, M., Mortier-Barrière, L, Martin, B., and Claverys, J. P. (2003) Transformation of Streptococcus pneumoniae relies on DprA- and RecA-dependent protection of incoming DNA single strands. Mol. Microbiol. 50, 527-536
37. Brimacombe, C. A., Ding, H., and Beatty, J. T. (2014) Rhodobacter capsulatus DprA is essential for RecA-mediated gene transfer agent (RcGTA) recipient capability regulated by quorum-sensing and the CtrA response regulator. Mol. Microbiol. 92,1260-1278
38. Dwivedi, G. R., Sharma, E., and Rao, D. N. (2013) HelicobacterpyloriDprA alleviates restriction barrier for incoming DNA. Nucleic Acids Res. 41, 3274-3288
39. Sinha, S., Meli, J. C., and Redfield, R. J. (2012) Seventeen Sxy-dependent cyclic AMP receptor protein site-regulated genes are needed for natural transformation in Haemophilus influenzae. J. Bacteriol. 194, 5245-5254
40. Wang, W., Ding,J., Zhang, Y., Hu, Y., and Wang, D. C. (2014) Structural insights into the unique single-stranded DNA-binding mode of Helicobacter pylori DprA. Nucleic Acids Res. 42, 3478 -3491
41. Quevillon-Cheruel, S., Campo, N., Mirouze, N., Mortier-Barrière, I., Brooks, M. A., Boudes, M., Durand, D., Soulet, A. L, Lisboa, J., Noirot, P., Martin, B., van Tilbeurgh, H., Noirot-Gros, M. F., Claverys, J. P., and Polard, P. (2012) Structure-function analysis of pneumococcal DprA protein reveals that dimerization is crucial for loading RecA recombinase onto DNA during transformation. Proc. Natl. Acad. Sci. U.S.A. 109, E2466-E2475
42. Lisboa, J., Andreani, J., Sanchez, D., Boudes, M., Collinet, B., Liger, D., van Tilbeurgh, H., Guérois, R., and Quevillon-Cheruel, S. (2014) Molecular determinants of the DprA-RecA interaction for nucleation on ssDNA. Nucleic Acids Res. 42, 7395-7408