Journal of Microbiology and Biotechnology

The Korean Society for Microbiology and Biotechnology (한국미생물·생명공학회)
권호 표지
DOI QR코드

DOI QR Code

Operon Required for Fruiting Body Development in Myxococcus xanthus

  • Kim, Do-Hee (Myxobacteria Bank, Department of Biotechnology, Hoseo University) ;
  • Chung, Jin-Woo (Myxobacteria Bank, Department of Biotechnology, Hoseo University) ;
  • Hyun, Hye-Sook (Myxobacteria Bank, Department of Biotechnology, Hoseo University) ;
  • Lee, Cha-Yul (Myxobacteria Bank, Department of Biotechnology, Hoseo University) ;
  • Lee, Kyoung (Department of Microbiology, Changwon National University) ;
  • Cho, Kyung-Yun (Myxobacteria Bank, Department of Biotechnology, Hoseo University)
  • Published : 2009.11.30
Download PDF
⟨ Previous Next ⟩

Abstract

We have used mutational analysis to identity four genes, MXAN3553, MXAN3554, MXAN3555, and MXAN3556, constituting an operon that is essential for normal fruiting body development in Myxococcus xanthus. Deletion of MXAN3553, which encoded a hypothetical protein, resulted in delayed fruiting body development. MXAN3554 was predicted to encode a metallopeptidase, and its deletion caused fruiting body formation to fail. Inactivation of MXAN3555, which encoded a putative NtrC-type response regulator, resulted in delayed aggregation and a severe reduction in sporulation. Fruiting bodies also failed to develop with the deletion of MXAN3556, another gene encoding a hypothetical protein.

Keywords

References

  1. Altschul, S. F., T. L. Madden, A. A.Schaffer, J. Zhang, Z. Zhang, W. Miller, and D. J. Lipman. 1997. Gapped BLAST and PSI-BLAST: A new generation of protein database search programs. Nucleic Acids Res. 25: 3389-3402 https://doi.org/10.1093/nar/25.17.3389
  2. Caberoy, N. B., R. D. Welch, J. S. JakobsenS. C. Slater, and A. G Garza. 2003. Global mutational analysis of NtrC-1ike activators in Myxococcus xanthus: Identifying activator mutants defective for motility and fruiting body development. J. Bacteriol. 185: 6083-6094 https://doi.org/10.1128/JB.185.20.6083-6094.2003
  3. Campos, J. M. and D. R. Zusman. 1975. Regulation of development in Myxococcus xanthus: Effect of 3':5'-cyclic AMP, ADP, and nutrition. Proc. Natl. Acad. Sci. USA. 72: 518-522 https://doi.org/10.1073/pnas.72.2.518
  4. Cho, K. and D. R. Zusman. 1999. Sporulation timing in Myxococcus xanthus is controlled by the espAB locus. Mol. Microbiol. 34: 714-725 https://doi.org/10.1046/j.1365-2958.1999.01633.x
  5. Diodati, M. E., F. Ossa, N. B. Caberoy, I. R. Jose, W. Hiraiwa, M. M. Igo, M. Singer, and A. G Garza. 2006. Nla18, a key regulatory protein required for normal growth and development of Myxococcus xanthus. J. Bacteriol. 188: 1733-1743 https://doi.org/10.1128/JB.188.5.1733-1743.2006
  6. Downard, J., S. V. Ramaswamy, and K. S. Kil. 1993. Identification of esg, a genetic locus involved in cell-cell signaling during Myxococcus xanthus development. J. Bacteriol. 175: 7762-7770
  7. Gill, R. E., M. Karlok, and D. Benton. 1993. Myxococcus xanthus encodes an ATP-dependent protease which is required for developmental gene transcription and intercellular signaling. J. Bacteriol. 175: 4538-4544
  8. Gronewold, T. M. and D. Kaiser. 2001. The act operon controls the level and time of C-signa1 production for Myxococcus xanthus development. Mol. Microbiol. 40: 744-756 https://doi.org/10.1046/j.1365-2958.2001.02428.x
  9. Hagen, D. C., A. P. Bretscher, and D. Kaiser. 1978. Synergism between morphogenetic mutants of Myxococcus xanthus. Dev. Biol. 64: 284-296 https://doi.org/10.1016/0012-1606(78)90079-9
  10. Hager, E., H. Tse, and R. E. Gill. 2001. Identification and characterization of spdR mutations that bypass the BsgA protease-dependent regulation of developmental gene expression in Myxococcus xanthus. Mol. Microbiol. 39: 765-780 https://doi.org/10.1046/j.1365-2958.2001.02266.x
  11. Higgs, P. I., K. Cho, D. E. Whitworth, L. S. Evans, and D. R. Zusman. 2005. Four unusual two-component signal transduction homologs, RedC-F, are necessary for timely development in Myxococcus xanthus. J. Bacteriol. 187: 8191-8195 https://doi.org/10.1128/JB.187.23.8191-8195.2005
  12. Jenkins L. S. and W. D. Nunn. 1987. Regulation of the ato operon by the atoC gene in Escherichia coli. J. Bacteriol. 169: 2096-2102
  13. Kirby, J. R. and D. R. Zusman. 2003. Chemosensory regulation of developmental gene expression in Myxococcus xanthus. Proc. Natl. Acad. Sci. USA. 100: 2008-2013 https://doi.org/10.1073/pnas.0330944100
  14. Kuspa, A., L. Plamann, and D. Kaiser. 1992. A-signalling and the cell density requirement for Myxococcus xanthus development. J. Bacteriol. 174: 7360-7369
  15. Lee, B., P. I. Higgs, D. R. Zusman, and K. Cho. 2005. EspC is involved in controlling the timing of development in Myxococcus xanthus. J. Bacteriol. 187: 5029-5031 https://doi.org/10.1128/JB.187.14.5029-5031.2005
  16. Link, A. J., D. Phillips, and G. M. Church. 1997. Methods for generating precise deletions and insertions in the genome of wild-type Escherichia coli: Application to open reading frame characterization. J. Bacteriol. 179: 6228-6237
  17. Lobedanz, S. and L. Sogaard-Andersen. 2003. Identification of the C-signal, a contact-dependent morphogen coordinating multiple developmental responses in Myxococcus xanthus. Genes & Dev. 17: 2151-2161 https://doi.org/10.1101/gad.274203
  18. Marchler-Bauer, A. and S. H. Bryant. 2004. CD-Search: Protein domain annotations on the fly. Nucleic Acids Res. 32: 327-331 https://doi.org/10.1093/nar/gkh454
  19. Miranda-Rios, J., R. Sanchez-Pescador, M. Urdea, and A. A. Covarrubias. 1987. The complete nucleotide sequence of the glnALG operon of Escherichia coli K12. Nucleic Acids Res. 15: 2757-2770 https://doi.org/10.1093/nar/15.6.2757
  20. Ramadurai, L. and R. K. Jayaswal. 1997. Molecular cloning, sequencing, and expression of lytM, a unique autolytic gene of Staphylococcus aureus. J. Bacteriol. 179: 3625-3631
  21. Rasmussen, A. A. and L. Sogaard-Andersen. 2003. TodK, a putative histidine protein kinase, regulates timing of fruiting body morphogenesis in Myxococcus xanthus. J. Bacteriol. 185: 5452-5464 https://doi.org/10.1128/JB.185.18.5452-5464.2003
  22. Rasmussen, A. A., S. L. Porter, J. P. Armitage, and L. Sogaard-Andersen. 2005. Coupling of multicellular morphogenesis and cellular differentiation by an unusual hybrid histidine protein kinase in Myxococcus xanthus. Mol. Microbiol. 56: 1358-1372 https://doi.org/10.1111/j.1365-2958.2005.04629.x
  23. Recsei, P. A., A. D. Gruss, and R. P. Novick. 1987. Cloning, sequence, and expression of the lysostaphin gene from Staphylococcus simulans. Proc. Natl. Acad. Sci. USA. 84: 1127-1131 https://doi.org/10.1073/pnas.84.5.1127
  24. Rosenkrands, I., P. B. Rasmussen, M. Carnio, S. Jacobsen, M. Theisen, and P. Andersen. 1998. Identification and characterization of a 29-kilodalton protein from Mycobacterium tuberculosis culture filtrate recognized by mouse memory effector cells. Infect. Immun. 66: 2728-2735
  25. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular Cloning: A Laboratory Manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York
  26. Schultz, J., R. R. Copley, T. Doerks, C. P. Ponting, and P. Bork. 2000. SMART: A web-based tool for the study of genetically mobile domains. Nucleic Acids Res. 28: 231-234 https://doi.org/10.1093/nar/28.1.231
  27. Shi, X., S. Wegener-Feldbrugge, S. Huntley, N. Hamann, R. Hedderich, and L. Segaard-Andersen. 2008. Bioinformatics and experimental analysis of proteins of two-component systems in Myxococcus xanthus. J. Bacteriol. 190: 613-624 https://doi.org/10.1128/JB.01502-07
  28. Shimkets, L. J. 1990. Social and developmental biology of the myxobacteria. Microbial. Rev. 54: 473-501
  29. Sun, H. and W. Shi. 2001. Genetic studies of mrp, a locus essential for cellular aggregation and sporulation of Myxococcus xanthus. J. Bacteriol. 183: 4786-4795 https://doi.org/10.1128/JB.183.16.4786-4795.2001
  30. Valdes-Stauber, N. and S. Scherer. 1996. Nucleotide sequence and taxonomical distribution of the bacteriocin gene lin cloned from Brevibacterium linens M18. Appl. Environ. Microbial. 62: 1283-1286
  31. Whitworth, D. E. and P. J. A. Cock. 2008. Two-component signal transduction systems of the myxobacteria, pp. 169-189. In D. E. Whitworth (ed.), Myxobacteria: multicellularity and differentiation. ASM Press, Washington, D.C.

Cited by

  1. A virus capsid‐like nanocompartment that stores iron and protects bacteria from oxidative stress vol.33, pp.17, 2009, https://doi.org/10.15252/embj.201488566
  2. XbmR, a new transcription factor involved in the regulation of chemotaxis, biofilm formation and virulence in Xanthomonas citri subsp. citri vol.17, pp.11, 2009, https://doi.org/10.1111/1462-2920.12684
  3. Encapsulins: molecular biology of the shell vol.52, pp.5, 2009, https://doi.org/10.1080/10409238.2017.1337709
  4. Nanotechnological Applications Based on Bacterial Encapsulins vol.11, pp.6, 2009, https://doi.org/10.3390/nano11061467