Skip to main content
Log in

A CtrA homolog affects swarming motility and encystment in Rhodospirillum centenum

  • Short Communication
  • Published:
Archives of Microbiology Aims and scope Submit manuscript

Abstract

The α-proteobacterium, Rhodospirillum centenum, has a complex life cycle that allows adaptation to different environments. Transitions between vegetative swim cell and swarmer cell types depend on whether the organism is growing in liquid surroundings or on a solid substrate. Moreover, starvation can induce vegetative cells to differentiate into quiescent cysts. This paper describes the results of our investigation into the role of a putative DNA-binding response regulator that is homologous to CtrA, the cell cycle regulator from Caulobacter crescentus. Deletion of ctrA from the R. centenum genome resulted in a viable strain with impaired swarming motility coupled with an increased tendency to form cysts. Conversely, overexpression of wild type CtrA or a phosphomimetic allele, CtrAD51E, suppressed cyst cell formation, whereas overexpression of a CtrAD51A allele failed to suppress encystment but did prevent swarming motility. Thus, we propose that CtrA participates within a two-component signal transduction pathway that promotes swarming motility while contributing to the suppression of cyst cell formation.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

References

  • Barnett MJ, Hung DY, Reisenauer A, Shapiro L, Long SR (2001) A homolog of the CtrA cell cycle regulator is present and essential in Sinorhizobium meliloti. J Bacteriol 183:3204–3210

    Article  PubMed  CAS  Google Scholar 

  • Bellefontaine A-F, Pierreux CE, Mertens A, Vandenhaute J, Letesson J-J, De Bolle X (2002) Plasticity of a transcriptional regulation network among alpha-proteobacteria is supported by the identification of CtrA targets in Brucella abortus. Mol Microbiol 43:945–960

    Article  PubMed  CAS  Google Scholar 

  • Berleman JE, Bauer CE (2004) Characterization of cyst cell formation in the purple photosynthetic bacterium Rhodospirillum centenum. Microbiology 150:383–390

    Article  PubMed  CAS  Google Scholar 

  • Berleman JE, Bauer CE (2005a) A che-like signal transduction cascade involved in controlling flagella biosynthesis in Rhodospirillum centenum. Mol Microbiol 55:1390–1402

    Article  PubMed  CAS  Google Scholar 

  • Berleman JE, Bauer CE (2005b) Involvement of a Che-like signal transduction cascade in regulating cyst cell development in Rhodospirillum centenum. Mol Microbiol 56:1457–1466

    Article  PubMed  CAS  Google Scholar 

  • Berleman JE, Hasselbring BM, Bauer CE (2004) Hyper-cyst mutants in Rhodospirillum centenum identify regulatory loci involved in cyst cell differentiation. J Bacteriol 186:5834–5841

    Article  PubMed  CAS  Google Scholar 

  • Blomfield IC, Vaughn V, Rest RF, Eisenstein BI (1991) Allelic exchange in Escherichia coli using the Bacillus subtilis sacB gene and a temperature-sensitive pSC101 replicon. Mol Microbiol 5:1447–1457

    Article  PubMed  CAS  Google Scholar 

  • Brilli M, Fondi M, Fani R, Mengoni A, Ferri L, Bazzicalupo M, Biondi EG (2010) The diversity and evolution of cell cycle regulation in alpha-proteobacteria: a comparative genomic analysis. BMC Syst Biol 4:52

    Article  PubMed  Google Scholar 

  • Din N, Shoemaker CJ, Akin KL, Frederick C, Bird TH (2010) Two putative histidine kinases are required for cyst formation in Rhodospirillum centenum. Arch Microbiol (in press)

  • Domian IJ, Quon KC, Shapiro L (1997) Cell type-specific phophosphorylation and proteolysis of a transcriptional regulator controls the G1-to-S transition in a bacterial cell cycle. Cell 90:415–424

    Article  PubMed  CAS  Google Scholar 

  • Favinger J, Stadtwald R, Gest H (1989) Rhodospirillum centenum, sp. nov., a thermotolerant cyst-forming anoxygenic photosynthetic bacterium. Antonie van Leeuwenhoek 55:291–296

    Article  PubMed  CAS  Google Scholar 

  • Griffith KL, Wolf RE Jr (2002) Measuring β-galactosidase activity in bacteria: cell growth, permeabilization, and enzyme assays in 96-well arrays. Biochem Biophys Res Commun 290:397–402

    Article  PubMed  CAS  Google Scholar 

  • Iniesta AA, McGrath PT, Reisenauer A, McAdams HH, Shapiro L (2006) A phospho-signaling pathway controls the localization and activity of a protease complex critical for bacterial cell cycle progression. Proc Natl Acad Sci 103:10935–10940

    Article  PubMed  CAS  Google Scholar 

  • Jacobs C, Domian IJ, Maddock JR, Shapiro L (1999) Cell cycle-dependent polar localization of an essential bacterial histidine kinase that controls DNA replication and cell division. Cell 97:111–120

    Article  PubMed  CAS  Google Scholar 

  • Jacobs C, Ausmees N, Cordwell SJ, Shapiro L, Laub MT (2003) Functions of the CckA histidine kinase in Caulobacter cell cycle control. Mol Microbiol 47:1279–1290

    Article  PubMed  CAS  Google Scholar 

  • Jiang ZY, Bauer CE (1997) Analysis of a chemotaxis operon from Rhodospirillum centenum. J Bacteriol 179:5712–5719

    PubMed  CAS  Google Scholar 

  • Jiang ZY, Rushing BG, Bai Y, Gest H, Bauer CE (1998) Isolation of Rhodospirillum centenum mutants defective in phototactic colony motility by transposon mutagenesis. J Bacteriol 180:1248–1255

    PubMed  CAS  Google Scholar 

  • Kovach ME, Elzer PH, Hill DS, Robertson GT, Farris MA, Roop II RM, Peterson KM (1995) Four new derivatives of the broad-host-range cloning vector pBBR1MCS, carrying different antibiotic-resistant cassettes. Gene 166:175–176

    Article  PubMed  CAS  Google Scholar 

  • Lang AS, Beatty JT (2000) Genetic analysis of a bacterial genetic exchange element: The gene transfer agent of Rhodobacter capsulatus. Proc Natl Acad Sci USA 97:859–864

    Article  PubMed  CAS  Google Scholar 

  • Lang AS, Beatty JT (2002) A bacterial signal transduction system controls genetic exchange and motility. J Bacteriol 184:913–918

    Article  PubMed  CAS  Google Scholar 

  • Laub MT, Chen SL, Shapiro L, McAdams HH (2002) Genes directly controlled by CtrA, a master regulator of the Caulobacter cell cycle. Proc Natl Acad Sci 99:4632–4637

    Article  PubMed  CAS  Google Scholar 

  • Lu YK, Marden J, Han M, Swingley WD, Mastrian SD, Chowdhury SR, Hao J, Helmy T, Kim S, Kurdoglu AA, Matthies HJ, Rollo D, Stothard P, Blankenship RE, Bauer CE, Touchman JW (2010) Metabolic flexibility revealed in the genome of the cyst-forming alpha-1 proteobacterium Rhodospirillum centenum. BMC Genomics 11:325

    Article  PubMed  Google Scholar 

  • Martínez-Hackert E, Stock AM (1997) Structural relationships in the OmpR family of winged-helix transcription factors. J Mol Biol 269:301–312

    Article  PubMed  Google Scholar 

  • Masuda S, Bauer CE (2004) Null mutation of HvrA compensates for loss of an essential relA/spoT-like gene in Rhodobacter capsulatus. J Bacteriol 186:235–239

    Article  PubMed  CAS  Google Scholar 

  • McClain J, Rollo DR, Rushing BG, Bauer CE (2002) Rhodospirillum centenum utilizes separate motor and switch components to control lateral and polar flagellum rotation. J Bacteriol 184:2429–2438

    Article  PubMed  CAS  Google Scholar 

  • Mercer RG, Callister SJ, Lipton MS, Pasa-Tolic L, Strnad H, Paces V, Beatty JT, Lang AS (2010) Loss of the response regulator CtrA causes pleiotropic effects on gene expression in Rhodobacter capsulatus but does not affect growth phase regulation. J Bacteriol 192:2701–2710

    Article  PubMed  CAS  Google Scholar 

  • Papadopoulos JS, Agarwala R (2007) COBALT: constraint-based alignment tool for multiple protein sequences. Bioinformatics 23:1073–1079

    Article  PubMed  CAS  Google Scholar 

  • Quon KC, Marczynski GT, Shapiro L (1996) Cell cycle control by an essential bacterial two-component signal transduction protein. Cell 84:83–93

    Article  PubMed  CAS  Google Scholar 

  • Ragatz L, Jiang ZY, Bauer CE, Gest H (1995) Macroscopic phototactic behavior of the purple photosynthetic bacterium, Rhodospirillum centenum. Arch Microbiol 163:1–6

    Article  PubMed  CAS  Google Scholar 

  • Sadasivan L, Neyra CA (1985) Flocculation in Azospirillum brasilense and Azospirillum lipoferum: exopolysaccharides and cyst formation. J Bacteriol 163:716–723

    PubMed  CAS  Google Scholar 

  • Sadasivan L, Neyra CA (1987) Cyst production and brown pigment formation in aging cultures of Azospirillum brasilense ATCC 29145. J Bacteriol 169:1670–1677

    PubMed  CAS  Google Scholar 

  • Sadoff HL (1973) Comparative aspects of morphogenesis in three prokaryotic genera. Annu Rev Microbiol 27:133–153

    Article  PubMed  CAS  Google Scholar 

  • Sadoff HL (1975) Encystment and germination in Azotobacter vinelandii. Bacteriol Rev 39:516–539

    PubMed  CAS  Google Scholar 

  • Siam R, Marczynski GT (2002) Glutamate at the phosphorylation site of response regulator CtrA provides essential activities without increasing DNA binding. Nucleic Acids Res 31:1775–1779

    Article  Google Scholar 

  • Stadtwald-Demchick R, Turner FR, Gest H (1990) Physiological properties of the thermotolerant photosynthetic bacterium, Rhodospirillum centenum. FEMS Microbiol Lett 67:139–144

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We thank Jenny Smith and Lissa Mojica for technical assistance. We also thank Carl Bauer and Curtis Loer for helpful comments during the preparation of this manuscript. An Undergraduate Research Fellowship awarded to A. MacKrell by the American Society for Microbiology supported this work.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Terry H. Bird.

Additional information

Communicated by Erko Stackebrandt.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Bird, T.H., MacKrell, A. A CtrA homolog affects swarming motility and encystment in Rhodospirillum centenum . Arch Microbiol 193, 451–459 (2011). https://doi.org/10.1007/s00203-011-0676-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00203-011-0676-y

Keywords

Navigation