Skip to main content
Log in

Chromobacterium violaceum adaptation to low-phosphate conditions

  • Original Paper
  • Published:
Archives of Microbiology Aims and scope Submit manuscript

Abstract

Chromobacterium violaceum is a free-living bacterium that inhabits low-nutrient environments such as the Amazon basin. Bacteria respond to phosphate (Pi) shortage by expressing a range of genes involved in Pi uptake and assimilation, known as the PHO regulon. Several PHO regulon genes have been annotated in the genome of C. violaceum. Here we show that C. violaceum is extremely well adapted to low-Pi conditions. Remarkably, this bacterium is able to grow in media containing only traces of Pi. The PHO regulon genes are induced upon Pi depletion, but the bacteria continued to grow under these conditions. Unlike other Proteobacteria hitherto analyzed, neither PstS nor PhoU play a role in the repression of the PHO regulon under Pi excess.

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

Similar content being viewed by others

References

  • Aguena M, Yagil E, Spira B (2002) Transcriptional analysis of the pst operon of Escherichia coli. Mol Genet Genomics 268(4):518–524

    Article  CAS  PubMed  Google Scholar 

  • Aguena M, Ferreira GM, Spira B (2009) Stability of the pstS transcript of Escherichia coli. Arch Microbiol 191(2):105–112

    Article  CAS  PubMed  Google Scholar 

  • Alexeyev MF (1999) The pKNOCK series of broad-host-range mobilizable suicide vectors for gene knockout and targeted DNA insertion into the chromosome of gram-negative bacteria. Biotechniques 26(5):824–826

    CAS  PubMed  Google Scholar 

  • Braibant M, Lefèvre P, de Wit L, Peirs P, Ooms J, Huygen K, Andersen AB, Content JA (1996) Mycobacterium tuberculosis gene cluster encoding proteins of a phosphate transporter homologous to the Escherichia coli Pst system. Gene 176(1–2):171–176

    Article  CAS  PubMed  Google Scholar 

  • Burut-Archanai S, Incharoensakdi A, Eaton-Rye JJ (2009) The extended n-terminal region of SphS is required for detection of external phosphate levels in Synechocystis sp. Pcc 6803. Biochem Biophys Res Commun 378(3):383–388

    Article  CAS  PubMed  Google Scholar 

  • Carmany DO, Hollingsworth K, McCleary WR (2003) Genetic and biochemical studies of phosphatase activity of PhoR. J Bacteriol 185(3):1112–1115

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ciprandi A, da Silva WM, Santos AV, de Castro Pimenta AM, Carepo MSP, Schneider MPC, Azevedo V, Silva A (2013) Chromobacterium violaceum: important insights for virulence and biotechnological potential by exoproteomic studies. Curr Microbiol 67(1):100–106

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Consortium BNGP (2003) The complete genome sequence of Chromobacterium violaceum reveals remarkable and exploitable bacterial adaptability. Proc Natl Acad Sci USA 100(20):11660–11665

    Article  Google Scholar 

  • de Almeida LG, Ortiz JH, Schneider RP, Spira B (2015) phoU inactivation in Pseudomonas aeruginosa enhances accumulation of ppGpp and polyphosphate. Appl Environ Microbiol 81(9):3006–3015

    Article  PubMed  PubMed Central  Google Scholar 

  • Diaz M, Esteban A, Fernandez-Abalos JM, Santamaria RI (2005) The high-affinity phosphate-binding protein PstS is accumulated under high fructose concentrations and mutation of the corresponding gene affects differentiation in Streptomyces lividans. Microbiology 151(Pt 8):2583–2592

    Article  CAS  PubMed  Google Scholar 

  • Franceschini A, Szklarczyk D, Frankild S, Kuhn M, Simonovic M, Roth A, Lin J, Minguez P, Bork P, von Mering C, Jensen LJ (2013) String v9.1: protein-protein interaction networks, with increased coverage and integration. Nucleic Acids Res 41(Database issue):D808–D815

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Galbiati HF, Taschner NP, Spira B (2014) The effect of the rpoSam allele on gene expression and stress resistance in Escherichia coli. Arch Microbiol 196(8):589–600

    Article  CAS  PubMed  Google Scholar 

  • Gardner SG, Johns KD, Tanner R, McCleary WR (2014) The PhoU protein from Escherichia coli interacts with PhoR, PstB, and metals to form a phosphate-signaling complex at the membrane. J Bacteriol 196(9):1741–1752

    Article  PubMed  PubMed Central  Google Scholar 

  • Geiger O, Röhrs V, Weissenmayer B, Finan TM, Thomas-Oates JE (1999) The regulator gene phoB mediates phosphate stress-controlled synthesis of the membrane lipid diacylglyceryl-n, n, n-trimethylhomoserine in Rhizobium (Sinorhizobium) meliloti. Mol Microbiol 32(1):63–73

    Article  CAS  PubMed  Google Scholar 

  • Gober JW, Shapiro L (1992) A developmentally regulated Caulobacter flagellar promoter is activated by 3′ enhancer and IHF binding elements. Mol Biol Cell 3(8):913–926

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hungria M, Astolfi-Filho S, Chueire LMO, Nicolás MF, Santos EBP, Bulbol MR, Souza-Filho A, Nogueira Assunção E, Germano MG, Vasconcelos ATR (2005) Genetic characterization of Chromobacterium isolates from black water environments in the Brazilian Amazon. Lett Appl Microbiol 41(1):17–23

    Article  CAS  PubMed  Google Scholar 

  • Jacobsen SM, Lane MC, Harro JM, Shirtliff ME, Mobley HL (2008) The high-affinity phosphate transporter Pst is a virulence factor for Proteus mirabilis during complicated urinary tract infection. FEMS Immunol Med Microbiol 52(2):180–193

    Article  CAS  PubMed  Google Scholar 

  • Lubin EA, Henry JT, Fiebig A, Crosson S, Laub MT (2015) Identification of the PhoB regulon and role of PhoU in the phosphate-starvation response of Caulobacter crescentus. J Bacteriol 198(1):187–200

    Article  PubMed  Google Scholar 

  • Luz DE, Nepomuceno RSL, Spira B, Ferreira RCC (2012) The Pst system of Streptococcus mutans is important for phosphate transport and adhesion to abiotic surfaces. Mol Oral Microbiol 27(3):172–181

    Article  CAS  PubMed  Google Scholar 

  • Makino K, Shinagawa H, Amemura M, Kawamoto T, Yamada M, Nakata A (1989) Signal transduction in the phosphate regulon of Escherichia coli involves phosphotransfer between PhoR and PhoB proteins. J Mol Biol 210(3):551–559

    Article  CAS  PubMed  Google Scholar 

  • McClain ME, Victoria RL, Richey JE (2001) The biogeochemistry of the Amazon basin. Oxford University Press, New York

    Google Scholar 

  • Miller JH (1992) A short course in bacterial genetics: a laboratory manual and handbook for Escherichia coli and related bacteria. Cold Spring Harbor Laboratory, Cold Spring Harbor

    Google Scholar 

  • Muda M, Rao NN, Torriani A (1992) Role of PhoU in phosphate transport and alkaline phosphatase regulation. J Bacteriol 174(24):8057–8064

    CAS  PubMed  PubMed Central  Google Scholar 

  • Neidhardt FC, Bloch PL, Smith DF (1974) Culture medium for enterobacteria. J Bacteriol 119(3):736–747

    CAS  PubMed  PubMed Central  Google Scholar 

  • Nikata T, Sakai Y, Shibat K, Kato J, Kuroda A, Ohtake H (1996) Molecular analysis of the phosphate-specific transport (pst) operon of Pseudomonas aeruginosa. Mol Gen Genet 250(6):692–698

    CAS  PubMed  Google Scholar 

  • Poole K, Hancock RE (1984) Phosphate transport in Pseudomonas aeruginosa. involvement of a periplasmic phosphate-binding protein. Eur J Biochem 144(3):607–612

    Article  CAS  PubMed  Google Scholar 

  • Qi Y, Kobayashi Y, Hulett FM (1997) The pst operon of Bacillus subtilis has a phosphate-regulated promoter and is involved in phosphate transport but not in regulation of the pho regulon. J Bacteriol 179(8):2534–2539

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rice P, Longden I, Bleasby A (2000) Emboss: the European molecular biology open software suite. Trends Genet 16(6):276–277

    Article  CAS  PubMed  Google Scholar 

  • Sambrook J, Russell DW (2001) Molecular cloning: a laboratory manual, vol 999. Cold Spring Harbor Laboratory Press, Cold Spring Harbor

    Google Scholar 

  • Scholten M, Tommassen J (1993) Topology of the phor protein of escherichia coli and functional analysis of internal deletion mutants. Mol Microbiol 8(2):269–275

    Article  CAS  PubMed  Google Scholar 

  • Shinagawa H, Makino K, Nakata A (1983) Regulation of the pho regulon in Escherichia coli k-12. genetic and physiological regulation of the positive regulatory gene phoB. J Mol Biol 168(3):477–488

    Article  CAS  PubMed  Google Scholar 

  • Simon R, Priefer U, Pühler A (1983) A broad host range mobilization system for in vivo genetic engineering: transposon mutagenesis in gram negative bacteria. Nat Biotechnol 1(9):784–791

    Article  CAS  Google Scholar 

  • Smil V (2000) Phosphorus in the environment: natural flows and human interferences. Ann Rev Energy Environ 25:53–88

    Article  Google Scholar 

  • Spira B, Yagil E (1999) The integration host factor (IHF) affects the expression of the phosphate-binding protein and of alkaline phosphatase in Escherichia coli. Curr Microbiol 38(2):80–85

    Article  CAS  PubMed  Google Scholar 

  • Spira B, Silberstein N, Yagil E (1995) Guanosine 3′,5′-bispyrophosphate (ppGpp) synthesis in cells of Escherichia coli starved for Pi. J Bacteriol 177(14):4053–4058

    CAS  PubMed  PubMed Central  Google Scholar 

  • Spira B, Aguena M, de Castro Oliveira JV, Yagil E (2010) Alternative promoters in the pst operon of Escherichia coli. Mol Genet Genomics 284(6):489–498

    Article  CAS  PubMed  Google Scholar 

  • Steed PM, Wanner BL (1993) Use of the rep technique for allele replacement to construct mutants with deletions of the pstSCAB-phoU operon: evidence of a new role for the PhoU protein in the phosphate regulon. J Bacteriol 175(21):6797–6809

    CAS  PubMed  PubMed Central  Google Scholar 

  • Surin BP, Rosenberg H, Cox GB (1985) Phosphate-specific transport system of Escherichia coli: nucleotide sequence and gene-polypeptide relationships. J Bacteriol 161(1):189–198

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wang L, Spira B, Zhou Z, Feng L, Maharjan RP, Li X, Li F, C McKenzie, Reeves PR, Ferenci T (2010) Divergence involving global regulatory gene mutations in an Escherichia coli population evolving under phosphate limitation. Genome Biol Evol 2:478–487

    Article  PubMed  PubMed Central  Google Scholar 

  • Wanner BL (1996) Phosphorus assimilation and control of the phosphate regulon. In: Neidhardt NC, Curtiss R, III, Ingraham JL, Lin ECC, Low KB, Magasanik B, Reznikoff WS, Riley M, Schaechter M, Umbarger HE (eds) Escherichia coli and Salmonella: cellular and molecular biology, 2nd edn. American Society for Microbiology, Washington, DC, pp 1357–1381

    Google Scholar 

  • Wanner BL, Wilmes-Riesenberg MR (1992) Involvement of phosphotransacetylase, acetate kinase, and acetyl phosphate synthesis in control of the phosphate regulon in Escherichia coli. J Bacteriol 174(7):2124–2130

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wu H, Kosaka H, Kato J, Kuroda A, Ikeda T, Takiguchi N, Ohtake H (1999) Cloning and characterization of Pseudomonas putida genes encoding the phosphate-specific transport system. J Biosci Bioeng 87(3):273–279

    Article  CAS  PubMed  Google Scholar 

  • Yu CS, Chen YC, Lu CH, Hwang JK (2006) Prediction of protein subcellular localization. Proteins 64(3):643–651

    Article  CAS  PubMed  Google Scholar 

  • Yuan ZC, Zaheer R, Morton R, Finan TM (2006) Genome prediction of PhoB regulated promoters in Sinorhizobium meliloti and twelve proteobacteria. Nucleic Acids Res 34(9):2686–2697  

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

We are grateful to Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP) and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for supporting this study. F.N.V. was supported by FAPESP scholarship 2009/05265-7.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Beny Spira.

Additional information

Communicated by Erko Stackebrandt.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 59 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

da Costa Vasconcelos, F.N., Padilla, G. & Spira, B. Chromobacterium violaceum adaptation to low-phosphate conditions. Arch Microbiol 198, 269–277 (2016). https://doi.org/10.1007/s00203-016-1188-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00203-016-1188-6

Keywords

Navigation