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Indole-3-acetic acid improves Escherichia coli’s defences to stress

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Abstract

Indole-3-acetic acid (IAA) is a ubiquitous molecule playing regulatory roles in many living organisms. To elucidate the physiological changes induced by IAA treatment, we used Escherichia coli K-12 as a model system. By microarray analysis we found that 16 genes showed an altered expression level in IAA-treated cells. One-third of these genes encode cell envelope components, or proteins involved in bacterial adaptation to unfavourable environmental conditions. We thus investigated the effect of IAA treatment on some of the structural components of the envelope that may be involved in cellular response to stresses. This showed that IAA-treated cells had increased the production of trehalose, lipopolysaccharide (LPS), exopolysaccharide (EPS) and biofilm. We demonstrated further that IAA triggers an increased tolerance to several stress conditions (heat and cold shock, UV-irradiation, osmotic and acid shock and oxidative stress) and different toxic compounds (antibiotics, detergents and dyes) and this correlates with higher levels of the heat shock protein DnaK. We suggest that IAA triggers an increased level of alert and protection against external adverse conditions by coordinately enhancing different cellular defence systems.

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References

  • Ashwell G (1966) Determination of deoxy sugars with 2-thiobarbituric acid. Methods Enzymol 6:89–92

    Google Scholar 

  • Baldi P, Long AD (2001) A bayesian framework for the analysis of microarray expression data: regularized t-test and statistical inferences of gene changes. Bioinformatics 17:509–519

    Article  PubMed  CAS  Google Scholar 

  • Benaroudj N, Lee DH, Goldberg AL (2001) Trehalose accumulation during cellular stress protects cells and cellular proteins from damage by oxygen radicals. J Biol Chem 276:24261–24267

    Article  PubMed  CAS  Google Scholar 

  • Blattner FR, Plunket GR, Bloch CA, Perna NT, Burland V, Riley M et al (1997) The complete genome sequence of Escherichia coli K-12. Science 277:1453–1461

    Article  PubMed  CAS  Google Scholar 

  • Bukau B, Hesterkamp T (1998) Role of DnaK and HscA homologs of Hsp70 chaperones in protein folding in E. coli. EMBO J 17:4818–4828

    Article  PubMed  Google Scholar 

  • Chang YY, Cronan EJ Jr (1999) Membrane cyclopropane fatty acid content is a major factor in acid resistance of Escherichia coli. Mol Microbiol 33:249–259

    Article  PubMed  CAS  Google Scholar 

  • Caldas T, Demont-Caulet N, Ghazi A, Richarme G (1999) Thermoprotection by glycine betaine and choline. Microbiology 145:2543–2548

    PubMed  CAS  Google Scholar 

  • Dalle-Donne I, Rossi R, Giustarini D, Milzani A, Colombo R (2003) Protein carbonyl groups as biomarkers of oxidative stress. Clin Chim Acta 329:23–28

    Article  PubMed  CAS  Google Scholar 

  • Davidson EA (1966) Determination of hexosamine. Methods Enzymol 8:56–60

    Google Scholar 

  • De Felice M, Griffo G, Lago TC, Limanuro D, Ricca E (1986) Detection of the acetolactate synthase isoenzyme I of Escherichia coli. Methods Enzymol 166:241–244

    Article  Google Scholar 

  • De Melo MP, De Lima TM, Pithon-Curi TC, Curi R (2004) The mechanism of indole acetic acid cytotoxicity. Toxicol Lett 148:103–111

    Article  PubMed  CAS  Google Scholar 

  • Deng M, Misra R (1996) Examination of asmA and its effect on the assembly of Escherichia coli outer membrane proteins. Mol Microbiol 21:605–612

    Article  PubMed  CAS  Google Scholar 

  • Diamant S, Eliahu N, Rosenthal D, Goloubinoff P (2001) Chemical chaperones regulate molecular chaperones in vitro and in cells under combined salt and heat stresses. J Biol Chem 276:39586–39591

    Article  PubMed  CAS  Google Scholar 

  • Dubois M, Gilles K, Hamilton JK, Rebers PA, Smith F (1951) A colorimetric method for the determination of sugars. Nature 168:167

    Article  PubMed  CAS  Google Scholar 

  • Edwards MD, Booth IR, Miller S (2004) Gating the bacterial mechanosensitive channel: MscS a new paradigm? Curr Opin Microbiol 7:163–167

    Article  PubMed  CAS  Google Scholar 

  • Ebright RH, Beckwith J (1985) The catabolite gene activator protein (CAP) is not required for indole-3-acetic acid to activate transcription of the araBAD operon of Escherichia coli K-12. Mol Gen Genet 201:51–55

    Article  PubMed  CAS  Google Scholar 

  • Echave P, Esparza-Ceròn MA, Cabiscol E, Tamarit J, Ros J, Membrillo-Hernàndez J, Lin ECC (2002) Dank dependence of mutant ethanol oxidoreductases evolved for aerobic function and protective role of the chaperone against protein oxidative damage in Escherichia coli. Proc Natl Acad Sci USA 99:4626–4631

    Article  PubMed  CAS  Google Scholar 

  • Folkes LK, Greco O, Dachs GU, Stratford MRL, Wardman P (2002) 5-Fluoroindole-3-acetic acid: a prodrug activated by a peroxidase with potential for use in target cancer therapy. Biochem Pharmacol 63:265–272

    Article  PubMed  CAS  Google Scholar 

  • Kandror O, Deleon A, Goldberg AL (2002) Trehalose synthesis is induced upon exposure of Escherichia coli to cold and is essential for viability at low temperatures. Proc Natl Acad Sci USA 99:9727–9732

    Article  PubMed  CAS  Google Scholar 

  • Kaushik JK, Bhat R (2003) Why is trehalose an exceptional protein stabilizer? J Biol Chem 278:26458–26465

    Article  PubMed  CAS  Google Scholar 

  • Kende H, Zeevaart JAD (1997) The five ‘classical’ plant hormones. Plant Cell 9:1197–1210

    Article  PubMed  CAS  Google Scholar 

  • Kline LS, Brown CS, Bankaitis V, Montefiori DC, Craig K (1980) Metabolite gene regulation of the L-arabinose operon in Escherichia coli with indoleacetic acid and other indole derivatives. Proc Natl Acad Sci USA 77:1768–1772

    Article  PubMed  CAS  Google Scholar 

  • Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685

    Article  PubMed  CAS  Google Scholar 

  • Leigh AJ, Signer RE, Walker GC (1985) Exopolysaccharide deficient mutants of Rhizobium meliloti that form ineffective nodules. Proc Natl Acad Sci USA 82:6231–6235

    Article  PubMed  CAS  Google Scholar 

  • Lemcke K, Prinsen E, Van Onckelen H, Schmülling T (2000) The ORF8 gene product of Agrobacterium rhizogenes TL-DNA has tryptophan 2-monooxygenase activity. Mol Plant Microbe Interact 13:787–790

    Article  PubMed  CAS  Google Scholar 

  • Leive L (1965) Release of lipopolysaccharide by EDTA treatment of E. coli. Biochem Biophys Res Commun 21:290–296

    Article  PubMed  CAS  Google Scholar 

  • Lillie SH, Pringle JR (1980) Reserve carbohydrate metabolism in Saccharomyces cerevisiae: responses to nutrient limitation. J Bacteriol 143:1384–1394

    PubMed  CAS  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25:402–408

    Article  PubMed  CAS  Google Scholar 

  • Lodato P, Se govia de Huergo M, Buera MP (1999) viability and thermal stability of a strain of Saccharomyces cerevisiae freeze-dried in different sugar and polymer matrices. Appl Microbiol Biotechnol 52:215–220

    Article  PubMed  CAS  Google Scholar 

  • Mah TF, Pitts B, Pellock B, Walker GC, Stewart PS, O’Toole GA (2001) A genetic basis for Pseudomonas aeruginosa biofilm antibiotic resistance. Nature 426:306–310

    Article  CAS  Google Scholar 

  • Marroquì S, Zorreguieta A, Santamarìa C, Temprano F, Soberòn M, Megìas M, Downie JA (2001) Enhanced symbiotic performance by Rhizobium tropici glycogen synthase mutants. J Bacteriol 183:854–864

    Article  PubMed  Google Scholar 

  • Morimoto RI (1993) Cells in stress: transcriptional activation of heat shock genes. Science 259:1409–1410

    Article  PubMed  CAS  Google Scholar 

  • Nikaido H (1976) Outer membrane of Salmonella typhimurium: transmembrane diffusion of some hydrophobic substances. Biochim Biophys Acta 433:118–132

    Article  PubMed  CAS  Google Scholar 

  • Osborn MJ (1963) Studies on the gram-negative cell wall. Biochemistry 50:499–506

    CAS  Google Scholar 

  • Polissi A, De Laurentis W, Zangrossi S, Briani F, Longhi V, Pesole G, Dehò G (2003) Res Microbiol 154:573–580

    Article  PubMed  CAS  Google Scholar 

  • Prusty R, Grisafi P, Fink GR (2004) The plant hormone indoleacetic acid induces invasive growth in Saccharomyces cerevisiae. Proc Natl Acad Sci USA 101:4153–4157

    Article  PubMed  CAS  Google Scholar 

  • Purvis JE, Yomano LP, Ingram LO (2005) Enhanced trehalose production improves growth of Escherichia coli under osmotic stress. Appl Environ Microbiol 71:3761–3769

    Article  PubMed  CAS  Google Scholar 

  • Rezuchova B, Miticka H, Homerova D, Roberts M, Kormanec J (2003) New members of the Escherichia coli δE regulon identified by a two-plasmid system. FEMS Microbiol Lett 225:1–7

    Article  PubMed  CAS  Google Scholar 

  • Stepanovic S, Vucovic D, Dakin I, Savic B, Svabic-Vlahovic M (2000) A modified microtiter-plate test for quantification of staphylococcal biofilm formation. J Microbiol Methods 40:175–179

    Article  PubMed  CAS  Google Scholar 

  • Saviozzi S, Iazzetti G, Caserta E, Guffanti A, Calogero RA (2004) Microarray data analysis and mining. Methods Mol Med 94:67–90

    PubMed  CAS  Google Scholar 

  • Singer AM, Lindquist S (1998) Thermotolerance in Saccharomyces cerevisiae: the Yin and Yang of trehalose. Trends Biotechnol 16:460–468

    Article  PubMed  CAS  Google Scholar 

  • Sukupolvi S, Vaara M, Helander IL, Viljanen P, Makela H (1984) New Salmonella typhimurium mutants with altered outer membrane permeability. J Bacteriol 159:704–712

    PubMed  CAS  Google Scholar 

  • Tamarit J, Cabiscol E, Ros J (1998) Identification of the major oxidatively damaged proteins in Escherichia coli cells exposed to oxidative stress. J Biol Chem 273:3027–3032

    Article  PubMed  CAS  Google Scholar 

  • Tusher VG, Tibshirani R, Chu G (2001) Significance analysis of microarrays applied to the ionising radiation response. Proc Natl Acad Sci USA 98:5116–5121

    Article  PubMed  CAS  Google Scholar 

  • Yoda K, Kawada T, Kaibara A, Fujie A, Abe M, Hashimoto H et al (2000) Biochi Biotechnol Biochem 64:1937–1941

    Article  CAS  Google Scholar 

  • Zimmer W, Wesche M, Timmermans L (1998) Identification and isolation of the indole-3-pyruvate decarboxylase gene from Azospirillum brasilense Sp7: sequencing and functional analysis of the gene locus. Curr Microbiol 36:327–331

    Article  PubMed  CAS  Google Scholar 

  • Zou Y, Crowley DJ, Houten BT (1998) Involvement of molecular chaperonins in nucleotide excision repair. J Biol Chem 276:12887–12892

    Article  Google Scholar 

Download references

Acknowledgements

We wish to thank S. Adhya and the E. coli Genetic Stock Centre for providing bacterial strains. We acknowledge A. Spena and J. Beckwith for their helpful discussion, C. Sole and R. Vito for technical assistance. This work was supported by the European Union INCO-DEV SONGLINES grant, project ICA4-CT-2001-10059 and by Italian MIUR, project FIRB RBNE0118BHE. We are grateful to P. De Luca (BioGEM Ariano Irpino-AV) and S. Crispi (IGB-Naples) who carried out the arrays hybridization and scanning.

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Bianco, C., Imperlini, E., Calogero, R. et al. Indole-3-acetic acid improves Escherichia coli’s defences to stress. Arch Microbiol 185, 373–382 (2006). https://doi.org/10.1007/s00203-006-0103-y

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  • DOI: https://doi.org/10.1007/s00203-006-0103-y

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