Abstract
Alkylhydroxybenzenes (AHB) were found to control the activation of protective functions of microorganisms by inducing stress gene expression and increasing the frequency of the intrapopulation phase transitions which are responsible for the phenotypic variability of bacteria. We established the dependence of the regulatory effects of AHB on their structure (alkyl radical length) and concentration. A reversion assay using the tryptophan auxotrophic strain Bacillus subtilis trpA5 B 1733 indicated a relationship between the reversion frequency that was 40–120 times higher than the background value and phase transition’s intensity (with R → S transition rates up to 87% in contrast to 2% in the control experiment) induced by specific doses (5–100 mg/ml) of long-chain AHB such as C12-AHB acting for a short time (1 h) on vegetative (dividing or stationary-phase) B. subtilis cells. Using four test strains constructed from Escherichia coli C600 thi, thr, leuΔ(pro-lac) with transcriptional or translational vectors containing the hybrid umuD-lacZ or osmE-lacZ operons, we demonstrated that AHB perform the regulatory functions involved in controlling the SOS response gene expression and the general rpoS -dependent stationary-phase regulon, respectively. The dose-dependent effect of long-chain AHB (within the 50–100 µg/ml range) resulting in a two- to threefold increase in the stress gene expression, similar to the effect of natural stress factors such as UV irradiation and starvation, provides evidence that AHB function as alarmones (danger signals). From the fact that the osm E gene is upregulated by 35–70 µg/ml C12-AHB (its regulation level is increased up to twofold), it follows that C12-AHB controls rpoS-dependent regulation and the transition to the stationary phase. The effect of the short-chain homologue C7-AHB substantially differs from that of C12-AHB. C7-AHB in concentrations of 10–100µg/ml causes a significant decrease in osmE and umuD expression. A 30-min preincubation of cells with 10–100µg/ml C7-AHB protected them from UV irradiation, as was observed as a 3.6-fold decrease in umuD expression. Comparative analysis of the marker gene’s expression values in the strains with the transcriptional and translational vectors demonstrates that AHB nonspecifically activate stress regulons at the transcription level.
Similar content being viewed by others
References
Hersh, M.N., Ponder, R.G., Hastings, P.J., and Rosenberg, S.M., Adaptive Mutation and Amplification in Escherichia coli: Two Pathways of Genome Adaptation Under Stress, Res. Microbiol., 2004, vol. 255, pp. 352–359.
Woude van der, M.V. and Baumler, A.J., Phase and Antigenic Variation in Bacteria, Clin. Microbiol. Rev., 2004, vol. 17, no. 3, pp. 581–611.
Aersten, A. and Michirlis, C.W., Diversify or Die: Generation of Diversity in Response to Stress, Crit. Rev. Microbiol, 2005, vol. 31, pp. 69–78.
Foster, P.L., Stress Induced Mutagenesis in Bacteria, Crit. Rev. Biochem. Mol. Biol., 2007, vol. 42, pp. 373–397.
Aburatani, S. and Horimoto, K., Elucidation of the Relationships Between LexA-Regulated Genes in the SOS Response, Genome Inform., 2005, vol. 16, no. 1, pp. 95–105.
Saint-Ruf, C., Pesut, J., Sopta, M., and Matic, I., Causes and Consequences of DNA Repair Activity Modulation during Stationary, Crit. Rev. Biochem. Mol. Biol., 2007, vol. 42, pp. 259–270.
Huisman, G.W. and Kolter, R., Sensing Starvation: A Homoserine Lactone-Dependent Signaling Pathway in Escherichia coli, Science, 1994, vol. 265, pp. 537–539.
El’-Registan, G.I., Mulyukin, A.L., Nikolaev, Yu.A., Suzina, N.E., Gal’chenko, V.F., and Duda, V.I., Adaptogenic Functions of Extracellular Autoregulators of Microorganisms, Mikrobiologiya, 2006, vol. 75, no. 4, pp. 446–456 [Microbiology (Engl. Transl.), vol. 75, no. 4, pp. 380–389].
Prozorov, A.A., Recombinational Rearrangements in Bacterial Genome and Bacterial Adaptation to the Environment, Mikrobiologiya, 2001, vol. 70, no. 5, pp. 581–594 [Microbiology (Engl. Transl.), vol. 70, no. 5, pp. 501–511].
Frenkiel-Krispin, D., Levin-Zaidman, S., Shimoni, E., Wolf, S.A., Wachtel, E.T., Arad, T., Finkel, S.E., Kolter, R., and Minsky, A., Regulated Phase Transition of Bacterial Chromatin: A Non-Enzymatic Pathway for Generic DNA Protection, The EMBO J., 2001, vol. 20, pp. 1184–1191.
Doroshenko, E.V., Loiko, N.G., Il’inskaya, O.N., Kolpakov, A.N., Gornova, N.B., Klimanova, E.V., and El’-Registan, G.I., Characterization of Bacillus cereus Dissociants, Mikrobiologiya, 2001, vol. 70, no. 6, pp. 811–819 [Microbiology (Engl. Transl.), vol. 70, no. 6, pp. 698–705].
Il’inskaya, O.N., Kolpakov, A.I., Zelenikhin, P.V., Kruglova, Z.F., Choidash, B., Doroshenko, E.V., Mulyukin, A.L., and El’-Registan, G.I., The Effect of Anabiosis Autoinducers on the Bacterial Genome, Mikrobiologiya, 2002, vol. 71, no. 2, pp. 194–199 [Microbiology (Engl. Transl.), vol. 71, no. 2, pp. 164–168].
Mulyukin, A.L., Vakhrushev, M.A., Strazhevskaya, N.B., Shmyrina, A.S., Zhdanov, R.I., Suzina, N.E., Duda, V.I., Kozlova, A.N., and El’-Registan, G.I., Effect of Alkylhydroxybenzenes, Microbial Anabiosis Inducers, on the Structural Organization of Pseudomonas aurantiaca DNA and on the Induction of Phenotypic Dissociation, Mikrobiologiya, 2005, vol. 74, no. 2, pp. 128–135 [Microbiology (Engl. Transl.), vol. 74, no. 2, pp. 128–135].
Stepanenko, I.Yu., Mulyukin, A.L, Kozlova, A.N., Nikolaev, Yu.A., and El’-Registan, G.I., The Role of Alkylhydroxybenzenes in the Adaptation of Micrococcus luteus to Heat Shock, Mikrobiologiya, 2005, vol. 74, no. 1, pp. 26–33 [Microbiology (Engl. Transl.), vol. 74, no. 1, pp. 20–26].
El-Registan, G.I., Mulyukin, A.L., Nikolaev, Yu.A., Stepanenko, I.Yu., Kozlova, A.N., Martirosova, E.I., Shanenko, E.F., Strakhovskaya, M.G., and Revina, A.A., The Role of Low-Molecular-Weight Autoregulatory Factors (Alkylhydroxybenzenes) in Resistance to Radiation and Heat Shock, Adv. Space Res., 2005, vol. 36, pp. 1718–1728.
Martirosova, E.I., Karpekina, T.A., and El’-Registan, G.I., Enzyme Modification by Natural Chemical Chaperons of Microorganisms, Mikrobiologiya, 2004, vol. 73, no. 5, pp. 708–715 [Microbiology (Engl. Transl.), vol. 73, no. 5, pp. 609–615].
Martirosova, E.I., Nikolaev, Yu.A., Shanenko, E.F., Krupyanskii, Yu.F., Loiko, N.G., and El’-Registan, G.I., Application of Hydroxybenzenes for Enhancing Enzyme Activity and Stability, Khim. Tekhnol., 2007, no. 6, pp. 250–256.
Davydova, O.K., Deryabin, D.G., and El’-Registan, G.I., Long-Term Preservation of DNA in Aqueous Solutions in the Presence of the Chemical Analogues of Microbial Autoregulators, Mikrobiologiya, 2006, vol. 75, no. 5, pp. 662–669 [Microbiology (Engl. Transl.), vol. 75, no. 5, pp. 575–581].
Kozubek, A. and Tyman, H.P., Resorcinolic Lipids, the Natural Non-Isoprenoid Phenolic Amphiphiles and Their Biological Activity, Chem. Rev., 1999, vol. 99, no. 1, pp. 1–31.
Zolotukhina, M., Ovcharova, I., Eremina, S., Errais, L., and Mironov, A.S., Comparison of the Structure and Regulation of the udp Gene of Vibrio cholerae, Yersinia pseudotuberculisis, Salmonella typhimurium, and Escherichia coli, Res. Microbiol., 2003, vol. 154, no. 7, pp. 510–520.
Miller, J.H., Experiments in Molecular Genetics, Cold Spring Harbor: Cold Spring Harbor Laboratories, 1972.
Strazhevskaya, N.B., Mulyukin, A.L., Shmyrina, A.S., Kraus, A., Lorents, V., Zhdanov, R.I., and El’-Registan, G.I., Characteristics of Pseudomonas aurantiaca DNA Supramolecular Complexes at Various Developmental Stages, Mikrobiologiya, 2009, vol. 78, no. 1, pp. 59–67 [Microbiology (Engl. Transl.), vol. 78, no. 1, pp. 48–55].
Margulis, A.B., Il’inskaya, O.N., Kolpakov, A.I., and El’-Registan, G.I., Induction of SOS Response by Autoregulatory Factors of Microorganisms, Genetika, 2003, vol. 39, no. 9, pp. 1180–1184 [Russ. J. Genetics (Engl. Transl.), vol. 39, no. 9, pp. 993–996].
Burke, P.V., Raitt, D.C., Allen, L.A., Kellogg, F.A., and Poyton, R.O., Effect of Oxygen Concentration on the Expression of Cytochrome c and Cytochrome c Oxidase Genes in Yeast, J. Biol. Chem., 1997, vol. 272, pp. 14705–14712.
Singh, U.S., Scannel, R.T., An, H.Y., Carter, B.J., and Hecht, S.M., DNA Cleavage by Di- and Tryhydroxyalkylbenzenes. Caracterization of Products and Role of O2, Cu(II) and Alkali, J. Am. Chem. Soc., 1995, vol. 117, pp. 12691–12699.
Petrovskii, A.S., Deryabin, D.G., Loiko, N.G., Mikhailenko, N.A., Kobzeva, T.G., Kanaev, P.A., Nikolaev, Yu.A., Krupyanskii, Yu.F., Kozlova, A.N., and El’-Registan, G.I., Regulation of the Functional Activity of Lysozyme by Alkylhydroxybenzenes, Mikrobiologiya, 2009, vol. 78, no. 2, pp. 176–185 [Microbiology (Engl. Transl.), vol. 78, no. 2, pp. 144–153].
Friedberg, E.C., Walker, G.C., and Siede, W., DNA Repair and Mutagenesis, Washington, DC: ASM Press, 1995, p. 698.
Oktyabr’skii, O.N. and Smirnova, G.V., Redox Regulation of Cellular Functions, Biokhimiya, 2007, vol. 72, no. 2, pp. 158–174 [Biochemistry (Moscow) (Engl. Transl.), vol. 72, no. 2, pp. 132–145].
Claycamp, H.G., Ho, K.K., and De Rose, C., Tiol and Hydrogen Peroxide Modification of RecA Induction in UV-Irradiation Wild Type and Catalse Deficient Escherichia coli K12, Mutat. Res., 1990, vol. 235, pp. 101–109.
Author information
Authors and Affiliations
Corresponding author
Additional information
Original Russian Text © N.A. Golod, N.G. Loiko, K.V. Lobanov, A.S. Mironov, T.A. Voieikova, V.F. Gal’chenko, Yu.A. Nikolaev, G.I. El’-Registan, 2009, published in Mikrobiologiya, 2009, Vol. 78, No. 6, pp. 731–741.
Rights and permissions
About this article
Cite this article
Golod, N.A., Loiko, N.G., Lobanov, K.V. et al. Involvement of alkylhydroxybenzenes, microbial autoregulators, in controlling the expression of stress regulons. Microbiology 78, 678–688 (2009). https://doi.org/10.1134/S0026261709060034
Received:
Published:
Issue Date:
DOI: https://doi.org/10.1134/S0026261709060034