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Hydrophobic substances induce water stress in microbial cells.

Bhaganna P, Volkers RJ, Bell AN, Kluge K, Timson DJ, McGrath JW, Ruijssenaars HJ, Hallsworth JE - Microb Biotechnol (2010)

Bottom Line: Such chemically diverse compounds may have distinct toxic activities for cellular systems; they may also share a common mechanism of stress induction mediated by their hydrophobicity.We hypothesized that the stressful effects of, and cellular adaptations to, hydrophobic stressors operate at the level of water : macromolecule interactions.Here, we present evidence that: (i) hydrocarbons reduce structural interactions within and between cellular macromolecules, (ii) organic compatible solutes - metabolites that protect against osmotic and chaotrope-induced stresses - ameliorate this effect, (iii) toxic hydrophobic substances induce a potent form of water stress in macromolecular and cellular systems, and (iv) the stress mechanism of, and cellular responses to, hydrophobic substances are remarkably similar to those associated with chaotrope-induced water stress.

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Affiliation: Department of Biological Sciences, University of Essex, Colchester CO4 3SQ, UK.

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Intracellular compatible‐solute contents of exponentially growing cells of P. putida (A and B) in minimal mineral‐salt media (at 30°C; see Fig. 2C) supplemented with (A) toluene and (B) 2,5‐dichlorophenol; and those of A. penicillioides (C and D) on MYPiA+sucrose (1.64 M, at 15°C; see Fig. S2) medium supplemented with (C) benzene and (D) octanol over a range of concentrations. Compatible solutes were (◊) glycerol, (▵) mannitol and () trehalose. Plotted values are means of triplicate experiments, and standard deviations are shown.
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f6: Intracellular compatible‐solute contents of exponentially growing cells of P. putida (A and B) in minimal mineral‐salt media (at 30°C; see Fig. 2C) supplemented with (A) toluene and (B) 2,5‐dichlorophenol; and those of A. penicillioides (C and D) on MYPiA+sucrose (1.64 M, at 15°C; see Fig. S2) medium supplemented with (C) benzene and (D) octanol over a range of concentrations. Compatible solutes were (◊) glycerol, (▵) mannitol and () trehalose. Plotted values are means of triplicate experiments, and standard deviations are shown.

Mentions: There are numerous studies of microbial activity in the presence of hydrophilic chaotropes that either correlate stressor tolerance with compatible‐solute concentration (e.g. Hallsworth, 1998; Hallsworth et al., 2003b), or demonstrate the upregulation of genes involved in compatible‐solute synthesis (e.g. Alexandre et al., 2001; Kurbatov et al., 2006; van Voorst et al., 2006; see also Table 2). We searched for evidence that compatible solutes protect diverse microbial species from stress induced by hydrophobic stressor and/or that such stressors (log P > 1.95) can upregulate the synthesis of intracellular compatible solutes. Surprisingly, we found a substantial number of studies that demonstrated a role for compatible solutes in hydrocarbon‐stressed cells for diverse bacterial species as well as the yeast Saccharomyces cerevisiae (for a selection of these see Table 2). We stressed cells of P. putida by culturing them in the presence of diverse hydrophobic stressors – benzene, toluene and 2,5‐dichlorophenol – over a range of concentrations, and harvested cells during the exponential growth phase to analyse compatible‐solute content (Fig. 6A and B). Intriguingly we only found one compatible solute, trehalose, that was synthesized and accumulated in response to toluene (Fig. 6A) but not benzene (data not shown) or 2,5‐dichlorophenol (Fig. 6B). Moreover, the accumulation of trehalose correlated with an unusually high toluene tolerance considering the high log P value of the latter (see Fig. 1B). Despite the comparable hydrophobicity of toluene and 2,5‐dichlorophenol, the trehalose‐protected cells were able to tolerate up to ≈ 4.5 mM toluene whereas the low‐trehalose cells in 2,5‐dichlorophenol‐supplemented media were unable to grow above 0.9 mM 2,5‐dichlorophenol (Fig. 2C). Generally, induction of compatible‐solute synthesis in response to turgor changes occurs at water activity values ≤ 0.985 (F.L. Alves and J.E. Hallsworth, unpubl. data) and toluene is therefore insufficiently soluble – by an order of magnitude – to generate an osmotic stress. The toluene‐induced accumulation of trehalose correlated with evidence that toluene upregulates genes involved in trehalose synthesis (e.g. Park et al., 2007).


Hydrophobic substances induce water stress in microbial cells.

Bhaganna P, Volkers RJ, Bell AN, Kluge K, Timson DJ, McGrath JW, Ruijssenaars HJ, Hallsworth JE - Microb Biotechnol (2010)

Intracellular compatible‐solute contents of exponentially growing cells of P. putida (A and B) in minimal mineral‐salt media (at 30°C; see Fig. 2C) supplemented with (A) toluene and (B) 2,5‐dichlorophenol; and those of A. penicillioides (C and D) on MYPiA+sucrose (1.64 M, at 15°C; see Fig. S2) medium supplemented with (C) benzene and (D) octanol over a range of concentrations. Compatible solutes were (◊) glycerol, (▵) mannitol and () trehalose. Plotted values are means of triplicate experiments, and standard deviations are shown.
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Related In: Results  -  Collection

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f6: Intracellular compatible‐solute contents of exponentially growing cells of P. putida (A and B) in minimal mineral‐salt media (at 30°C; see Fig. 2C) supplemented with (A) toluene and (B) 2,5‐dichlorophenol; and those of A. penicillioides (C and D) on MYPiA+sucrose (1.64 M, at 15°C; see Fig. S2) medium supplemented with (C) benzene and (D) octanol over a range of concentrations. Compatible solutes were (◊) glycerol, (▵) mannitol and () trehalose. Plotted values are means of triplicate experiments, and standard deviations are shown.
Mentions: There are numerous studies of microbial activity in the presence of hydrophilic chaotropes that either correlate stressor tolerance with compatible‐solute concentration (e.g. Hallsworth, 1998; Hallsworth et al., 2003b), or demonstrate the upregulation of genes involved in compatible‐solute synthesis (e.g. Alexandre et al., 2001; Kurbatov et al., 2006; van Voorst et al., 2006; see also Table 2). We searched for evidence that compatible solutes protect diverse microbial species from stress induced by hydrophobic stressor and/or that such stressors (log P > 1.95) can upregulate the synthesis of intracellular compatible solutes. Surprisingly, we found a substantial number of studies that demonstrated a role for compatible solutes in hydrocarbon‐stressed cells for diverse bacterial species as well as the yeast Saccharomyces cerevisiae (for a selection of these see Table 2). We stressed cells of P. putida by culturing them in the presence of diverse hydrophobic stressors – benzene, toluene and 2,5‐dichlorophenol – over a range of concentrations, and harvested cells during the exponential growth phase to analyse compatible‐solute content (Fig. 6A and B). Intriguingly we only found one compatible solute, trehalose, that was synthesized and accumulated in response to toluene (Fig. 6A) but not benzene (data not shown) or 2,5‐dichlorophenol (Fig. 6B). Moreover, the accumulation of trehalose correlated with an unusually high toluene tolerance considering the high log P value of the latter (see Fig. 1B). Despite the comparable hydrophobicity of toluene and 2,5‐dichlorophenol, the trehalose‐protected cells were able to tolerate up to ≈ 4.5 mM toluene whereas the low‐trehalose cells in 2,5‐dichlorophenol‐supplemented media were unable to grow above 0.9 mM 2,5‐dichlorophenol (Fig. 2C). Generally, induction of compatible‐solute synthesis in response to turgor changes occurs at water activity values ≤ 0.985 (F.L. Alves and J.E. Hallsworth, unpubl. data) and toluene is therefore insufficiently soluble – by an order of magnitude – to generate an osmotic stress. The toluene‐induced accumulation of trehalose correlated with evidence that toluene upregulates genes involved in trehalose synthesis (e.g. Park et al., 2007).

Bottom Line: Such chemically diverse compounds may have distinct toxic activities for cellular systems; they may also share a common mechanism of stress induction mediated by their hydrophobicity.We hypothesized that the stressful effects of, and cellular adaptations to, hydrophobic stressors operate at the level of water : macromolecule interactions.Here, we present evidence that: (i) hydrocarbons reduce structural interactions within and between cellular macromolecules, (ii) organic compatible solutes - metabolites that protect against osmotic and chaotrope-induced stresses - ameliorate this effect, (iii) toxic hydrophobic substances induce a potent form of water stress in macromolecular and cellular systems, and (iv) the stress mechanism of, and cellular responses to, hydrophobic substances are remarkably similar to those associated with chaotrope-induced water stress.

View Article: PubMed Central - PubMed

Affiliation: Department of Biological Sciences, University of Essex, Colchester CO4 3SQ, UK.

Show MeSH
Related in: MedlinePlus