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Protective role of glycerol against benzene stress: insights from the Pseudomonas putida proteome

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Abstract

Chemical activities of hydrophobic substances can determine the windows of environmental conditions over which microbial systems function and the metabolic inhibition of microorganisms by benzene and other hydrophobes can, paradoxically, be reduced by compounds that protect against cellular water stress (Bhaganna et al. in Microb Biotechnol 3:701–716, 2010; Cray et al. in Curr Opin Biotechnol 33:228–259, 2015a). We hypothesized that this protective effect operates at the macromolecule structure–function level and is facilitated, in part at least, by genome-mediated adaptations. Based on proteome profiling of the soil bacterium Pseudomonas putida, we present evidence that (1) benzene induces a chaotrope-stress response, whereas (2) cells cultured in media supplemented with benzene plus glycerol were protected against chaotrope stress. Chaotrope-stress response proteins, such as those involved in lipid and compatible-solute metabolism and removal of reactive oxygen species, were increased by up to 15-fold in benzene-stressed cells relative to those of control cultures (no benzene added). By contrast, cells grown in the presence of benzene + glycerol, even though the latter grew more slowly, exhibited only a weak chaotrope-stress response. These findings provide evidence to support the hypothesis that hydrophobic substances induce a chaotropicity-mediated water stress, that cells respond via genome-mediated adaptations, and that glycerol protects the cell’s macromolecular systems. We discuss the possibility of using compatible solutes to mitigate hydrocarbon-induced stresses in lignocellulosic biofuel fermentations and for industrial and environmental applications.

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Notes

  1. That is, their adverse impacts on the cell typically result from chaotropic activity (Bhaganna et al. 2010; McCammick et al. 2010; Cray et al. 2013b, 2014, 2015a; Ball and Hallsworth 2015).

  2. See Hallsworth and Magan (1994, 1995), Sauer and Galinski (1998), Cray et al. (2013a, 2015a), Kar et al. ( 2015), Rangel et al. (2015a).

  3. In other words, there was an apparent cessation of biotic activity (NB stressor concentrations at which metabolic activity and cell division cease and at which death occurs can differ; see Santos et al. 2015).

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Acknowledgments

This project was carried out within the research program of the Kluyver Centre for Genomics of Industrial Fermentation which is part of the Netherlands Genomics Initiative/Netherlands Organization for Scientific Research, the EU-funded MIFRIEND and LINDANE projects, a Beaufort Marine Research Award for Marine Biodiscovery (Marine Institute, Ireland), and a Biotechnology and Biological Sciences Research Council-funded project (UK; Grant No. BBF0034711) which is part of the Pseudomonas putida Systems Biology of Microorganisms project (PSYSMO). We are grateful for useful discussions with Giuseppe Albano (Edinburgh University, UK), Philip G. Hamill, Luke Morton, Allen Y. Mswaka, Andrew Stevenson, and Dave J. Timson, (Queen’s University Belfast), Victor de Lorenzo (Centro Nacional de Biotecnología, CSIC, Spain), Terry J. McGenity and Jen Waring (University of Essex), Mary Palfreyman (Outwood Grange College, UK), and Kenneth N. Timmis (Helmholtz Centre for Infection Research, Germany).

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  1. Agata Bielecka

    Present address: Molecular Biology Department, Helmholtz Centre for Infection Research, D-38124, Braunschweig, Germany

  2. Gabriella Molinari

    Present address: Central Facility for Microscopy, Helmholtz Centre for Infection Research, D-38124, Braunschweig, Germany

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  1. MBC, School of Biological Sciences, Institute for Global Food Security, Queen’s University Belfast, Belfast, BT9 7BL, Ireland

    Prashanth Bhaganna & John E. Hallsworth

  2. Environmental Microbiology Laboratory, Helmholtz Centre for Infection Research, D-38124, Braunschweig, Germany

    Agata Bielecka & Gabriella Molinari

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Bhaganna, P., Bielecka, A., Molinari, G. et al. Protective role of glycerol against benzene stress: insights from the Pseudomonas putida proteome. Curr Genet 62, 419–429 (2016). https://doi.org/10.1007/s00294-015-0539-1

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  • Issue Date:

  • DOI: https://doi.org/10.1007/s00294-015-0539-1

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