Analysis of Organic Solvent Tolerance in Escherichia coli Using Gene Expression Profiles from DNA Microarrays

HAYASHI, SHUHEI; Aono, Rikizo; HANAI, TAIZO; Mori, Hirotada; Kobayashi, T.; Honda, Hiroyuki

doi:10.1263/jbb.95.379

Cited by 8 publications

(7 citation statements)

References 12 publications

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“…2) and also identified an isopropylmalate dehydrogenase (CAC0970) adjacent to aconitase (CAC0971) to be part of the specific butanol-stress response. Glycerol metabolism genes have been implicated with hexane tolerance in the solvent-tolerant E. coli strain OST3410 which expresses the glycerol metabolism genes glpB, glpC (both are glycerol-3-phosphate dehydrogenase subunits), glpF (glycerol uptake facilitator), and glpQ (glycerophosphoryl diester phophodiesterase) higher than the parent strain JA300, and also upregulated expression of these genes in OST3410 following hexane stress (Hayashi et al, 2003), while higher expression of glpC has also been observed in other solvent-tolerant E. coli strains following treatment with xylene and cyclohexane (Shimizu et al, 2005). We observed differential upregulation of a glycerol uptake facilitator (glpF, CAC1319) and a glycerol-3-phosphate dehydrogenase (glpA, CAC1322) following butanol stress in C. acetobutylicum, suggesting a conserved mechanism of solvent tolerance.…”

Section: Genes Specific To the Butanol-stress Responsementioning

confidence: 99%

“…Mechanisms of solvent and carboxylic acid toxicity/stress have been studied mostly in Gram-negative (Gram À ) organisms and notably in Escherichia coli (Arnold et al, 2001;Chang and Cronan, 1999;Hayashi et al, 2003;Isken and de Bont, 1998;Kirkpatrick et al, 2001;Roe et al, 2002;Russell and Diez-Gonzalez, 1998;Sardessai and Bhosle, 2002;Zaldivar and Ingram, 1999). For example, Gram À organisms have evolved adaptive mechanisms to tolerate solvents, including alterations in cell membrane, active secretion, and activation of general stress response (Isken and de Bont, 1998;Sardessai and Bhosle, 2002).…”

Section: Introductionmentioning

confidence: 99%

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Metabolite stress and tolerance in the production of biofuels and chemicals: Gene‐expression‐based systems analysis of butanol, butyrate, and acetate stresses in the anaerobe Clostridium acetobutylicum

Alsaker

Paredes

Papoutsakis

2010

Biotech & Bioengineering

202

189

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Metabolite accumulation has pleiotropic, toxic, or beneficial effects on cell physiology, but such effects are not well understood at the molecular level. Cells respond and adapt to metabolite stress by mechanisms largely unexplored, especially in the context of multiple and simultaneous stresses. Solventogenic and related clostridia have an inherent advantage for production of biofuels and chemicals directly from cellulosic material and other complex carbohydrates, but issues of product/metabolite tolerance and related culture productivities remain. Using DNA microarray-based gene expression analysis, the transcriptional-stress responses of Clostridium acetobutylicum to fermentation acids acetate and butyrate and the solvent product butanol were analyzed and compared in the context of cell physiology. Ontological analysis demonstrated that stress by all three metabolites resulted in upregulation of genes related to post-translational modifications and chaperone activity, and downregulation of the translationmachinery genes. Motility genes were downregulated by acetate-stress only. The general metabolite stress included upregulation of numerous stress genes (dnaK, groES, groEL, hsp90, hsp18, clpC, and htrA), the solventogenic operon aad-ctfA-ctfB, and other solventogenic genes. Acetate stress downregulated expression of the butyryl-CoA-and butyrate-formation genes, while butyrate stress downregulated expression of acetate-formation genes. Pyrimidine-biosynthesis genes were downregulated by most stresses, but purine-biosynthesis genes were upregulated by acetate and butyrate, possibly for thiamine and histidine biosynthesis. Methionine-biosynthesis genes were upregulated by acetate stress, indicating a possibly conserved stress response mechanism also observed in Escherichia coli. Nitrogen-fixation gene expression was upregulated by acetate stress. Butyrate stress upregulated many iron-metabolism genes, riboflavin-biosynthesis genes, and several genes related to cellular repair from oxidative stress, such as perR and superoxide dismutases. Butanol stress upregulated the glycerol metabolism genes glpA and glpF. Surprisingly, metabolite stress had no apparent effect on the expression of the sporulation-cascade genes. It is argued that the list of upregulated genes in response to the three metabolite stresses includes several genes whose overexpression would likely impart tolerance, thus making the information generated in this study, a valuable source for the development of tolerant recombinant strains.

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Section: Genes Specific To the Butanol-stress Responsementioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Metabolite stress and tolerance in the production of biofuels and chemicals: Gene‐expression‐based systems analysis of butanol, butyrate, and acetate stresses in the anaerobe Clostridium acetobutylicum

Alsaker

Paredes

Papoutsakis

2010

Biotech & Bioengineering

202

189

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“…Upregulation of gene expression, increased synthesis and/or enhanced stress tolerance associated with diverse chaperonins, heat-shock proteins and other protein-stabilization proteins (e.g. CspA, DnaJ, DnaK, GroEL, GroES, GrpE, HtpX, IbpA, HtpG, HSIV, HSIU, trigger protein) in response to toluene and xylene in P. putida (Segura et al, 2005;Dominguez-Cuevas et al, 2006;Volkers et al, 2006;Ballerstedt et al, 2007), benzene and hexane in E. coli (Hs1J, HtpX, IbpAB; Blom et al, 1992;Hayashi et al, 2003), biphenyl in B. xenovorans (Denef et al, 2004) and octanol and pentane in S. cerevisiae (see Fujita et al, 2004). (Similar responses are seen in mammalian cells in response to benzene and Lindane; e.g.…”

Section: Protein Stabilizationmentioning

confidence: 99%

Hydrophobic substances induce water stress in microbial cells

Bhaganna

Volkers

Bell

et al. 2010

Microbial Biotechnology

121

185

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SummaryUbiquitous noxious hydrophobic substances, such as hydrocarbons, pesticides and diverse industrial chemicals, stress biological systems and thereby affect their ability to mediate biosphere functions like element and energy cycling vital to biosphere health. 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. These findings suggest that it may be possible to devise new interventions for microbial processes in both natural environments and industrial reactors to expand microbial tolerance of hydrophobic substances, and hence the biotic windows for such processes.

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“…We have studied OST mechanisms of E. coli using a DNA microarray (10,11). Many genes were induced 30 min after exposure to organic solvents and one of the up-regulated genes, glpC, increased the OST of E. coli (10).…”

mentioning

confidence: 99%

Time-course data analysis of gene expression profiles reveals purR regulon concerns in organic solvent tolerance in Escherichia coli

Shimizu

Hayashi

Doukyu

et al. 2005

Journal of Bioscience and Bioengineering

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Analysis of Organic Solvent Tolerance in Escherichia coli Using Gene Expression Profiles from DNA Microarrays

Cited by 8 publications

References 12 publications

Metabolite stress and tolerance in the production of biofuels and chemicals: Gene‐expression‐based systems analysis of butanol, butyrate, and acetate stresses in the anaerobe Clostridium acetobutylicum

Metabolite stress and tolerance in the production of biofuels and chemicals: Gene‐expression‐based systems analysis of butanol, butyrate, and acetate stresses in the anaerobe Clostridium acetobutylicum

Hydrophobic substances induce water stress in microbial cells

Time-course data analysis of gene expression profiles reveals purR regulon concerns in organic solvent tolerance in Escherichia coli

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