Membrane cyclopropane fatty acid content is a major factor in acid resistance of Escherichia coli

Abstract

Cyclopropane fatty acid (CFA) formation is a post‐synthetic modification of the lipid bilayer that occurs as cultures of Escherichia coli and many other bacteria enter stationary phase. We report the first distinct phenotype for this membrane modification; early stationary phase cultures of strains lacking CFA (as a result of a null mutation in the cfa gene) are abnormally sensitive to killing by a rapid shift from neutral pH to pH 3. This sensitivity to acid shock is dependent on CFA itself because resistance to acid shock is restored to cfa mutant strains by incorporation of CFAs from the growth medium or by introduction of a functional cfa gene on a plasmid. The synthesis of CFA depends in part on the RpoS sigma factor, but the role of RpoS in resistance to acid shock involves additional factors because strains with null mutations in both cfa and rpoS are more sensitive to acid shock than either single mutant strain. Exponential phase cultures of E. coli are much more sensitive to acid shock than stationary phase cultures, but survival is greatly increased if the exponential phase cultures are exposed to moderately acid conditions (pH 5) before shift to pH 3. We show that exposure to moderately acid conditions gives a marked increase in cfa transcription. The efficiency of the survival of acid shock is extremely strain dependent, even among putative wild‐type strains. Much, but not all, of this variability can be explained by the partially or totally defective RpoS alleles carried by many strains.

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

“…In E. coli, acetate treatment induces cfa expression (Arnold et al, 2001), and deletion increases acid-stress sensitivity (Chang and Cronan, 1999). In C. acetobutylicum, the cfa gene is differentially upregulated following acetate stress.…”

“…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).…”

Global transcriptome response to ionic liquid by a tropical rain forest soil bacterium,Enterobacter lignolyticus

“…However, the increase in cyclopropane fatty acid production during [C 2 mim]Cl exposure demonstrates the distinct effect of ionic liquid on the bacterium. A number of studies using E. coli and lactobacilli have demonstrated that methylation of the cis-acyl chain double bond to form a cyclopropane ring plays a significant role in tolerance to acid, salt, butanol, and other stressors by reducing membrane fluidity and decreasing permeability (50)(51)(52)(53)(54). It is probable that cyclopropane fatty acid production plays a similar role in [C 2 mim]Cl tolerance by stabilizing the cell membrane.…”

Cyclopropane fatty acyl synthase in Sinorhizobium meliloti

“…While the biological roles of CFAs in bacteria are not completely understood (Cronan, 2002), it has been demonstrated that cyclopropane-containing lipids protect bacteria from adverse conditions such as acidity (Ballen et al, 1998;Brown et al, 1997;Chang & Cronan, 1999;Kim et al, 2005), freeze-drying (Munoz-Rojas et al, 2006), desiccation (Boumahdi et al, 2001) and exposure to pollutants (Fang et al, 2007;Mrozik et al, 2005Mrozik et al, , 2006. There is some debate as to whether an increase in cyclopropane content of bacterial membranes leads to a decrease in membrane fluidity (Loffhagen et al, 2007;Munoz-Rojas et al, 2006).…”