Shifts in the Membrane Fatty Acid Profile ofStreptococcus mutansEnhance Survival in Acidic Environments

Abstract

Acid adaptation of Streptococcus mutans UA159 involves several different mechanisms, including the ability to alter its proportion of long-chain, monounsaturated membrane fatty acids (R. G. Quivey, Jr., R. Faustoferri, K. Monahan, and R. Marquis, FEMS Microbiol. Lett. 189:89-92, 2000). In the present study, we examined the mechanism and timing of changes in fatty acid ratios and the potential benefit that an increased proportion of long-chained fatty acids has for the organism during growth at low pH. Cells taken from steady-state cultures at intermediate pH values of 6.5, 6, and 5.5 showed incremental changes from the short-chained, saturated membrane fatty acid profile normally seen in pH 7 cultures to the long-chained, monounsaturated fatty acids more typically observed in acidic cultures (pH 5). Our observations showed that the bacterium was capable of effecting the majority of changes in approximately 20 min, far less than one generation time. However, reversion to the distribution of fatty acids seen in cells growing at a pH of 7 required a minimum of 10 generations. Fatty acid composition analysis of cells taken from cultures treated with chloramphenicol suggested that the changes in fatty acid distribution did not require de novo protein synthesis. Cells treated with the fatty acid biosynthesis inhibitor cerulenin were unable to alter their membrane fatty acid profiles and were unable to survive severe acidification. Results presented here indicate that membrane fatty acid redistribution is important for low pH survival and, as such, is a component of the S. mutans acid-adaptation arsenal.Streptococcus mutans is an etiologic agent of the disease dental caries. The organism resides in supragingival plaque, a biofilm formed above the gumline in the oral cavity. A major characteristic contributing to the organism's pathogenicity is its ability to metabolize many sugars, and as a consequence S. mutans produces various organic acids. Acid production consequently lowers the pH of the surrounding environment, and over time the drop in pH will lead to tooth demineralization and the development of caries. The organism, however, is capable of surviving in low-pH environments and can metabolize glucose and acidify the environment to a pH of 3.5 (3).To withstand the acidification of its environment, S. mutans utilizes a series of adaptive mechanisms, including increases in both the activity and amounts of F 1 F 0 ATPase and a low-pHinducible DNA repair system (22). One of the main defenses against environmental challenges such as acid shock is the bacterial membrane itself. When the total membrane fatty acid content of S. mutans UA159 was examined after the organism had been grown to steady state at pH values of 7 and 5, a major shift in total membrane fatty acid composition was observed wherein cells grown at pH 5 produced a higher proportion of long-chained, monounsaturated fatty acids than cells grown at pH 7 (21). However, the causal relationship between membrane fatty acid changes and resistance to external aci...

Closely related intertidal and deep-sea Halomonhystera species have distinct fatty acid compositions

“…5b) and consisted of C16:1ω7 (32.0 %), C18:1ω9 (51.1 %) and C18:1ω7 (16.8 %). composition is known to rapidly (24-72 h) respond to changes in diet [66] and even daily/hourly fluctuations in FA composition have been observed previously [18,23]. The barrier function of the cytoplasmic membrane is known to depend critically on the physical state of lipid bilayers [11], making it susceptible to environmental changes.…”

Changes in protein expression in Burkholderia vietnamiensis PR1301 at pH 5 and 7 with and without nickel

“…3). In contrast, Fozo & Quivey (2004) observed a decrease in the amount of short-chain saturated fatty acids relative to long-chain monounsaturated fatty acids in Streptococcus mutans as the pH increased from 5 to 6.5. Cells that had shifted to long-chain fatty acids demonstrated increased survival at pH 2.5 compared with cells that were unable to make the shift (Fozo & Quivey, 2004).…”

“…The altered level of 3-oxoacyl-ACP synthase expression suggests that PR1 may be making changes to its membrane. Bacteria are known to modify their cellular membrane structure and composition at acid pH in order to protect the cell (Quivey et al, 2000;Fozo & Quivey, 2004;Leaphart et al, 2006). A more rigid membrane has been observed in acidic environments as a way to reduce proton permeability (Hornbaek et al, 2004).…”

Ultrastructural and physiological changes induced by different stress conditions on the human parasite Trypanosoma cruzi

“…6). In bacteria, a similar phenomenon has been attributed to changes in the lipid composition of the bacterial membrane (Fozo and Quivey 2004;MayorgaReyes et al 2009). In T. cruzi, the inhibition of ergoesterol synthesis, a membrane lipid, induces abnormal morphology of the parasite (Veiga- Santos et al 2012).…”