Correlation of intracellular trehalose concentration with desiccation resistance of soil Escherichia coli populations

Abstract

Naturalized soil Escherichia coli populations need to resist common soil desiccation stress in order to inhabit soil environments. In this study, four representative soil E. coli strains and one lab strain, MG1655, were tested for desiccation resistance via die-off experiments in sterile quartz sand under a potassium acetate-induced desiccation condition. The desiccation stress caused significantly lower die-off rates of the four soil strains (0.17 to 0.40 day(-1)) than that of MG1655 (0.85 day(-1)). Cellular responses, including extracellular polymeric substance (EPS) production, exogenous glycine betaine (GB) uptake, and intracellular compatible organic solute synthesis, were quantified and compared under the desiccation and hydrated control conditions. GB uptake appeared not to be a specific desiccation response, while EPS production showed considerable variability among the E. coli strains. All E. coli strains produced more intracellular trehalose, proline, and glutamine under the desiccation condition than the hydrated control, and only the trehalose concentration exhibited a significant correlation with the desiccation-contributed die-off coefficients (Spearman's ρ = -1.0; P = 0.02). De novo trehalose synthesis was further determined for 15 E. coli strains from both soil and nonsoil sources to determine its prevalence as a specific desiccation response. Most E. coli strains (14/15) synthesized significantly more trehalose under the desiccation condition, and the soil E. coli strains produced more trehalose (106.5 ± 44.9 μmol/mg of protein [mean ± standard deviation]) than the nonsoil reference strains (32.5 ± 10.5 μmol/mg of protein).

Fig 1

An example of the ¹H NMR spectra of intracellular organic solutes of soil E. coli strain S-B54 under the desiccation stress.

Fig 2

Reduction of culturable E. coli cells as a result of dessication in quartz sand microcosms over time. C_d represents the E. coli concentration under the dessication condition, and C_w represents the E. coli concentration under the hydrated control condition. The bar graph shows the change of water content in the dessicated microcosms. Error bars show standard errors of the means from triplicate microcosms.

Fig 3

Concentration of GB taken up by the E. coli strains under the desiccated condition (solid bars) and the hydrated condition (open bars). Error bars are the standard errors of the means from triplicate tests.

Fig 4

Production of EPS by the E. coli strains under the desiccated condition (solid bars) and the hydrated condition (open bars). Error bars are the standard errors of the means from triplicate tests.

Fig 5

Intracellular concentrations of trehalose in 10 soil E. coli strains (designated with an S), four E. coli isolates from municipal wastewater (designated by WW), and the lab strain MG1655 under the desiccation condition (solid bars) or the hydrated condition (open bars).