The extent of the temperature-induced membrane remodeling in two closely related Bordetella species reflects their adaptation to diverse environmental niches

Abstract

Changes in environmental temperature represent one of the major stresses faced by microorganisms as they affect the function of the cytoplasmic membrane. In this study, we have analyzed the thermal adaptation in two closely related respiratory pathogens <i>Bordetella pertussis</i> and <i>Bordetella bronchiseptica</i> Although <i>B. pertussis</i> represents a pathogen strictly adapted to the human body temperature, <i>B. bronchiseptica</i> causes infection in a broad range of animals and survives also outside of the host. We applied GC-MS to determine the fatty acids of both <i>Bordetella</i> species grown at different temperatures and analyzed the membrane fluidity by fluorescence anisotropy measurement. In parallel, we also monitored the effect of growth temperature changes on the expression and production of several virulence factors. In response to low temperatures, <i>B. pertussis</i> adapted its fatty acid composition and membrane fluidity to a considerably lesser extent when compared with <i>B. bronchiseptica</i> Remarkably, <i>B. pertussis</i> maintained the production of virulence factors at 24 °C, whereas <i>B. bronchiseptica</i> cells resumed the production only upon temperature upshift to 37 °C. This growth temperature-associated differential modulation of virulence factor production was linked to the phosphorylation state of transcriptional regulator BvgA. The observed differences in low-temperature adaptation between <i>B. pertussis</i> and <i>B. bronchiseptica</i> may result from selective adaptation of <i>B. pertussis</i> to the human host. We propose that the reduced plasticity of the <i>B. pertussis</i> membranes ensures sustained production of virulence factors at suboptimal temperatures and may play an important role in the transmission of the disease.