Acceleration of starvation- and glycerol-induced myxospore formation by prior heat shock in Myxococcus xanthus

Abstract

The effect of heat shock on Myxococcus xanthus was investigated during both glycerol-and starvationinduced development. Cells heat shocked at 40°C for 1 h prior to a development-inducing signal displayed an accelerated rate of myxospore formation at 30°C. Additionally, M. xanthus cells heat shocked prior to glycerol induction formed a greater total number of myxospores when sporulation was complete than did control cells maintained at 30°C. However, in starvation-induced fruiting cells the total number of myxospores in control and heat-shocked populations was about equal when fruiting body and myxospore formation was complete. When extended heat shock (3 h) was applied to cells prior to development, no acceleration of myxospore formation was observed. Heat shock elicited the premature expression of many developmentally regulated proteins. Cell fractionation and analysis by sodium dodecyl sulfate-polyacrylamide gel electrophoresis and fluorography revealed the subcellular location and molecular weights of the 18 glycerol-induced and 9 starvation-induced developmental proteins. Comparison with previously identified M. xanthus heat shock proteins showed that nine of the developmental proteins found in glycerol-induced cells and three of the developmental proteins found in starvation-induced cells were heat shock proteins. Furthermore, heat shock increased the activity of alkaline phosphatase, a developmentally regulated enzyme, in vegetative cells, glycerol-induced cells, and starvation-induced cells.All organisms respond to elevated temperatures by altering their pattern of growth and protein synthesis (16). Upon exposure to elevated temperatures, cells rapidly cease growth, repress the synthesis of most vegetative polypeptides, and coordinately synthesize a small number of different proteins (16). These heat shock proteins (HSPs) may also be induced by other environmental stresses, such as exposure to various alcohols, oxidants (16), and abnormal proteins (1).In many diverse organisms, such as Saccharomyces cerevisiae (13), Drosophila melanogaster (22), and mice (12), some heat shock genes are expressed during particular stages of cellular development. The association of HSPs with certain periods of cellular differentiation suggests that these proteins may be involved in both normal developmental processes and stress responses.Myxococcus xanthus is a gram-negative, rod-shaped, gliding bacterium (9). Although it is a procaryote, it exhibits a complex program of multicellular development. When subjected to starvation on a solid surface, cells migrate inwards towards localized aggregation centers to form raised mounds of cells. Within these mounds, individual cells differentiate to form round, environmentally resistant myxospores. These mounds of cells and spores are termed fruiting bodies (15). This process of fruiting body formation is cell density dependent, includes the temporal expression of proteins such as myxobacterial hemagglutinin (5) and proteins U (11) and S (8), and extends over a 48-to 72-h period (6...

Multiple chaperonins in bacteria—novel functions and non-canonical behaviors

“…Interestingly, major duplication occurs with the genes encoding molecular chaperones, although some of the duplicated paralogs are not heat induced (Otani et al 2001). As observed in the pulse-chase experiments with 35 S-labeled cells during vegetative growth and spore formation stages, heat-shock genes follow social phase-specific expression patterns (Nelson and Killeen 1986;Killeen and Nelson 1988) and probably support the sociality of these organisms (Weimer et al 1998;Yang et al 1998).…”

Characterization of Streptomyces albus 18-kilodalton heat shock-responsive protein

“…The pleiotropic phenotypes of dnaK and groEL mutants and biochemical studies have demonstrated that these proteins have physiologically diverse functions due to their role as molecular chaperones; they mediate the correct assembly of other polypeptides (4). However, some organisms may have adapted HSPs for special requirements; HSPs in some prokaryotic and eukaryotic cells have been shown to play a role during development (11,12,20). Significantly, there are reports indicating induction of GroEL at a crucial point of the Streptomyces cell cycle (5).…”

Heat shock and development induce synthesis of a low-molecular-weight stress-responsive protein in the myxobacterium Stigmatella aurantiaca

“…Heat shock prior to chemical induction of development or starvation leads to accelerated and enhanced spore formation. These effects appear to be dependent on the actual expression of heat shock genes, which might sensitize the cells to other stressors to which they subsequently respond more rapidly (15,20).…”