Effects of intracellular trehalose content on Streptomyces griseus spores

Abstract

The disaccharide trehalose is accumulated as a storage product by spores of Streptomyces griseus. Growth on media containing excess glucose yielded spores containing up to 25% of their dry weight as trehalose. Spores containing as little as 1% of their dry weight as trehalose were obtained during growth on media containing a limiting amount of glucose. Spores containing low levels of trehalose accumulated this sugar when incubated with glucose. The increase in trehalose content coincided with increases in spore refractility, heat resistance, desiccation resistance, and the time required for spore germination in complex media. Trehalose is accumulated by a wide variety of actinomycetes and related bacteria and may be partially responsible for their resistance properties.The life cycle of members of the genus Streptomyces is characterized by vegetative mycelial growth followed by the formation of chains of unicellular spores (15,19). These spores are dormant cells which are relatively resistant to desiccation, sonic vibration, enzymatic digestion, and exposure to moderately high temperatures.Trehalose (a-D-glucopyranosyl-a-D-glucopyranoside) is an important storage compound of the streptomycetes (12) and is particularly abundant in spores (4,15). Trehalose is also a common reserve material in the dormant spores and cysts of fungi and other lower eucaryotic organisms (7,13). The accumulation of trehalose sugar by a wide variety of desiccation-resistant eucaryotic and procaryotic organisms suggests that the sugar may play some common role associated with the resistance properties of these organisms. The level of resistance to heat or desiccation of a variety of organisms correlates with their trehalose content (5,7,14,39). Trehalose protects biological membranes against the deleterious effects of dehydration (7). The resistance properties of the organisms that accumulate this sugar may be attributed in part to this protective interaction.Streptomyces spores provide an interesting experimental system for studying trehalose accumulation and catabolism. The trehalose content of streptomycete spores varies with the sporulation conditions (20,22 10 mM MOPS buffer (pH 7.0). Spores were incubated in the germination medium at a final concentration of 2 x 108/ml at 33°C for 3 to 4 h. The germinated spores were harvested by centrifugation, washed 3 times with 10 mM MOPS buffer (pH 7.0), and inoculated into DMC at a final concentration of 5 x 106 spores per ml. All cultures were incubated at 30°C unless stated otherwise.Mycelia were harvested from liquid culture by centrifugation for 10 min at 10,000 x g at 4°C. Spores were harvested from solid media as described previously (18)

Trehalose accumulation in vegetative cells and spores of Myxococcus xanthus

“…Identification of trehalose in glycerol-induced spores was originally based on enzymatic analyses and paper chromatography (11). We verified that the accumulated sugar was trehalose by 13C NMR spectroscopy.…”

“…They lack components of the thick spore coat and are not as resistant as fruiting body spores (8,16). The presence of large amounts of the disaccharide trehalose in glycerolinduced spores has been previously reported (11). In this study we examined the accumulation of trehalose by vegetative cells, glycerol-induced spores, and fruiting body * Corresponding author.…”

“…Glycerol-induced spores are metabolically and structurally different from spores formed in fruiting bodies on a solid surface (8 In other organisms increased trehalose content is associated with elevated levels of resistance to heat and desiccation (1,11). The spores of M. xanthus are more resistant than vegetative cells to heat and desiccation (16).…”

“…Trehalose is found in the spores or cysts of a variety of organisms, including actinomycetes, fungi, nematodes, and brine shrimp (1,5,11). Trehalose content has been correlated with the heat or desiccation resistance of several of these organisms (1,11) and has been demonstrated to protect membranes in vitro from the deleterious effects of dehydration (1).…”

“…Trehalose content has been correlated with the heat or desiccation resistance of several of these organisms (1,11) and has been demonstrated to protect membranes in vitro from the deleterious effects of dehydration (1). Considerable evidence indicates that the hydroxyl groups of trehalose interact with the phosphate head groups of membrane phospholipids (1)(2)(3)10).…”