Glassy State in Bacterial Spores Predicted by Polymer Glass‐Transition Theory

Sapru, V.; Labuza, Ted P

doi:10.1111/j.1365-2621.1993.tb04294.x

Cited by 74 publications

(41 citation statements)

References 30 publications

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“…If this is the case, then enzyme action in the spore core would be precluded further by the prevention of interaction of enzymes and their small molecule substrates. Indeed, as noted above there is evidence that has been interpreted as indicating that at least ions in the dormant spore core are immobile and that the spore core is in a glass-like state (9)(10)(11)(12)(13). In any event, the environment within the core of the dormant and stage I-germinated spore is a very special and unique one, and the features of this environment clearly contribute to the dormancy as well as the resistance of the dormant spore.…”

Section: Resultsmentioning

confidence: 99%

“…However, it is certainly possible that the amount of water in the spore core is too low to allow sufficient macromolecular movement for enzyme action. Indeed, there are data that have been interpreted as indicating that (i) ions in the spore core are relatively immobile (9,10), and (ii) the dormant spore core is in a glass-like state (11)(12)(13). In addition, the levels of DPA in the spore core are far above its solubility, and available data indicate that at least the great majority of spore DPA is not in solution (14,15).…”

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confidence: 99%

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A soluble protein is immobile in dormant spores of Bacillus subtilis but is mobile in germinated spores: Implications for spore dormancy

Cowan

Koppel²,

Setlow³

et al. 2003

Proc. Natl. Acad. Sci. U.S.A.

143

116

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Fluorescence redistribution after photobleaching has been used to show that a cytoplasmic GFP fusion is immobile in dormant spores of Bacillus subtilis but becomes freely mobile in germinated spores in which cytoplasmic water content has increased Ϸ2-fold. The GFP immobility in dormant spores is not due to the high levels of dipicolinic acid in the spore cytoplasm, because GFP was also immobile in germinated cwlD spores that had excreted their dipicolinic acid but where cytoplasmic water content had only increased to a level similar to that in dormant spores of several other Bacillus species. The immobility of a normally mobile protein in dormant wild-type spores and germinated cwlD spores is consistent with the lack of metabolism and enzymatic activity in these spores and suggests that protein immobility, presumably due to low water content, is a major reason for the metabolic dormancy of spores of Bacillus species.S pores of various Bacillus species are formed in the process of sporulation, and these spores are adapted for long-term survival because they are resistant to many environmental stresses and are metabolically dormant (1-4). However, given the proper stimulus, generally the appearance of specific nutrients in the environment, the dormant spores can return to life through the process of spore germination and then outgrowth (2). A major factor in spore dormancy and resistance is the low level of water in the spore cytoplasm or core [25-55% of the mass of the hydrated dormant spore core depending on the species (1, 3-5)]; another factor may be the high level of pyridine-2,6-dicarboxylic acid [dipicolinic acid (DPA)] (Ϸ10% of the mass of the hydrated stage II-germinated spore core) in the spore core, likely present as a chelate with divalent cations, predominantly Ca 2ϩ (1,6). DPA is released in the first minutes of spore germination and is replaced with water as the spore-core water content rises slightly; these spores are said to have completed stage I of germination (2, 7). Subsequently, the large peptidoglycan cortex around the spore core is degraded, and removal of this restraint allows the spore core to expand rapidly by uptake of water and thus complete stage II of germination (2, 7). This latter event results in a level of core water (75-80% of wet weight) that is similar to that in growing cells (8). As noted above, there is neither metabolism nor enzyme action in the cytoplasm of dormant spores, although there are several enzyme-substrate pairs located in this region of the spore (3). There is also no detectable metabolism or enzyme action in the core of stage I-germinated spores that have excreted their DPA but have not degraded their cortex (7). However, in fully germinated (stage II) spores in which the cortex has been degraded and the cytoplasm is fully hydrated, enzyme action and metabolism begin rapidly (2).One explanation that has been put forward for the lack of enzyme action in dormant and stage I-germinated spores is that the level of water in these spores is too low to allow enzyme a...

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Section: Resultsmentioning

confidence: 99%

mentioning

confidence: 99%

A soluble protein is immobile in dormant spores of Bacillus subtilis but is mobile in germinated spores: Implications for spore dormancy

Cowan

Koppel²,

Setlow³

et al. 2003

Proc. Natl. Acad. Sci. U.S.A.

143

116

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“…Anhydrobiotic organisms-including plant seeds, yeast cells, and certain plants and invertebrates-achieve dormancy by replacing most of the cell water by compatible osmolytes, such as trehalose or sucrose, thereby transforming the cytoplasm into a metastable glassy state (5,6). Although bacterial spores do not accumulate glass-forming osmolytes, it has been proposed that the spore's core region is also in a glassy state (7)(8)(9). If so, spore dormancy could simply be attributed to the extreme retardation of diffusive molecular motions in the highly viscous glass state.…”

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confidence: 99%

The physical state of water in bacterial spores

Sunde

Setlow

Hederstedt

et al. 2009

Proc. Natl. Acad. Sci. U.S.A.

153

155

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The bacterial spore, the hardiest known life form, can survive in a metabolically dormant state for many years and can withstand high temperatures, radiation, and toxic chemicals. The molecular basis of spore dormancy and resistance is not understood, but the physical state of water in the different spore compartments is thought to play a key role. To characterize this water in situ, we recorded the water 2 H and 17 O spin relaxation rates in D2O-exchanged Bacillus subtilis spores over a wide frequency range. The data indicate high water mobility throughout the spore, comparable with binary proteinwater systems at similar hydration levels. Even in the dense core, the average water rotational correlation time is only 50 ps. Spore dormancy therefore cannot be explained by glass-like quenching of molecular diffusion but may be linked to dehydration-induced conformational changes in key enzymes. The data demonstrate that most spore proteins are rotationally immobilized, which may contribute to heat resistance by preventing heat-denatured proteins from aggregating irreversibly. We also find that the water permeability of the inner membrane is at least 2 orders of magnitude lower than for model membranes, consistent with the reported high degree of lipid immobilization in this membrane and with its proposed role in spore resistance to chemicals that damage DNA. The quantitative results reported here on water mobility and transport provide important clues about the mechanism of spore dormancy and resistance, with relevance to food preservation, disease prevention, and astrobiology.Bacillus subtilis ͉ hydration ͉ magnetic relaxation dispersion ͉ spore dormancy ͉ spore resistance

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“…Formerly, it was interpreted in terms of a polymer glass-transition [45]. In this framework, the spores would remain in their dormant glassy state until melting and energy adsorption would occur at the endothermic transition temperature.…”

Section: Discussionmentioning

confidence: 99%

Proton dynamics in bacterial spores, a neutron scattering investigation

Noue

Peters

Gervais

et al. 2015

EPJ Web of Conferences

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Abstract.Results from first neutron scattering experiments on bacterial spores are reported. The elastic intensities and mean square displacements have a non-linear behaviour as function of temperature, which is in agreement with a model presenting more pronounced variations at around 330 K (57• C) and 400 K (127 • C). Based on the available literature on thermal properties of bacterial spores, mainly referring to differential scanning calorimetry, they are suggested to be associated to main endothermic transitions induced by coat and/or core bacterial response to heat treatment.

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Glassy State in Bacterial Spores Predicted by Polymer Glass‐Transition Theory

Cited by 74 publications

References 30 publications

A soluble protein is immobile in dormant spores of Bacillus subtilis but is mobile in germinated spores: Implications for spore dormancy

A soluble protein is immobile in dormant spores of Bacillus subtilis but is mobile in germinated spores: Implications for spore dormancy

The physical state of water in bacterial spores

Proton dynamics in bacterial spores, a neutron scattering investigation

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