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The physical state of water in bacterial spores.

ABSTRACT: 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 D(2)O-exchanged Bacillus subtilis spores over a wide frequency range. The data indicate high water mobility throughout the spore, comparable with binary protein-water 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.

SUBMITTER: Sunde EP

PROVIDER: S-EPMC2780810 | biostudies-literature | 2009 Nov

REPOSITORIES: biostudies-literature

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The physical state of water in bacterial spores.

Sunde Erik P EP Setlow Peter P Hederstedt Lars L Halle Bertil B

Proceedings of the National Academy of Sciences of the United States of America 20091105 46

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 D(2)O-exchanged Bacillus subtilis spores over a wid ...[more]

PMID: 19892742

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Project description:UnlabelledBacterial spores, despite being metabolically dormant, possess the remarkable capacity to detect nutrients and other molecules in their environment through a biochemical sensory apparatus that can trigger spore germination, allowing the return to vegetative growth within minutes of exposure of germinants. We demonstrate here that bacterial spores of multiple species retain memory of transient exposures to germinant stimuli that can result in altered responses to subsequent exposure. The magnitude and decay of these memory effects depend on the pulse duration as well as on the separation time, incubation temperature, and pH values between the pulses. Spores of Bacillus species germinate in response to nutrients that interact with germinant receptors (GRs) in the spore's inner membrane, with different nutrient types acting on different receptors. In our experiments, B. subtilis spores display memory when the first and second germinant pulses target different receptors, suggesting that some components of spore memory are downstream of GRs. Furthermore, nonnutrient germinants, which do not require GRs, exhibit memory either alone or in combination with nutrient germinants, and memory of nonnutrient stimulation is found to be more persistent than that induced by GR-dependent stimuli. Spores of B. cereus and Clostridium difficile also exhibit germination memory, suggesting that memory may be a general property of bacterial spores. These observations along with experiments involving strains with mutations in various germination proteins suggest a model in which memory is stored primarily in the metastable states of SpoVA proteins, which comprise a channel for release of dipicolinic acid, a major early event in spore germination.ImportanceCellular memory is defined as a sustained response to a transient environmental stimulus, and yet its generation and storage have not been described in bacterial spores. We demonstrate here that bacterial spores of multiple species retain memory of transient exposures to germinant stimuli that can result in altered responses to subsequent exposure. Memory was induced by activation of germinant receptors (GRs) or by GR-independent germinants and was accessed by both GR-dependent and GR-independent germinants. Analysis of effects on memory of exposure to GR-dependent and GR-independent germinants as well as in spores lacking various germination proteins suggests a model in which memory is stored primarily in metastable states of SpoVA proteins which comprise a channel for release of spore dipicolinic acid. Spore memory can also significantly reduce the concentration of nutrient germinants necessary to trigger germination, and this may be used to respond to low levels of nutrient germinants.

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The physical state of water in bacterial spores.

Publications

The physical state of water in bacterial spores.

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