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Intracellular membranes of bacterial endospores are reservoirs for spore core membrane expansion during spore germination.

ABSTRACT: Bacterial endospores are formed by certain bacteria, such as Bacillus subtilis or the pathogenic Bacillus anthracis and Clostridioides difficile, to allow survival in environmental conditions which are lethal to vegetative bacteria. The spores possess a particular architecture and molecular inventory which endow them with a remarkable resistance against desiccation, heat and radiation. Another remarkable spore feature is their rapid return to vegetative growth during spore germination and outgrowth. The underlying processes of this latter physiological and morphological transformation involve a number of different events, some of which are mechanistically not entirely understood. One of these events is the expansion of the central spore core, which contains the DNA, RNA and most spore enzymes. To date, it has been unclear how the ~1.3- to 1.6-fold expansion of the core membrane surface area that accompanies core expansion takes place, since this occurs in the absence of significant if any ATP synthesis. In the current work, we demonstrate the presence of intracellular membrane structures in spores located just below the core membrane. During spore germination these internal core membranes disappear when the core size increases, suggesting that they are integrated into the core membrane to allow core expansion. These intracellular membranes are most probably present as more or less compressed vesicles or tubules within the dormant spore core. Investigations of spores from different species suggest that these intracellular membrane structures below the core membrane are a general feature of endospore forming bacteria.

SUBMITTER: Laue M

PROVIDER: S-EPMC6065386 | biostudies-other | 2018 Jul

REPOSITORIES: biostudies-other

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Intracellular membranes of bacterial endospores are reservoirs for spore core membrane expansion during spore germination.

Laue Michael M Han Hong-Mei HM Dittmann Christin C Setlow Peter P

Scientific reports 20180730 1

Bacterial endospores are formed by certain bacteria, such as Bacillus subtilis or the pathogenic Bacillus anthracis and Clostridioides difficile, to allow survival in environmental conditions which are lethal to vegetative bacteria. The spores possess a particular architecture and molecular inventory which endow them with a remarkable resistance against desiccation, heat and radiation. Another remarkable spore feature is their rapid return to vegetative growth during spore germination and outgro ...[more]

PMID: 30061638

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Project description:We present a stochastic mathematical model of the intracellular infection dynamics of Bacillus anthracis in macrophages. Following inhalation of B. anthracis spores, these are ingested by alveolar phagocytes. Ingested spores then begin to germinate and divide intracellularly. This can lead to the eventual death of the host cell and the extracellular release of bacterial progeny. Some macrophages successfully eliminate the intracellular bacteria and will recover. Here, a stochastic birth-and-death process with catastrophe is proposed, which includes the mechanism of spore germination and maturation of B. anthracis. The resulting model is used to explore the potential for heterogeneity in the spore germination rate, with the consideration of two extreme cases for the rate distribution: continuous Gaussian and discrete Bernoulli. We make use of approximate Bayesian computation to calibrate our model using experimental measurements from in vitro infection of murine peritoneal macrophages with spores of the Sterne 34F2 strain of B. anthracis. The calibrated stochastic model allows us to compute the probability of rupture, mean time to rupture, and rupture size distribution, of a macrophage that has been infected with one spore. We also obtain the mean spore and bacterial loads over time for a population of cells, each assumed to be initially infected with a single spore. Our results support the existence of significant heterogeneity in the germination rate, with a subset of spores expected to germinate much later than the majority. Furthermore, in agreement with experimental evidence, our results suggest that most of the spores taken up by macrophages are likely to be eliminated by the host cell, but a few germinated spores may survive phagocytosis and lead to the death of the infected cell. Finally, we discuss how this stochastic modelling approach, together with dose-response data, allows us to quantify and predict individual infection risk following exposure.

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Dataset Information

Intracellular membranes of bacterial endospores are reservoirs for spore core membrane expansion during spore germination.

Publications

Intracellular membranes of bacterial endospores are reservoirs for spore core membrane expansion during spore germination.

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