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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.

Project description:UnlabelledBacterial spore germination is a process whereby a dormant spore returns to active, vegetative growth, and this process has largely been studied in the model organism Bacillus subtilis. In B. subtilis, the initiation of germinant receptor-mediated spore germination is divided into two genetically separable stages. Stage I is characterized by the release of dipicolinic acid (DPA) from the spore core. Stage II is characterized by cortex degradation, and stage II is activated by the DPA released during stage I. Thus, DPA release precedes cortex hydrolysis during B. subtilis spore germination. Here, we investigated the timing of DPA release and cortex hydrolysis during Clostridium difficile spore germination and found that cortex hydrolysis precedes DPA release. Inactivation of either the bile acid germinant receptor, cspC, or the cortex hydrolase, sleC, prevented both cortex hydrolysis and DPA release. Because both cortex hydrolysis and DPA release during C. difficile spore germination are dependent on the presence of the germinant receptor and the cortex hydrolase, the release of DPA from the core may rely on the osmotic swelling of the core upon cortex hydrolysis. These results have implications for the hypothesized glycine receptor and suggest that the initiation of germinant receptor-mediated C. difficile spore germination proceeds through a novel germination pathway.ImportanceClostridium difficile infects antibiotic-treated hosts and spreads between hosts as a dormant spore. In a host, spores germinate to the vegetative form that produces the toxins necessary for disease. C. difficile spore germination is stimulated by certain bile acids and glycine. We recently identified the bile acid germinant receptor as the germination-specific, protease-like CspC. CspC is likely cortex localized, where it can transmit the bile acid signal to the cortex hydrolase, SleC. Due to the differences in location of CspC compared to the Bacillus subtilis germinant receptors, we hypothesized that there are fundamental differences in the germination processes between the model organism and C. difficile. We found that C. difficile spore germination proceeds through a novel pathway.

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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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