Absence of oxygen affects the capacity to sporulate and the spore properties of Bacillus cereus

Abbas, Amina Aicha; Planchon, Stella; Jobin, Michel-Philippe; Schmitt, Philippe

doi:10.1016/j.fm.2014.03.004

Cited by 31 publications

(16 citation statements)

References 64 publications

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“…Regulation of exosporium formation warrants further investigation. Recently, it was discovered that production of spores of a particular strain of B. cereus under conditions of anaerobiosis resulted in defects in the exosporium structure (206). Based on what we know regarding spore formation by B. anthracis, it could be anticipated that reduced oxygen tension might result in reduced sporulation efficiencies.…”

Section: Discussionmentioning

confidence: 99%

The Exosporium Layer of Bacterial Spores: a Connection to the Environment and the Infected Host

Stewart

2015

Microbiol Mol Biol Rev

138

155

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SUMMARYMuch of what we know regarding bacterial spore structure and function has been learned from studies of the genetically well-characterized bacteriumBacillus subtilis. Molecular aspects of spore structure, assembly, and function are well defined. However, certain bacteria produce spores with an outer spore layer, the exosporium, which is not present onB. subtilisspores. Our understanding of the composition and biological functions of the exosporium layer is much more limited than that of other aspects of the spore. Because the bacterial spore surface is important for the spore's interactions with the environment, as well as being the site of interaction of the spore with the host's innate immune system in the case of spore-forming bacterial pathogens, the exosporium is worthy of continued investigation. Recent exosporium studies have focused largely on members of theBacillus cereusfamily, principallyBacillus anthracisandBacillus cereus. Our understanding of the composition of the exosporium, the pathway of its assembly, and its role in spore biology is now coming into sharper focus. This review expands on a 2007 review of spore surface layers which provided an excellent conceptual framework of exosporium structure and function (A. O. Henriques and C. P. Moran, Jr., Annu Rev Microbiol61:555–588, 2007,http://dx.doi.org/10.1146/annurev.micro.61.080706.093224). That review began a process of considering outer spore layers as an integrated, multilayered structure rather than simply regarding the outer spore components as independent parts.

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Section: Discussionmentioning

confidence: 99%

The Exosporium Layer of Bacterial Spores: a Connection to the Environment and the Infected Host

Stewart

2015

Microbiol Mol Biol Rev

138

155

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“…In contrast, increased resistance to wet heat correlated with higher sporulation temperatures for B. subtilis spores (3). However, some environmental conditions such as anaerobiosis are known to lead to increased heat resistance of B. cereus spores (71). Heat resistance is multifactorial, and a number of factors, such as a higher quantity of DPA, lower spore water content, or the structure of the cortex, could explain the higher heat resistance of ⌬cotE than WT spores (3,4).…”

Section: Discussionmentioning

confidence: 99%

Sporulation Temperature Reveals a Requirement for CotE in the Assembly of both the Coat and Exosporium Layers of Bacillus cereus Spores

Bressuire-Isoard

Bornard²,

Henriques

et al. 2016

Appl Environ Microbiol

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The Bacillus cereus spore surface layers consist of a coat surrounded by an exosporium. We investigated the interplay between the sporulation temperature and the CotE morphogenetic protein in the assembly of the surface layers of B. cereus ATCC 14579 spores and on the resulting spore properties. The cotE deletion affects the coat and exosporium composition of the spores formed both at the suboptimal temperature of 20°C and at the optimal growth temperature of 37°C. Transmission electron microscopy revealed that ⌬cotE spores had a fragmented and detached exosporium when formed at 37°C. However, when produced at 20°C, ⌬cotE spores showed defects in both coat and exosporium attachment and were susceptible to lysozyme and mutanolysin. Thus, CotE has a role in the assembly of both the coat and exosporium, which is more important during sporulation at 20°C. CotE was more represented in extracts from spores formed at 20°C than at 37°C, suggesting that increased synthesis of the protein is required to maintain proper assembly of spore surface layers at the former temperature. ⌬cotE spores formed at either sporulation temperature were impaired in inosine-triggered germination and resistance to UV-C and H 2 O 2 and were less hydrophobic than wild-type (WT) spores but had a higher resistance to wet heat. While underscoring the role of CotE in the assembly of B. cereus spore surface layers, our study also suggests a contribution of the protein to functional properties of additional spore structures. Moreover, it also suggests a complex relationship between the function of a spore morphogenetic protein and environmental factors such as the temperature during spore formation. Bacterial endospores are formed in a wide range of ecological niches in soil, as well as in the gastrointestinal tract of invertebrate and vertebrate animals, and in both natural and anthropized environments (1). Physical and chemical conditions prevailing in such niches play a major role in triggering sporulation and in determining the final properties of the resulting spores (2). Laboratory experiments demonstrate the major influence of environment, in particular of temperature, on the efficiency and yield of sporulation, and in spore resistance to wet heat, UV, high hydrostatic pressure, and preservatives or spore response to germinants (3; reviewed in references 1 and 4). Spore resistance and functional properties result from the assembly of several protective structures: cortex, coat, and exosporium. The spore peptidoglycan cortex, a structure common to all endospores, is a major factor in the resistance of spores to heat (1, 4). The cortex is surrounded by a proteinaceous coat, and in organisms such as Bacillus anthracis or Bacillus cereus the coat is further enveloped by an exosporium, a "balloon-like" structure consisting of a paracrystalline basal layer and an external hair-like nap formed mainly by the collagen-like glycoprotein BclA (5-11). While the coat contributes to protection against peptidoglycan-breaking enzymes, UV light, and oxidative...

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“…The growth and sporulation model (equations 1, 2, and 5) was used to fit the kinetics of B. subtilis BSB1 cultivated in whey and of Bacillus licheniformis Ad978 cultivated in batch in Hageman medium supplemented with 1% brain heart infusion (BHI) at two temperatures. Kinetics from the literature (24) were used also to fit the model, like the kinetics obtained with Bacillus cereus AH187 cultivated in the chemically defined MODS medium (50) in aerobiosis at 37°C (Fig. 2).…”

Section: Importancementioning

confidence: 99%

Differentiation of Vegetative Cells into Spores: a Kinetic Model Applied to Bacillus subtilis

Gauvry

Mathot

Couvert

et al. 2019

Appl Environ Microbiol

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Spore-forming bacteria are natural contaminants of food raw materials, and sporulation can occur in many environments from farm to fork. In order to characterize and to predict spore formation over time, we developed a model that describes both the kinetics of growth and the differentiation of vegetative cells into spores. The model is based on a classical growth model and enables description of the kinetics of sporulation with the addition of three parameters specific to sporulation. Two parameters are related to the probability of each vegetative cell to commit to sporulation and to form a spore, and the last one is related to the time needed to form a spore once the cell is committed to sporulation. The goodness of fit of this growth-sporulation model was assessed using growth-sporulation kinetics at various temperatures in laboratory medium or in whey for Bacillus subtilis, Bacillus cereus, and Bacillus licheniformis. The model accurately describes the kinetics in these different conditions, with a mean error lower than 0.78 log 10 CFU/ml for the growth and 1.08 log 10 CFU/ml for the sporulation. The biological meaning of the parameters was validated with a derivative strain of Bacillus subtilis 168 which produces green fluorescent protein at the initiation of sporulation. This model provides physiological information on the spore formation and on the temporal abilities of vegetative cells to differentiate into spores and reveals the heterogeneity of spore formation during and after growth. Citation Gauvry E, Mathot A-G, Couvert O, Leguérinel I, Jules M, Coroller L. 2019. Differentiation of vegetative cells into spores: a kinetic model applied to Bacillus subtilis. Appl Environ Microbiol 85:e00322-19. https://doi .on July 10, 2020 by guest http://aem.asm.org/ Downloaded from RESULTSModel development and experimental strategy. The growth of vegetative cells was described by a modified logistic model (equation 1) and their differentiation into spores over time with specific sporulation parameters: the probability (t max , , and P max ; see below) of vegetative cells to give a mature spore (heat resistant) during the incubation and the time needed for the spore formation (t f

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Absence of oxygen affects the capacity to sporulate and the spore properties of Bacillus cereus

Cited by 31 publications

References 64 publications

The Exosporium Layer of Bacterial Spores: a Connection to the Environment and the Infected Host

The Exosporium Layer of Bacterial Spores: a Connection to the Environment and the Infected Host

Sporulation Temperature Reveals a Requirement for CotE in the Assembly of both the Coat and Exosporium Layers of Bacillus cereus Spores

Differentiation of Vegetative Cells into Spores: a Kinetic Model Applied to Bacillus subtilis

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