The first step in both events is the localization of proteins to a site of membrane curvature , Second, a scaffold of coat material is assembled at the initial site of localization, and protein polymerization proceeds around the circumference of the developing vesicle. Ultimately, the process terminates with membrane fission at the opposite pole of the vesicle.
Brun, Y. Google Scholar. Cohn, F. Pflanzen 7 , — Along with Koch below , this paper contains the first and highly prescient description of sporulation. Koch, R. Nicholson, W. Resistance of Bacillus endospores to extreme terrestrial and extraterrestrial environments. Kennedy, M. Preservation records of micro-organisms: evidence of the tenacity of life. Microbiology , — PubMed Google Scholar.
Sneath, P. Longevity of micro-organisms. Nature , — Jacotot, H. Pasteur 87 , — CAS Google Scholar. Hierarchical evolution of the bacterial sporulation network. Galperin, M. Genomic determinants of sporulation in Bacilli and Clostridia: towards the minimal set of sporulation-specific genes. A comprehensive study of sporulation gene conservation among endospore formers. Earl, A. Ecology and genomics of Bacillus subtilis. Trends Microbiol. Wu, M. Life in hot carbon monoxide: the complete genome sequence of Carboxydothermus hydrogenoformans Z PLoS Genet.
Hubert, C. A constant flux of diverse thermophilic bacteria into the cold Arctic seabed. Science , — Eckburg, P. Diversity of the human intestinal microbial flora. Fujita, M. Evidence that entry into sporulation in Bacillus subtilis is governed by a gradual increase in the level and activity of the master regulator Spo0A.
Genes Dev. Molle, V. The Spo0A regulon of Bacillus subtilis. Popham, D. Specialized peptidoglycan of the bacterial endospore: the inner wall of the lockbox. Life Sci. Henriques, A. Structure, assembly, and function of the spore surface layers.
A thorough review that includes a comprehensive list of coat proteins in B. Driks, A. The Bacillus anthracis spore. Aspects Med. Vasudevan, P. Spore cortex formation in Bacillus subtilis is regulated by accumulation of peptidoglycan precursors under the control of sigma K. Fay, A. McKenney, P. Dynamics of spore coat morphogenesis in Bacillus subtilis. This study ties the phenomenon of spore encasement to the regulation of expression of individual spore coat genes.
Aronson, A. Structure and morphogenesis of the bacterial spore coat. Warth, A. The composition and structure of bacterial spores. Cell Biol. Tocheva, E. Peptidoglycan remodeling and conversion of an inner membrane into an outer membrane during sporulation.
Cell , — A distance-weighted interaction map reveals a previously uncharacterized layer of the Bacillus subtilis spore coat. Boydston, J. The ExsY protein is required for complete formation of the exosporium of Bacillus anthracis. Giorno, R. Morphogenesis of the Bacillus anthracis spore. Bozue, J. Bacillus anthracis spores of the bclA mutant exhibit increased adherence to epithelial cells, fibroblasts, and endothelial cells but not to macrophages.
Chen, G. Bacillus anthracis and Bacillus subtilis spore surface properties and transport. Colloids Surf. B Biointerfaces 76 , — Kailas, L. Natl Acad. USA , — This study provides a high-resolution characterization of the exosporium structure, revealing a crystalline layer made of a honeycomb-like array of cups.
Permpoonpattana, P. Surface layers of Clostridium difficile endospores. Setlow, P. I will survive: DNA protection in bacterial spores. Hullo, M. CotA of Bacillus subtilis is a copper-dependent laccase. Liu, G. Color me bad: microbial pigments as virulence factors. Eisenman, H. Synthesis and assembly of fungal melanin. Klobutcher, L. Laaberki, M. Role of spore coat proteins in the resistance of Bacillus subtilis spores to Caenorhabditis elegans predation.
Carroll, A. Paredes-Sabja, D. Germination of spores of Bacillales and Clostridiales species: mechanisms and proteins involved. Shah, I. Bacillus subtilis spore coat. Stewart, B. Studies on the spores of aerobic bacteria. The occurrence of alanine racemase. Steichen, C. Identification of the immunodominant protein and other proteins of the Bacillus anthracis exosporium.
Todd, S. Genes of Bacillus cereus and Bacillus anthracis encoding proteins of the exosporium. Chesnokova, O. The spore-specific alanine racemase of Bacillus anthracis and its role in suppressing germination during spore development.
Pierce, K. Gene cloning and characterization of a second alanine racemase from Bacillus subtilis encoded by yncD. FEMS Microbiol. Butzin, X. Analysis of the effects of a gerP mutation on the germination of spores of Bacillus subtilis.
Chirakkal, H. Analysis of spore cortex lytic enzymes and related proteins in Bacillus subtilis endospore germination. Bagyan, I. Localization of the cortex lytic enzyme CwlJ in spores of Bacillus subtilis.
Lambert, E. Imamura, D. Localization of proteins to different layers and regions of Bacillus subtilis spore coats. Buist, G. LysM, a widely distributed protein motif for binding to peptido glycans. Ebmeier, S. Small proteins link coat and cortex assembly during sporulation in Bacillus subtilis. Santo, L. Ultrastructural analysis during germination and outgrowth of Bacillus subtilis spores. Non-uniform assembly of the Bacillus anthracis exosporium and a bottle cap model for spore germination and outgrowth.
A description of the polarity of the spore envelope and a model for spore germination and outgrowth. Holt, S. Comparative ultrastructure of selected aerobic spore-forming bacteria: a freeze-etching study. Traag, B. Do mycobacteria produce endospores? Walker, J. Clostridium taeniosporum spore ribbon-like appendage structure, composition and genes. Lequette, Y. Role played by exosporium glycoproteins in the surface properties of Bacillus cereus spores and in their adhesion to stainless steel.
Buhr, T. Siala, A. Populations of spore-forming bacteria in an acid forest soil, with special reference to Bacillus subtilis. Roles of Bacillus endospores in the environment. Donovan, W. Genes encoding spore coat polypeptides from Bacillus subtilis. Beall, B. Cloning and characterization of a gene required for assembly of the Bacillus subtilis spore coat.
Zheng, L. Gene encoding a morphogenic protein required in the assembly of the outer coat of the Bacillus subtilis endospore. Lai, E. Proteomic analysis of the spore coats of Bacillus subtilis and Bacillus anthracis. Kuwana, R. Proteomics characterization of novel spore proteins of Bacillus subtilis. As a cell begins the process of forming an endospore, it divides asymmetrically Stage II. This results in the creation of two compartments, the larger mother cell and the smaller forespore.
These two cells have different developmental fates. Intercellular communication systems coordinate cell-specific gene expression through the sequential activation of specialized sigma factors in each of the cells.
Next Stage III , the peptidoglycan in the septum is degraded and the forespore is engulfed by the mother cell, forming a cell within a cell. Finally, the mother cell is destroyed in a programmed cell death, and the endospore is released into the environment.
The endospore will remain dormant until it senses the return of more favorable conditions. Some Epulopiscium -like surgeonfish symbionts form mature endospores at night.
These spores possess all of the characteristic protective layers seen in B. These are the largest endospores described thus far, with the largest being over times larger than a Bacillus subtilis endospore. The formation of endospores may help maintain the symbiotic association between these Epulopiscium -like symbionts and their surgeonfish hosts.
Germination involves the dormant endospore starting metabolic activity and thus breaking hibernation. It is commonly characterised by rupture or absorption of the spore coat, swelling of the endospore, an increase in metabolic activity, and loss of resistance to environmental stress.
As a simplified model for cellular differentiation, the molecular details of endospore formation have been extensively studied, specifically in the model organism Bacillus subtilis. These studies have contributed much to our understanding of the regulation of gene expression, transcription factors, and the sigma factor subunits of RNA polymerase.
Endospores of the bacterium Bacillus anthracis were used in the anthrax attacks. The powder found in contaminated postal letters was composed of extracellular anthrax endospores. Inhalation, ingestion or skin contamination of these endospores led to a number of deaths.
Geobacillus stearothermophilus endospores are used as biological indicators when an autoclave is used in sterilization procedures. Bacillus subtilis spores are useful for the expression of recombinant proteins and in particular for the surface display of peptides and proteins as a tool for fundamental and applied research in the fields of microbiology, biotechnology and vaccination. Learning Objectives Describe the function and advantage of endospore formation, as well as the methods for viewing it.
Key Points Examples of bacteria that can form endospores include Bacillus and Clostridium. Key Terms endospore : A dormant, tough, and non-reproductive structure produced by certain bacteria from the Firmicute phylum. Three important food sectors are discussed in this paper. In the fruit juice industry, Alicyclobacillus acidoterrestris , present on raw fruits, has become a major quality-target organism. In the ready-to-eat food sector, B. There is a clear association between soil-borne endospore forming bacteria and food contamination.
Several reasons can be proposed to explain this phenomenon, and most are related to some general characteristics of the spores, which are formed at the end of the growth phase within the vegetative mother cell acting as sporangium hence, endospores and released in the environment as survival structures Figure 1.
These are 1 their ubiquitous presence in soil, 2 their resistance to heat in common industrial processes such as pasteurization, 3 the adhesive characters of particular spores that facilitate their attachment to processing equipment, and 4 their ability to germinate and grow in favorable conditions [ 1 ]. Several spore formers either need or tolerate specific conditions for germination and growth, which all can occur in food even in combination, such as low or high temperatures and anaerobic or acidophilic conditions.
The concerted characteristics of spores and vegetative cells of particular soil-borne species make them potential sole surviving and growing contaminants in specific industrially processed foods.
Some of them seem even to be of more recent concern, which might be the result of increasing tolerance, adaptation, or resistance of spores or vegetative cells of particular spore-forming species to conditions or treatments that were previously presumed either to stop growth low temperatures and low pH or to inactivate all living material ultrahigh heat treatment UHT and commercial sterilization.
The food industry seems to be increasingly confronted with tolerant or resistant spore formers that might be side effects of the use of new ingredients, the application of new processing and packaging technologies, and the highly increased production and marketing of convenience foods. In the last two decades, there has been a significant increase in the production and sale of ready-to-eat or ready-to-cook foods stored under refrigerated conditions [ 2 ].
Spore formers cause two kinds of problems in the food industry. In the first place, there are some food-borne pathogens such as Bacillus cereus and Clostridium botulinum. Secondly, there is the reduction of shelf life and food spoilage. Microbial spoilage of food is usually indicated by changes in texture or the development of off-flavours. In this paper, recent data revealing the role of soil as primary contamination source for spore formers in food B.
Soil is heavily contaminated with B. It has long been believed that this organism has a saprophytic life cycle in soil with the presence of spores that only germinate and grow upon contact with soil-associated organic matter i. However, in laboratory experiments with liquid soil extract and artificial soil microcosms, it was observed that B. In addition to a full life cycle in soil, B.
Bacillus thuringiensis, being an insect pathogen of the B. Presumably, B. Less is known on the ecology of the other members of the B. It has been speculated that climate change may modify the spreading of B.
Alternatively, B. This adaptation might contribute at the end of the chain to a progressive change in prevalence or concentration in foods. Soil, together with air, is probably the primary source of food contamination. Being a soil resident, B. At harvest, this plant raw material can be used for direct human consumption as fresh produce, as ingredients for food or feed production, or directly as animal feed.
Dairy cows consuming such feed will excrete B. On the other hand, as B. Nevertheless, recent investigations in Denmark have shown that B. Since these strains harboured genes encoding enterotoxins, increased concern regarding the residual amount of B. Despite these observations, problems of B. A combination of the specific attributes of the spores and of the resulting vegetative cells give B. Firstly, like all bacterial spores, B. As a result, a final product may be contaminated with spores that face little or no competition from vegetative species that would otherwise outgrow B.
A second aspect is that B. According to Wijman et al. Spores embedded in biofilms are protected against disinfectants [ 24 ]. A third aspect is the use of extended refrigeration in food production and distribution, as well as in the kitchen, to increase the shelf life of processed foods.
An important feature of B. Moreover, it is important to note that the majority of B. Due to its ubiquitous presence in soil and on plant material which is used for a variety of purposes and in food processing environments, as well as its special characteristics described above, the presence of B. The level of B. However, upon storage of processed foods or the use of contaminated ingredients in complex foods, conditions may allow germination and outgrowth of spores to levels that present hazards for consumers.
Outbreaks of B. Dierick, pers. In the last decades, the importance of the psychrotolerant aerobic endospore formers for the keeping quality of milk has increased significantly, owing to extended refrigerated storage of raw milk before processing on the farm, higher pasteurization temperatures, reduction of postpasteurization contamination, and prolonged shelf-life requirements of the consumer product.
It should be remembered that pasteurization activates spore germination and thus enhances vegetative cell growth. Growth of B. Too high levels of B. This may be due to the fact that in the cold dairy chain, selection occurs for psychrotolerant members of the B. It has been shown that these strains are less toxigenic than mesophilic B. Emetic food poisoning related to the consumption of dairy products has been reported see references in [ 28 ].
If contaminated milk is used for milk powder, a risk to the consumer exists if this milk powder is used in baby food or as raw ingredient in foodstuffs, where proliferation of B.
From the above, it is not surprising that B. In the Netherlands, a maximum B. During recent decades, several possible contamination routes for B. As for the raw milk route of contamination, only in recent years evidence has been obtained using sensitive detection methods, as B. Raw milk in the farm tank is contaminated with B. Contamination of the exterior of the teats occurs when they are contaminated with dirt; during the grazing season of the cows, this dirt is mainly soil, while during the housing season the attached dirt is mainly faeces and bedding material.
During milking, this dirt is rinsed off and spores present in the dirt can contaminate the raw milk. As a result, soil, feed through excretion of spores in faeces , and bedding material are the major sources of contamination of raw milk with B. Soil on farms is very frequently contaminated with B. Another important source of contamination of raw milk with B. Highly variable levels of B. It is assumed that Bacillus spp. Thus B. Using molecular typing, silage has been shown to be a significant source of contamination of raw milk with spores, including those of B.
The spores in silage principally arise from soil and farmyard manure. Nowadays, ensiled grass and maize form the major part of the feed ration of cattle in Europe and North America during the whole milking year.
It is important to prevent outgrowth of spores in silage by application of special cultures of lactic acid bacteria or chemical additives to improve aerobic stability of the silage [ 9 ]; however, these measures are not always used on the farm.
In the housing period of the cows, feed is the only source of spores, and teats become contaminated mainly through the bedding material that is contaminated with faeces Table 2. However, using a predictive modeling approach, it was found that soil was far more important than feed and hence bedding material as source of B.
According to the model, during the housing period, the concentration of spores of B.
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