Timing of Protein Synthesis during Germination and Outgrowth of Spores of Bacillus cereus Strain T

Steinberg, William M.; Halvorson, Harlyn O.; Keynan, A.; Weinberg, Eric S.

doi:10.1038/208710a0

Cited by 40 publications

(35 citation statements)

References 9 publications

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“…Since vegetative cells of the Sterne strain are rapidly inactivated in macrophages (Kang et al, 2005;Hu et al, 2006), their small number could be due to either the immediate inactivation of spores once they had germinated and grown out or germinated spores per se could be killed. Chloramphenicol is known to block outgrowth but not germination (Steinberg et al, 1965) and this has been confirmed using 50 mg mL À1 for Sterne spores in a nutrient medium (data not shown). Chloramphenicol is known to block outgrowth but not germination (Steinberg et al, 1965) and this has been confirmed using 50 mg mL À1 for Sterne spores in a nutrient medium (data not shown).…”

Section: Germinated Spores Are Inactivated In Macrophages Before Outgmentioning

confidence: 62%

Factors involved in the germination and inactivation ofBacillus anthracisspores in murine primary macrophages

Emerson

Aronson

2007

FEMS Microbiology Letters

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Since macrophages have been implicated in inhalation anthrax either for defense and/or as enablers for spore trafficking, their function has been further defined. Spores were efficiently taken up by primary mouse bone marrow-derived macrophages even in the absence of serum but a minimal amount was required for spore germination and subsequent inactivation. With 10% fetal bovine serum (FBS) virtually all of the spores germinated but when the concentration of FBS was lowered to 1.0% or less, or when 10% horse serum replaced FBS, only 50% of the spores were inactivated within 1 h with no subsequent loss. Chloramphenicol, which blocks spore outgrowth but not germination, did not inhibit spore killing in macrophages. Based on complete inhibition of germination by d-alanine plus d-histidine, it is likely that only two of the several Bacillus anthracis germination systems are involved within macrophages. d-Histidine inhibits the gerH system previously implicated in germination within macrophages. d-Alanine is likely to block the gerX system since disruption of the gerXA gene resulted in little germination within 4 h in macrophages. Macrophages provide a major line of defense against infection by efficiently sequestering spores and in the presence of minimal nutrients effectively killing those that germinate before outgrowth.

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Section: Germinated Spores Are Inactivated In Macrophages Before Outgmentioning

confidence: 62%

Factors involved in the germination and inactivation ofBacillus anthracisspores in murine primary macrophages

Emerson

Aronson

2007

FEMS Microbiology Letters

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“…In Bacillus anthracis some of these proteins are expressed specifically late during sporulation, suggesting a loading mechanism that equips the spore with enzymes that may be essential in the early events during germination and outgrowth (32). Nevertheless, active, transcription-dependent protein synthesis is an absolute requirement for the outgrowth of B. subtilis spores, as has been demonstrated by the effects of transcription-and translationinhibiting antibiotics on germination and outgrowth (44,62).…”

Section: Transcriptional Processes During Early Stages Of Outgrowth (mentioning

confidence: 99%

Analysis of Temporal Gene Expression duringBacillus subtilisSpore Germination and Outgrowth

et al. 2007

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Bacillus subtilis forms dormant spores upon nutrient depletion. Under favorable environmental conditions, the spore breaks its dormancy and resumes growth in a process called spore germination and outgrowth. To elucidate the physiological processes that occur during the transition of the dormant spore to an actively growing vegetative cell, we studied this process in a time-dependent manner by a combination of microscopy, analysis of extracellular metabolites, and a genome-wide analysis of transcription. The results indicate the presence of abundant levels of late sporulation transcripts in dormant spores. In addition, the results suggest the existence of a complex and well-regulated spore outgrowth program, involving the temporal expression of at least 30% of the B. subtilis genome.A number of bacterial species such as bacilli and clostridia have the ability to form dormant spores. The spore has a specialized and complex structure, enabling the organism to survive for a long time under harsh environmental conditions and in the absence of nutrients. When triggered by specific nutrients, the spore is capable of breaking dormancy (germination) and initiating vegetative growth (34, 52). The Bacillus subtilis spore is composed of a dehydrated central compartment (the spore core) engulfed by two protective outer layers: a thick spore-specific peptidoglycan layer known as the spore cortex and a multilayered protein structure known as the coat (12).The process of endospore formation in Bacillus subtilis has been studied in great detail. Studies have revealed a highly ordered and strictly regulated program ensuring the correct coordination of various aspects of the sporulation process, such as asymmetric cell division, prespore engulfment, spore maturation, and mother cell lysis (22). The sporulation program involves the timed activation of several mother cell and forespore compartment-and sporulation stage-dependent RNA polymerase sigma factors that transcribe specific sets of sporulation genes. Eventually, the sporulation program results in the lysis of the mother cell and the release of a dormant spore (22).The process of spore germination and outgrowth has been studies in less detail. Spore germination is initiated when the spore senses the appropriate trigger molecules, often simple sugars and/or amino acids. The germinant molecules are sensed by germination receptors. This, by an unknown mechanism, leads to an irreversible commitment of a spore to germination. The germinating spore initially releases Zn 2ϩ and H ϩ (65). Simultaneously (and probably as a consequence), the pH of the spore core rises from 6.5 to 7.7. In a second stage, the germinating spore releases the spore core's large supply of dipicolinic acid (pyridine-2,6-dicarboxylic acid), and the spore core is rehydrated. Subsequently, cortex lytic enzymes are activated and the protective spore peptidoglycan cortex is degraded. This enables the germinating spore to hydrate the spore core further and to swell. These germination events coincide with a loss of...

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“…Further investigations on Bacillus megaterium revealed quantitative differences in the assortment of cytochromes and in the levels of the respiratory activities of mother cell and forespore (10). In contrast to the developing forespore, the dormant spore is devoid of significant endogenous respiration (13,21); apparently this is not merely due to the depletion of endogenous substrates, since the membrane particles of dormant spores are poorly active in the oxidation of NADH (25). These data suggest that the forespore respiratory system is inactivated during the finals steps of morphogenesis.…”

mentioning

confidence: 99%

Respiratory systems of the Bacillus cereus mother cell and forespore

Escamilla¹,

Ramı́rez²,

Del-Arenal³

et al. 1986

J Bacteriol

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The respiratory systems of the mother cells and forespores of Bacilus cereus were compared throughout the maturation stages (E to VI) of sporulation. The results indicated that both cell compartments contain the same assortment of oxidoreductases and cytochromes. However membrane fractions from young forespores were clearly distinct from those of the mother cell, i.e., lower content of cytochrome aa3, lower cytochrome c oxidase activity, higher concentration of cytochrome o, and a lower sensitivity of the respiration to the inhibiting effect of cyanide. This suggests that the cyanide-resistant pathway contributes more importantly to forespore respiratory activity than to activity in the mother cell compartment. During the maturation stages, the forespore NADH oxidase activity declined faster than in the mother cells. Other activities studied decreased steadily in both cell compartments. These findings together with the analysis of the kinetics of NADHdependent reduction of cytochromes in the mature spore membranes indicated an impairment of electron flow between NADH dehydrogenase and cytochrome b. This impairment could be overcome by the addition of menadione.The sporulating cell of Bacillus species contains two distinct compartments: mother cell and forespore. The biochemical analysis of the separate entities has been made possible by the development of adequate forespore release techniques (1, 6). The evidence accumulated indicated that even very early in its development some of the biochemical properties of the forespore differ distinctly from those of mother cell (for a review, see reference 17). Early work on isolated young forespores suggested the presence of a membrane-bound respiratory system with a capacity to oxidize endogenous substrates and added NADH (2,5,8,24). Further investigations on Bacillus megaterium revealed quantitative differences in the assortment of cytochromes and in the levels of the respiratory activities of mother cell and forespore (10). In contrast to the developing forespore, the dormant spore is devoid of significant endogenous respiration (13, 21); apparently this is not merely due to the depletion of endogenous substrates, since the membrane particles of dormant spores are poorly active in the oxidation of NADH (25). These data suggest that the forespore respiratory system is inactivated during the finals steps of morphogenesis.The present work deals with the characterization of the respiratory systems of mother cells and forespores of Bacillus cereus and their regulation during maturation stages. In addition the composition and activity of the electron transport system of young forespores and dormant spores were compared. The results indicate that the respiratory system of the forespore differs from that of the mother cell in several respects. Furthermore the inactivation observed in the forespore respiratory system does not occur in the mother cell compartment, and the electron flow in the mature spore is impaired between NADH dehydrogenase and cytochrome b (cyt b). The impa...

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Timing of Protein Synthesis during Germination and Outgrowth of Spores of Bacillus cereus Strain T

Cited by 40 publications

References 9 publications

Factors involved in the germination and inactivation ofBacillus anthracisspores in murine primary macrophages

Factors involved in the germination and inactivation ofBacillus anthracisspores in murine primary macrophages

Analysis of Temporal Gene Expression duringBacillus subtilisSpore Germination and Outgrowth

Respiratory systems of the Bacillus cereus mother cell and forespore

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