Identification and characterization of a germination operon on the virulence plasmid pXOl of <i>Bacillus anthracis</i>

Guidi‐Rontani, Chantal; Pereira, Yannick; Ruffie, Stéphanie; Sirard, Jean‐Claude; Weber-Levy, Martine; Mock, Michèle

doi:10.1046/j.1365-2958.1999.01485.x

Cited by 119 publications

(99 citation statements)

References 40 publications

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“…Recent sequencing and genetic studies have identified members of the gerA family of operons in other endospore-forming bacteria including Bacillus cereus (3), Bacillus anthracis (9), Bacillus halodurans (23), Clostridium acetobutylicum (Genome Therapeutics Corporation), Clostridium difficile (Sanger Centre), and Clostridium pasteurianum (GenBank). However, thus far no gerA homologs have been identified in other bacterial groups.…”

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Role of Ger Proteins in Nutrient and Nonnutrient Triggering of Spore Germination in Bacillus subtilis

2000

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DormantBacillus subtilis spores germinate in the presence of particular nutrients called germinants. The spores are thought to recognize germinants through receptor proteins encoded by the gerA family of operons, which includes gerA, gerB, and gerK. We sought to substantiate this putative function of the GerA family proteins by characterizing spore germination in a mutant strain that contained deletions at all known gerA-like loci. As expected, the mutant spores germinated very poorly in a variety of rich media. In contrast, they germinated like wild-type spores in a chemical germinant, a 1-1 chelate of Ca 2؉ and dipicolinic acid (DPA). These observations showed that proteins encoded by gerA family members are required for nutrient-induced germination but not for chemical-triggered germination, supporting the hypothesis that the GerA family encodes receptors for nutrient germinants. Further characterization of Ca 2؉ -DPA-induced germination showed that the effect of Ca 2؉ -DPA on spore germination was saturated at 60 mM and had a K m of 30 mM. We also found that decoating spores abolished their ability to germinate in Ca 2؉ -DPA but not in nutrient germinants, indicating that Ca 2؉ -DPA and nutrient germinants probably act through parallel arms of the germination pathway.Bacillus subtilis cells form metabolically dormant spores when starved for one or more nutrients (7). In the presence of particular nutrients, called germinants, the spores break dormancy through the process of germination and, after going through outgrowth, eventually resume vegetative growth (15). It is currently believed that spores recognize nutrient germinants through receptor proteins encoded by three loci (gerA, gerB, and gerK). This hypothesis is based on genetic studies which showed that spores containing mutations at any one of these loci fail to germinate in response to specific germinants (14,15,19). Further support for the receptor hypothesis came from the finding that dominant mutations in gerB allow spores to germinate in novel germinants (17). The gerA, gerB, and gerK loci are each tricistronic operons encoding proteins which share significant homology across the three operons (4,12,25). Two of the three proteins encoded by each operon are predicted to be membrane proteins, which is again consistent with the idea that they encode germinant receptors (4, 25). The proteins, however, have been refractory to in vitro biochemical manipulation, and thus the receptor hypothesis remains untested.Recent sequencing and genetic studies have identified members of the gerA family of operons in other endospore-forming bacteria including Bacillus cereus (3), Bacillus anthracis (9), Bacillus halodurans (23), Clostridium acetobutylicum (Genome Therapeutics Corporation), Clostridium difficile (Sanger Centre), and Clostridium pasteurianum (GenBank). However, thus far no gerA homologs have been identified in other bacterial groups. Furthermore, the B. cereus gerA operon homolog, gerI, has been implicated in inosine-induced spore germination in that ...

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Role of Ger Proteins in Nutrient and Nonnutrient Triggering of Spore Germination in Bacillus subtilis

2000

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“…These sensors belong to the GerA family of germinant receptors, which are best characterized in Bacillus subtilis but which have also been studied in other Bacillus spp. (2,5,15,16,18,19,29,30).Six tricistronic gerA-like chromosomal loci (gerAA, gerAB, gerAC) plus the gerX locus carried on pXO1 exist in B. anthracis; these loci encode germinant recognition proteins (6,10,11,25). The gerS operon in B. anthracis mediates germination in response to aromatic ring structures and is required for germination in the presence of cultured M (11, 12).…”

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“…Six tricistronic gerA-like chromosomal loci (gerAA, gerAB, gerAC) plus the gerX locus carried on pXO1 exist in B. anthracis; these loci encode germinant recognition proteins (6,10,11,25). The gerS operon in B. anthracis mediates germination in response to aromatic ring structures and is required for germination in the presence of cultured M (11, 12).…”

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Macrophage-Mediated Germination of Bacillus anthracis Endospores Requires the gerH Operon

Weiner

Hanna

2003

Infect Immun

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The gerHABC operon of Bacillus anthracis, encoding a gerA-like family member of germinant sensors, was shown to be required for endospore germination in the presence of macrophages and in macrophage-conditioned media. The loss of the germination phenotype in macrophage cultures of B. anthracis gerH-null endospores was restored by complementation in trans with a wild-type copy of gerH expressed under the control of its own promoter. Using endospores from both the parental strain B. anthracis Sterne and an isogenic gerH-null strain, we partially characterized germinants secreted by macrophages into the extracellular medium.Bacillus anthracis endospores can persist for long periods in soil but, upon entering a host, germinate quickly into vegetative bacilli that grow and cause disease (4). Endospores germinate inside of or proximal to phagocytes. These cells are believed to be de facto sites of germination and contribute to the establishment of B. anthracis infection, as phagocytes are the primary means of bacterial access to the body in cases of inhalation anthrax (6,8,10,20). Several recent studies examined the fate of B. anthracis endospores in macrophages (M). Guidi-Rontani et al. showed that murine alveolar phagocytes ingest endospores that then germinate and grow into vegetative bacilli but do not replicate (6). Welkos et al. observed intact endospores and recently germinated nascent bacilli within phagosomes in M that are subsequently destroyed by these immune cells (26,27,28). Work by Dixon et al. indicated that newly vegetative bacilli escape from the phagocytic vesicles of the M where they can replicate freely in the host cell cytoplasm and release themselves from the M (3). Though there are important differences among these researchers' observations of the ultimate fates of phagocytosed endospores, it is generally agreed that germinant sensors recognize and bind small-molecule germinants and initiate the germination cascade (17). These sensors belong to the GerA family of germinant receptors, which are best characterized in Bacillus subtilis but which have also been studied in other Bacillus spp. (2,5,15,16,18,19,29,30).Six tricistronic gerA-like chromosomal loci (gerAA, gerAB, gerAC) plus the gerX locus carried on pXO1 exist in B. anthracis; these loci encode germinant recognition proteins (6,10,11,25). The gerS operon in B. anthracis mediates germination in response to aromatic ring structures and is required for germination in the presence of cultured M (11, 12). The gerH operon also mediates germination in response to aromatic ring structures and germination triggered by inosine (Ino) in combination with amino acids (25). The germinants recognized by the gerX operon on pXO1 have not yet been identified, although ⌬Sterne strains lacking pXO1 do not exhibit any gross germination defects in vitro (11,12). Endospores from a gerXnull strain, identified by Guidi-Rontani et al., germinates slightly less well than do Sterne endospores in the presence of M (6, 12). One ger locus has homology to the gerL locus...

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“…Previous reports had suggested that the GerX, GerH, and to a lesser extent the GerS receptors, are important for the establishment of anthrax infection and disease progression (Guidi-Rontani et al, 1999;Ireland and Hanna, 2002b;Kang et al, 2005;. However, recent data shows that as long as one of the genomically encoded receptors (GerH, GerK, GerL, or GerS) is present, B. anthracis spores remain fully virulent in an inhalational anthrax murine model (Carr et al, 2010).…”

Section: Bacillus Anthracis Ger Receptorsmentioning

confidence: 99%

The Ger Receptor Family from Sporulating Bacteria

Roß

Abel-Santos

2010

Current Issues in Molecular Biology

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Bacterial spores are specialized cells that are exceptionally resistant to environmental stress. Spores convert back to actively growing cells, a process called germination, upon nutrient detection. The most common, initial step in the germination process is the recognition of small molecule germinants by germination (Ger) receptors. Ger receptors are inner-membrane heterocomplexes formed by three distinct protein products, the A-, B-, and C-subunits. In this review, we discuss and contrast published reports on representative Ger receptors from different Bacilli and Clostridia. We also present evidence for unrecognized germination pathways independent of Ger receptors. We further emphasize the function of L-alanine as a universal germinant. We also comment on biochemical aspects of germinant recognition and interaction between Ger receptor proteins. We propose that there are six general strategies used by Bacilli and Clostridia to integrate multiple germination signals. The use of different germinant recognition strategies results in germination response flexibility. Consequently, sporulating bacterial species that use the same biomolecules as germination signals can have different germination profiles. Finally, we discuss future directions for understanding the function of Ger receptors.

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Identification and characterization of a germination operon on the virulence plasmid pXOl of Bacillus anthracis

Cited by 119 publications

References 40 publications

Role of Ger Proteins in Nutrient and Nonnutrient Triggering of Spore Germination in Bacillus subtilis

Role of Ger Proteins in Nutrient and Nonnutrient Triggering of Spore Germination in Bacillus subtilis

Macrophage-Mediated Germination of Bacillus anthracis Endospores Requires the gerH Operon

The Ger Receptor Family from Sporulating Bacteria

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