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Comparative transcriptional profiling of Bacillus cereus sensu lato strains during growth in CO2-bicarbonate and aerobic atmospheres.

Passalacqua KD, Varadarajan A, Byrd B, Bergman NH - PLoS ONE (2009)

Bottom Line: Although much of this phenotypic range can be attributed to the presence or absence of a few key virulence factors, there are other virulence-associated loci that are conserved throughout the B. cereus group, and we hypothesized that these genes may be regulated differently in pathogenic and non-pathogenic strains.We have shown that homologous and even identical genes within the genomes of three closely related members of the B. cereus sensu lato group are in some instances regulated very differently, and that these differences can have important implications for virulence.This study provides insights into the evolution of the B. cereus group, and highlights the importance of looking beyond differences in gene content in comparative genomics studies.

View Article: PubMed Central - PubMed

Affiliation: School of Biology, Georgia Institute of Technology, Atlanta, Georgia, United States of America.

ABSTRACT

Background: Bacillus species are spore-forming bacteria that are ubiquitous in the environment and display a range of virulent and avirulent phenotypes. This range is particularly evident in the Bacillus cereus sensu lato group; where closely related strains cause anthrax, food-borne illnesses, and pneumonia, but can also be non-pathogenic. Although much of this phenotypic range can be attributed to the presence or absence of a few key virulence factors, there are other virulence-associated loci that are conserved throughout the B. cereus group, and we hypothesized that these genes may be regulated differently in pathogenic and non-pathogenic strains.

Methodology/principal findings: Here we report transcriptional profiles of three closely related but phenotypically unique members of the Bacillus cereus group--a pneumonia-causing B. cereus strain (G9241), an attenuated strain of B. anthracis (Sterne 34F(2)), and an avirulent B. cereus strain (10987)--during exponential growth in two distinct atmospheric environments: 14% CO(2)/bicarbonate and ambient air. We show that the disease-causing Bacillus strains undergo more distinctive transcriptional changes between the two environments, and that the expression of plasmid-encoded virulence genes was increased exclusively in the CO(2) environment. We observed a core of conserved metabolic genes that were differentially expressed in all three strains in both conditions. Additionally, the expression profiles of putative virulence genes in G9241 suggest that this strain, unlike Bacillus anthracis, may regulate gene expression with both PlcR and AtxA transcriptional regulators, each acting in a different environment.

Conclusions/significance: We have shown that homologous and even identical genes within the genomes of three closely related members of the B. cereus sensu lato group are in some instances regulated very differently, and that these differences can have important implications for virulence. This study provides insights into the evolution of the B. cereus group, and highlights the importance of looking beyond differences in gene content in comparative genomics studies.

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Growth curves of strains B. cereus G9241, B. anthracis Sterne 34F2, and B. cereus 10987 in MGM with normal aeration and with 14% CO2+0.8% bicarbonate.(A) The three Bacillus strains plotted against each other in each condition, exhibiting similar growth rates. (B) The three Bacillus species plotted against themselves in each condition, showing slightly slower growth rates for G9241 and B. anthracis Sterne in the CO2 environment. Curves are representative examples of 5 experiments with similar trends.
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pone-0004904-g001: Growth curves of strains B. cereus G9241, B. anthracis Sterne 34F2, and B. cereus 10987 in MGM with normal aeration and with 14% CO2+0.8% bicarbonate.(A) The three Bacillus strains plotted against each other in each condition, exhibiting similar growth rates. (B) The three Bacillus species plotted against themselves in each condition, showing slightly slower growth rates for G9241 and B. anthracis Sterne in the CO2 environment. Curves are representative examples of 5 experiments with similar trends.

Mentions: For characterization of the global transcriptional patterns of B. cereus G9241, B. anthracis Sterne 34F2, and B. cereus 10987 (hereafter referred to as G9241, B. anthracis, and 10987, respectively), we first determined the growth characteristics of these three strains in a semi-defined medium under both high aeration and 14% CO2+0.8% bicarbonate conditions (hereafter referred to as O2 and CO2). The medium used in this study, Modified G Medium (MGM), is typically used to produce high levels of B. anthracis spores (see Methods). This medium was used in earlier transcriptional profiling studies of B. anthracis, and its use here provides for continuity with those studies [8], [9]. Figure 1 illustrates the growth characteristics of the three Bacilli in MGM in O2 and CO2 (1 experiment representative of 5). Overall, the three strains grew at a slightly slower rate in CO2 than in O2, which is unsurprising, since energy production is generally more efficient in aerobic atmospheres. Depending on the time points used to calculate doubling times, rates of doubling in O2 ranged from 24 to 44 minutes, whereas doubling times in CO2 ranged from 31–55 minutes. However, within each growth condition, the strains displayed similar growth kinetics (Figure 1A), and they all reached stationary phase within 6 hours.


Comparative transcriptional profiling of Bacillus cereus sensu lato strains during growth in CO2-bicarbonate and aerobic atmospheres.

Passalacqua KD, Varadarajan A, Byrd B, Bergman NH - PLoS ONE (2009)

Growth curves of strains B. cereus G9241, B. anthracis Sterne 34F2, and B. cereus 10987 in MGM with normal aeration and with 14% CO2+0.8% bicarbonate.(A) The three Bacillus strains plotted against each other in each condition, exhibiting similar growth rates. (B) The three Bacillus species plotted against themselves in each condition, showing slightly slower growth rates for G9241 and B. anthracis Sterne in the CO2 environment. Curves are representative examples of 5 experiments with similar trends.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2654142&req=5

pone-0004904-g001: Growth curves of strains B. cereus G9241, B. anthracis Sterne 34F2, and B. cereus 10987 in MGM with normal aeration and with 14% CO2+0.8% bicarbonate.(A) The three Bacillus strains plotted against each other in each condition, exhibiting similar growth rates. (B) The three Bacillus species plotted against themselves in each condition, showing slightly slower growth rates for G9241 and B. anthracis Sterne in the CO2 environment. Curves are representative examples of 5 experiments with similar trends.
Mentions: For characterization of the global transcriptional patterns of B. cereus G9241, B. anthracis Sterne 34F2, and B. cereus 10987 (hereafter referred to as G9241, B. anthracis, and 10987, respectively), we first determined the growth characteristics of these three strains in a semi-defined medium under both high aeration and 14% CO2+0.8% bicarbonate conditions (hereafter referred to as O2 and CO2). The medium used in this study, Modified G Medium (MGM), is typically used to produce high levels of B. anthracis spores (see Methods). This medium was used in earlier transcriptional profiling studies of B. anthracis, and its use here provides for continuity with those studies [8], [9]. Figure 1 illustrates the growth characteristics of the three Bacilli in MGM in O2 and CO2 (1 experiment representative of 5). Overall, the three strains grew at a slightly slower rate in CO2 than in O2, which is unsurprising, since energy production is generally more efficient in aerobic atmospheres. Depending on the time points used to calculate doubling times, rates of doubling in O2 ranged from 24 to 44 minutes, whereas doubling times in CO2 ranged from 31–55 minutes. However, within each growth condition, the strains displayed similar growth kinetics (Figure 1A), and they all reached stationary phase within 6 hours.

Bottom Line: Although much of this phenotypic range can be attributed to the presence or absence of a few key virulence factors, there are other virulence-associated loci that are conserved throughout the B. cereus group, and we hypothesized that these genes may be regulated differently in pathogenic and non-pathogenic strains.We have shown that homologous and even identical genes within the genomes of three closely related members of the B. cereus sensu lato group are in some instances regulated very differently, and that these differences can have important implications for virulence.This study provides insights into the evolution of the B. cereus group, and highlights the importance of looking beyond differences in gene content in comparative genomics studies.

View Article: PubMed Central - PubMed

Affiliation: School of Biology, Georgia Institute of Technology, Atlanta, Georgia, United States of America.

ABSTRACT

Background: Bacillus species are spore-forming bacteria that are ubiquitous in the environment and display a range of virulent and avirulent phenotypes. This range is particularly evident in the Bacillus cereus sensu lato group; where closely related strains cause anthrax, food-borne illnesses, and pneumonia, but can also be non-pathogenic. Although much of this phenotypic range can be attributed to the presence or absence of a few key virulence factors, there are other virulence-associated loci that are conserved throughout the B. cereus group, and we hypothesized that these genes may be regulated differently in pathogenic and non-pathogenic strains.

Methodology/principal findings: Here we report transcriptional profiles of three closely related but phenotypically unique members of the Bacillus cereus group--a pneumonia-causing B. cereus strain (G9241), an attenuated strain of B. anthracis (Sterne 34F(2)), and an avirulent B. cereus strain (10987)--during exponential growth in two distinct atmospheric environments: 14% CO(2)/bicarbonate and ambient air. We show that the disease-causing Bacillus strains undergo more distinctive transcriptional changes between the two environments, and that the expression of plasmid-encoded virulence genes was increased exclusively in the CO(2) environment. We observed a core of conserved metabolic genes that were differentially expressed in all three strains in both conditions. Additionally, the expression profiles of putative virulence genes in G9241 suggest that this strain, unlike Bacillus anthracis, may regulate gene expression with both PlcR and AtxA transcriptional regulators, each acting in a different environment.

Conclusions/significance: We have shown that homologous and even identical genes within the genomes of three closely related members of the B. cereus sensu lato group are in some instances regulated very differently, and that these differences can have important implications for virulence. This study provides insights into the evolution of the B. cereus group, and highlights the importance of looking beyond differences in gene content in comparative genomics studies.

Show MeSH
Related in: MedlinePlus