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Grazing protozoa and the evolution of the Escherichia coli O157:H7 Shiga toxin-encoding prophage.

Steinberg KM, Levin BR - Proc. Biol. Sci. (2007)

Bottom Line: Why then does E. coli O157:H7 code for virulence determinants, like the Shiga toxins (Stxs), responsible for the morbidity and mortality of colonized humans?Here, we test the hypothesis that the carriage of the Stx-encoding prophage of E. coli O157:H7 increases the rate of survival of E. coli in the presence of grazing protozoa, Tetrahymena pyriformis.In the presence but not the absence of Tetrahymena, the carriage of the Stx-encoding prophage considerably augments the fitness of E. coli K-12 as well as clinical isolates of E. coli O157 by increasing the rate of survival of the bacteria in the food vacuoles of these ciliates.

View Article: PubMed Central - PubMed

Affiliation: Graduate Program in Population Biology, Ecology and Evolution, Emory University, Atlanta, GA 30322, USA. kmeltz@emory.edu

ABSTRACT
Humans play little role in the epidemiology of Escherichia coli O157:H7, a commensal bacterium of cattle. Why then does E. coli O157:H7 code for virulence determinants, like the Shiga toxins (Stxs), responsible for the morbidity and mortality of colonized humans? One possibility is that the virulence of these bacteria to humans is coincidental and these virulence factors evolved for and are maintained for other roles they play in the ecology of these bacteria. Here, we test the hypothesis that the carriage of the Stx-encoding prophage of E. coli O157:H7 increases the rate of survival of E. coli in the presence of grazing protozoa, Tetrahymena pyriformis. In the presence but not the absence of Tetrahymena, the carriage of the Stx-encoding prophage considerably augments the fitness of E. coli K-12 as well as clinical isolates of E. coli O157 by increasing the rate of survival of the bacteria in the food vacuoles of these ciliates. Grazing protozoa in the environment or natural host are likely to play a significant role in the ecology and maintenance of the Stx-encoding prophage of E. coli O157:H7 and may well contribute to the evolution of the virulence of these bacteria to colonize humans.

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C600gfp (prophage negative) and C600Pgfp (prophage positive) exposed to high density of Tetrahymena. (a) Estimated bacterial densities (CFU data) at 12 and 24 h, C600Pgfp (closed triangles) and C600gfp (open triangles). (b) Number of viable C600gfp and C600Pgfp cells per food vacuole, direct counts of fluorescing cells (*p<0.05 and ****p<0.00005). (c) C600Pgfp in food vacuoles. (d) C600gfp in food vacuoles. Scale bar, 5 μm.
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fig5: C600gfp (prophage negative) and C600Pgfp (prophage positive) exposed to high density of Tetrahymena. (a) Estimated bacterial densities (CFU data) at 12 and 24 h, C600Pgfp (closed triangles) and C600gfp (open triangles). (b) Number of viable C600gfp and C600Pgfp cells per food vacuole, direct counts of fluorescing cells (*p<0.05 and ****p<0.00005). (c) C600Pgfp in food vacuoles. (d) C600gfp in food vacuoles. Scale bar, 5 μm.

Mentions: The results of our plating experiments suggest that the colonies on the plates arise from single cells rather than vacuoles containing multiple bacteria. The colonies on the tetrazolium arabinose agar did not contain Ara− and Ara+ sectors and when restreaked on this indicator agar, the colonies produced were monomorphic Ara− or Ara+. As estimated from either colony count data or number of fluorescing bacteria per vesicle, there are more surviving prophage-bearing E. coli in the presence of Tetrahymena than prophage-free bacteria (figure 5a,b). The survival of the bacteria within the food vacuoles can be seen from confocal micrographs of Tetrahymena in figure 5c,d. In figure 5c, where C600 carries the prophage, there are an abundance of viable cells within the food vesicles. This is clearly not the case when C600 does not carry the prophage (figure 5d). In the absence of Tetrahymena, there is no difference in the rate of survival of the bacteria with the gfp with and without the prophage (data not shown).


Grazing protozoa and the evolution of the Escherichia coli O157:H7 Shiga toxin-encoding prophage.

Steinberg KM, Levin BR - Proc. Biol. Sci. (2007)

C600gfp (prophage negative) and C600Pgfp (prophage positive) exposed to high density of Tetrahymena. (a) Estimated bacterial densities (CFU data) at 12 and 24 h, C600Pgfp (closed triangles) and C600gfp (open triangles). (b) Number of viable C600gfp and C600Pgfp cells per food vacuole, direct counts of fluorescing cells (*p<0.05 and ****p<0.00005). (c) C600Pgfp in food vacuoles. (d) C600gfp in food vacuoles. Scale bar, 5 μm.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2211389&req=5

fig5: C600gfp (prophage negative) and C600Pgfp (prophage positive) exposed to high density of Tetrahymena. (a) Estimated bacterial densities (CFU data) at 12 and 24 h, C600Pgfp (closed triangles) and C600gfp (open triangles). (b) Number of viable C600gfp and C600Pgfp cells per food vacuole, direct counts of fluorescing cells (*p<0.05 and ****p<0.00005). (c) C600Pgfp in food vacuoles. (d) C600gfp in food vacuoles. Scale bar, 5 μm.
Mentions: The results of our plating experiments suggest that the colonies on the plates arise from single cells rather than vacuoles containing multiple bacteria. The colonies on the tetrazolium arabinose agar did not contain Ara− and Ara+ sectors and when restreaked on this indicator agar, the colonies produced were monomorphic Ara− or Ara+. As estimated from either colony count data or number of fluorescing bacteria per vesicle, there are more surviving prophage-bearing E. coli in the presence of Tetrahymena than prophage-free bacteria (figure 5a,b). The survival of the bacteria within the food vacuoles can be seen from confocal micrographs of Tetrahymena in figure 5c,d. In figure 5c, where C600 carries the prophage, there are an abundance of viable cells within the food vesicles. This is clearly not the case when C600 does not carry the prophage (figure 5d). In the absence of Tetrahymena, there is no difference in the rate of survival of the bacteria with the gfp with and without the prophage (data not shown).

Bottom Line: Why then does E. coli O157:H7 code for virulence determinants, like the Shiga toxins (Stxs), responsible for the morbidity and mortality of colonized humans?Here, we test the hypothesis that the carriage of the Stx-encoding prophage of E. coli O157:H7 increases the rate of survival of E. coli in the presence of grazing protozoa, Tetrahymena pyriformis.In the presence but not the absence of Tetrahymena, the carriage of the Stx-encoding prophage considerably augments the fitness of E. coli K-12 as well as clinical isolates of E. coli O157 by increasing the rate of survival of the bacteria in the food vacuoles of these ciliates.

View Article: PubMed Central - PubMed

Affiliation: Graduate Program in Population Biology, Ecology and Evolution, Emory University, Atlanta, GA 30322, USA. kmeltz@emory.edu

ABSTRACT
Humans play little role in the epidemiology of Escherichia coli O157:H7, a commensal bacterium of cattle. Why then does E. coli O157:H7 code for virulence determinants, like the Shiga toxins (Stxs), responsible for the morbidity and mortality of colonized humans? One possibility is that the virulence of these bacteria to humans is coincidental and these virulence factors evolved for and are maintained for other roles they play in the ecology of these bacteria. Here, we test the hypothesis that the carriage of the Stx-encoding prophage of E. coli O157:H7 increases the rate of survival of E. coli in the presence of grazing protozoa, Tetrahymena pyriformis. In the presence but not the absence of Tetrahymena, the carriage of the Stx-encoding prophage considerably augments the fitness of E. coli K-12 as well as clinical isolates of E. coli O157 by increasing the rate of survival of the bacteria in the food vacuoles of these ciliates. Grazing protozoa in the environment or natural host are likely to play a significant role in the ecology and maintenance of the Stx-encoding prophage of E. coli O157:H7 and may well contribute to the evolution of the virulence of these bacteria to colonize humans.

Show MeSH
Related in: MedlinePlus