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Journal of Bacteriology, August 2009, p. 5116-5122, Vol. 191, No. 16
0021-9193/09/$08.00+0     doi:10.1128/JB.00508-09
Copyright © 2009, American Society for Microbiology. All Rights Reserved.

Shiga Toxin as a Bacterial Defense against a Eukaryotic Predator, Tetrahymena thermophila{triangledown}

William Lainhart,{dagger} Gino Stolfa,{dagger} and Gerald B. Koudelka*

Department of Biological Sciences University at Buffalo, Buffalo, New York 14260

Received 13 April 2009/ Accepted 27 May 2009

Bacterially derived exotoxins kill eukaryotic cells by inactivating factors and/or pathways that are universally conserved among eukaryotic organisms. The genes that encode these exotoxins are commonly found in bacterial viruses (bacteriophages). In the context of mammals, these toxins cause diseases ranging from cholera to diphtheria to enterohemorrhagic diarrhea. Phage-carried exotoxin genes are widespread in the environment and are found with unexpectedly high frequency in regions lacking the presumed mammalian "targets," suggesting that mammals are not the primary targets of these exotoxins. We suggest that such exotoxins may have evolved for the purpose of bacterial antipredator defense. We show here that Tetrahymena thermophila, a bacterivorous predator, is killed when cocultured with bacteria bearing a Shiga toxin (Stx)-encoding temperate bacteriophage. In cocultures with Tetrahymena, the Stx-encoding bacteria display a growth advantage over those that do not produce Stx. Tetrahymena is also killed by purified Stx. Disruption of the gene encoding the StxB subunit or addition of an excess of the nontoxic StxB subunit substantially reduced Stx holotoxin toxicity, suggesting that this subunit mediates intake and/or trafficking of Stx by Tetrahymena. Bacterially mediated Tetrahymena killing was blocked by mutations that prevented the bacterial SOS response (recA mutations) or by enzymes that breakdown H2O2 (catalase), suggesting that the production of H2O2 by Tetrahymena signals its presence to the bacteria, leading to bacteriophage induction and production of Stx.

* Corresponding author. Mailing address: Department of Biological Sciences, University at Buffalo, Cooke Hall, North Campus, Buffalo, NY 14260. Phone: (716) 645-2363, ext. 158. Fax: (716) 645-2975. E-mail: koudelka{at}buffalo.edu

{triangledown} Published ahead of print on 5 June 2009.

{dagger} These authors contributed equally to this work.

Journal of Bacteriology, August 2009, p. 5116-5122, Vol. 191, No. 16
0021-9193/09/$08.00+0     doi:10.1128/JB.00508-09
Copyright © 2009, American Society for Microbiology. All Rights Reserved.





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