Shiga Toxin as a Bacterial Defense against a Eukaryotic Predator, Tetrahymena thermophila
- 15 August 2009
- journal article
- Published by American Society for Microbiology in Journal of Bacteriology
- Vol. 191 (16), 5116-5122
- https://doi.org/10.1128/jb.00508-09
Abstract
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 H(2)O(2) (catalase), suggesting that the production of H(2)O(2) by Tetrahymena signals its presence to the bacteria, leading to bacteriophage induction and production of Stx.Keywords
This publication has 69 references indexed in Scilit:
- Refined annotation and assembly of the Tetrahymena thermophila genome sequence through EST analysis, comparative genomic hybridization, and targeted gap closureBMC Genomics, 2008
- Grazing protozoa and the evolution of the Escherichia coli O157:H7 Shiga toxin-encoding prophageProceedings Of The Royal Society B-Biological Sciences, 2007
- The Tetrahymena thermophila Phagosome ProteomeEukaryotic Cell, 2006
- Macronuclear Genome Sequence of the Ciliate Tetrahymena thermophila, a Model EukaryotePLoS Biology, 2006
- Slot blot immunoassay as a tool for plasmid-encoded toxin detection in enteroaggregative Escherichia coli culture supernatantsDiagnostic Microbiology and Infectious Disease, 2006
- Elucidation of Clathrin-Mediated Endocytosis in Tetrahymena Reveals an Evolutionarily Convergent Recruitment of DynaminPLoS Genetics, 2005
- Off the hook – how bacteria survive protozoan grazingTrends in Microbiology, 2005
- Toxin Gene Expression by Shiga Toxin-Producing Escherichia coli: the Role of Antibiotics and the Bacterial SOS ResponseEmerging Infectious Diseases, 2000
- Hemorrhagic Colitis Associated with a RareEscherichia coliSerotypeNew England Journal of Medicine, 1983
- Kinetics of recA protein-directed inactivation of repressors of phage λ and phage P22Journal of Molecular Biology, 1980