Widespread occurrence of phage-encoded exotoxin genes in terrestrial and aquatic environments in Southern California

Casas, Veronica; Miyake, Jon H.; Balsley, Heather; Roark, Julie; Telles, Serena; Leeds, Steven; Zurita, Ivan; Breitbart, Mya; Bartlett, Doug; Azam, Farooq; Rohwer, Forest

doi:10.1111/j.1574-6968.2006.00345.x

Cited by 52 publications

(35 citation statements)

References 29 publications

(41 reference statements)

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“…Interactions of host bacteria with temperate bacteriophage also may influence microbial processes. Most notable are virulence factors of many pathogenic bacteria, such as exotoxins, that are phage encoded (7,8). Indirect evidence for a link between quorum sensing and the regulation of the lytic/lysogenic switch appeared recently when quorum sensing was shown to increase Shiga toxin (Stx toxin) production along with the transcription of -like phage genes in E. coli O157:H7 (48).…”

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confidence: 99%

Acyl-Homoserine Lactones Can Induce Virus Production in Lysogenic Bacteria: an Alternative Paradigm for Prophage Induction

Ghosh

Roy

Williamson

et al. 2009

Appl Environ Microbiol

108

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Prophage typically are induced to a lytic cycle under stressful environmental conditions or when the host's survival is threatened. However, stress-independent, spontaneous induction also occurs in nature and may be cell density dependent, but the in vivo signal(s) that can trigger induction is unknown. In the present study, we report that acyl-homoserine lactones (AHL), the essential signaling molecules of quorum sensing in many gram-negative bacteria, can trigger phage production in soil and groundwater bacteria. This phenomenon also was operative in a lysogen of Escherichia coli. In model coculture systems, we monitored the real-time AHL production from Pseudomonas aeruginosa PAO1 using an AHL bioluminescent sensor and demonstrated that -prophage induction in E. coli was correlated with AHL production. As a working model in E. coli, we show that the induction responses of with AHL remained unaffected when recA was deleted, suggesting that this mechanism does not involve an SOS response. In the same lysogen we also demonstrated that sdiA, the AHL receptor, and rcsA, a positive transcriptional regulator of exopolysaccharide synthesis, are involved in the AHL-mediated induction process. These findings relate viral reproduction to chemical signals associated with high host cell abundance, suggesting an alternative paradigm for prophage induction.

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confidence: 99%

Acyl-Homoserine Lactones Can Induce Virus Production in Lysogenic Bacteria: an Alternative Paradigm for Prophage Induction

Ghosh

Roy

Williamson

et al. 2009

Appl Environ Microbiol

108

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“…Phage-encoded exotoxins such as cholera toxin, diphtheria toxin, botulinium toxin, and Shiga toxin cause disease in mammals (4). Although these toxins do affect humans and other mammals, these phagecarried exotoxin genes are found at high frequencies in free phages and lysogenic bacteria that are isolated from environments where the presumed corresponding targets are not prevalent (6). These exotoxins kill eukaryotic cells by means of receptors and pathways that are generally conserved among eukaryotic organisms.…”

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confidence: 99%

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

2009

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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.

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“…For instance, Casas et al (19) demonstrated that phage-encoded exotoxins are widespread in water, sediment, and soil. Additionally, sequence analysis revealed a large number of protein secretion systems and virulence gene homologues in marine bacteria (6).…”

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Widespread Occurrence of Bacterial Human Virulence Determinants in Soil and Freshwater Environments

Søborg

Hendriksen

Kilian

et al. 2013

Appl Environ Microbiol

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bThe occurrence of 22 bacterial human virulence genes (encoding toxins, adhesins, secretion systems, regulators of virulence, inflammatory mediators, and bacterial resistance) in beech wood soil, roadside soil, organic agricultural soil, and freshwater biofilm was investigated by nested PCR. The presence of clinically relevant bacterial groups known to possess virulence genes was tested by PCR of 16S and 23S rRNA genes. For each of the virulence genes detected in the environments, sequencing and NCBI BLAST analysis confirmed the identity of the PCR products. The virulence genes showed widespread environmental occurrence, as 17 different genes were observed. Sixteen genes were detected in beech wood soil, and 14 were detected in roadside and organic agricultural soils, while 11 were detected in the freshwater biofilm. All types of virulence traits were represented in all environments; however, the frequency at which they were detected was variable. A principal-component analysis suggested that several factors influenced the presence of the virulence genes; however, their distribution was most likely related to the level of contamination by polycyclic aromatic hydrocarbons and pH. The occurrence of the virulence genes in the environments generally did not appear to be the result of the presence of clinically relevant bacteria, indicating an environmental origin of the virulence genes. The widespread occurrence of the virulence traits and the high degree of sequence conservation between the environmental and clinical sequences suggest that soil and freshwater environments may constitute reservoirs of virulence determinants normally associated with human disease.

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Widespread occurrence of phage-encoded exotoxin genes in terrestrial and aquatic environments in Southern California

Cited by 52 publications

References 29 publications

Acyl-Homoserine Lactones Can Induce Virus Production in Lysogenic Bacteria: an Alternative Paradigm for Prophage Induction

Acyl-Homoserine Lactones Can Induce Virus Production in Lysogenic Bacteria: an Alternative Paradigm for Prophage Induction

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

Widespread Occurrence of Bacterial Human Virulence Determinants in Soil and Freshwater Environments

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