Molecular Mechanisms Governing “Hair-Trigger” Induction of Shiga Toxin-Encoding Prophages

Chakraborty, Dolonchapa; Clark, Eric M.; Mauro, Steven A.; Koudelka, Gerald B.

doi:10.3390/v10050228

Cited by 15 publications

(21 citation statements)

References 47 publications

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“…The first step in prophage induction is a RecA-dependent autocleavage of the cI repressor that is required for lysogenic establishment to repress the prophage replication and subsequent activation of lytic promoters [27]. Expression of stx2 and induction of Stx-prophage also result from proteolytic cleavage of the cI repressor, allowing expression of early and middle phage genes [19,28,29]. Absence of cI leads to the expression of the anti-terminators Q.…”

Section: Discussionmentioning

confidence: 99%

“…Shiga toxin production in Escherichia coli is coregulated through induction of the prophage that encodes toxin gene stx2 [11][12][13][14][15][16][17][18]. Activation of the SOS response by MTC and H 2 O 2 , which cause DNA damage, or antimicrobial agents such as quinolones, which inhibit DNA replication, triggers substantial Stx-phage induction and results in high Stx2 production [11][12][13][14][15][16][17]19]. Since the effect of H 2 O 2 or antibiotics on ArtAB production in Salmonella spp.…”

Section: Introductionmentioning

confidence: 99%

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Influence of SOS-inducing agents on the expression of ArtAB toxin gene in Salmonella enterica and Salmonella bongori

et al. 2020

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Salmonella enterica subspecies enterica serovar Typhimurium (S. Typhimurium) definitive phage type 104 (DT104), S. enterica subspecies enterica serovar Worthington (S. Worthington) and S. bongori produce ArtA and ArtB (ArtAB) toxin homologues, which catalyse ADP-ribosylation of pertussis toxin-sensitive G protein. ArtAB gene (artAB) is encoded on prophage in DT104 and its expression is induced by mitomycin C (MTC) and hydrogen peroxide (H 2 O 2 ) that trigger the bacterial SOS response. Although the genetic regulatory mechanism associated with artAB expression is not characterized, it is thought to be associated with prophage induction, which occurs when the RecA-mediated SOS response is triggered. Here we show that subinhibitory concentration of quinolone antibiotics that are SOS-inducing agents, also induce ArtAB production in these Salmonella strains. Both MTC and fluoroquinolone antibiotics such as enrofloxacin-induced artA and recA transcription and artAB-encoding prophage (ArtAB-prophage) in DT104 and S. Worthington. However, in S. bongori, which harbours artAB genes on incomplete prophage, artA transcription was induced by MTC and enrofloxacin, but prophage induction was not observed. Taken together, these results suggest that SOS response followed by induction of artAB transcription is essential for ArtAB production. H 2 O 2 -mediated induction of ArtAB prophage and efficient production of ArtAB was observed in DT104 but not in S. Worthington and S. bongori. Therefore, induction of artAB expression with H 2 O 2 is strain-specific, and the mode of action of H 2 O 2 as an SOS-inducing agent might be different from those of MTC and quinolone antibiotics.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Influence of SOS-inducing agents on the expression of ArtAB toxin gene in Salmonella enterica and Salmonella bongori

et al. 2020

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“…In a small subset of the lysogens the prophage is induced to lytic cycle by stimuli like H 2 O 2 (Shimizu et al, 2009; Los et al, 2010, 2013). The lysis of the bacteria causes the release of Shiga toxin which acts on their predators (protozoan or neutrophils as the case maybe) (Dydecka et al, 2017; Chakraborty et al, 2018). The attenuation or inactivation of the predators is thought to increase the survivability of the rest of the population.…”

Section: Why Are Prophages Prevalent In Bacterial Genomes?mentioning

confidence: 99%

Bacterial ‘Grounded’ Prophages: Hotspots for Genetic Renovation and Innovation

2019

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Bacterial genomes are highly plastic allowing the generation of variants through mutations and acquisition of genetic information. The fittest variants are then selected by the econiche thereby allowing the bacterial adaptation and colonization of the habitat. Larger genomes, however, may impose metabolic burden and hence bacterial genomes are optimized by the loss of frivolous genetic information. The activity of temperate bacteriophages has acute consequences on the bacterial population as well as the bacterial genome through lytic and lysogenic cycles. Lysogeny is a selective advantage as the prophage provides immunity to the lysogen against secondary phage attack. Since the non-lysogens are eliminated by the lytic phages, lysogens multiply and colonize the habitat. Nevertheless, all lysogens have an imminent risk of lytic cycle activation and cell lysis. However, a mutation in the attachment sites or in the genes that encode the specific recombinase responsible for prophage excision could result in ‘grounding’ of the prophage. Since the lysogens with grounded prophage are immune to respective phage infection as well as dodge the induction of lytic cycle, we hypothesize that the selection of these mutant lysogens is favored relative to their normal lysogenic counterparts. These grounded prophages offer several advantages to the bacterial genome evolution through propensity for genetic variations including inversions, deletions, and insertions via horizontal gene transfer. We propose that the grounded prophages expedite bacterial genome evolution by acting as ‘genetic buffer zones’ thereby increasing the frequency as well as the diversity of variations on which natural selection favors the beneficial variants. The grounded prophages are also hotspots for horizontal gene transfer wherein several ecologically significant genes such as those involved in stress tolerance, antimicrobial resistance, and novel metabolic pathways, are integrated. Moreover, the high frequency of genetic changes within prophages also allows proportionate probability for the de novo genesis of genetic information. Through sequence analyses of well-characterized E. coli prophages we exemplify various roles of grounded prophages in E. coli ecology and evolution. Therefore, the temperate prophages are one of the most significant drivers of bacterial genome evolution and sites of biogenesis of genetic information.

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“…Toxin molecules lacking the signal leading peptide for secretion are released upon cell lysis. The lysogeny in stxconverting phages is less stable compared to stx-lambdoid phages [11][12][13][14] resulting in higher rate of spontaneous induction and in increased sensitivity to environmental factors. Many antibiotics also increase the induction rate of Stx-converting prophages thus enhancing the toxin production.…”

Section: Introductionmentioning

confidence: 99%

The lysogenization of the non-O157Escherichia colistrains by stx-converting bacteriophage phi24B is associated with the O antigen loss and reduced fitness

Golomidova

Efimov

Kulikov

et al. 2019

Preprint

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The lysogenization of the non-O157 Escherichia coli strains by stxconverting bacteriophage phi24B is associated with the O antigen loss and reduced fitnessThe ability of the Shiga-toxigenic E. coli (STEC) to produce the toxin depends on the lysogenic conversion by stx-bacteriophages. The canonical stx-phage phi24B can lysogenize a wide variety of E. coli strains. In vivo the secondary lysogenization of symbiotic E. coli strains by the phages released by infecting STEC populations may contribute to the overall patient toxic load and to lead to the emergence of new pathogenic STEC strains. However, in our experiment all the phi24B lysogens obtained from the environmental E. coli isolates had compromised O-antigen (Oag) biosynthesis. These lysogenic strains gained the sensitivity to the T5-like bacteriophages and featured increased sensitivity to the bactericidal activity of the horse serum. We conclude that in most of E. coli strains the Oag effectively restricts phi24B infection. The lysogenic clones predominantly rise from the Oag deficient mutants and therefore they have reduced fitness compared to the parental strain.

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Molecular Mechanisms Governing “Hair-Trigger” Induction of Shiga Toxin-Encoding Prophages

Cited by 15 publications

References 47 publications

Influence of SOS-inducing agents on the expression of ArtAB toxin gene in Salmonella enterica and Salmonella bongori

Influence of SOS-inducing agents on the expression of ArtAB toxin gene in Salmonella enterica and Salmonella bongori

Bacterial ‘Grounded’ Prophages: Hotspots for Genetic Renovation and Innovation

The lysogenization of the non-O157Escherichia colistrains by stx-converting bacteriophage phi24B is associated with the O antigen loss and reduced fitness

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