Prophage Activation in the Intestine: Insights Into Functions and Possible Applications

Hu, Jie; Ye, Hao; Wang, Shilan; Wang, Junjun; Han, Dandan

doi:10.3389/fmicb.2021.785634

Cited by 37 publications

(22 citation statements)

References 130 publications

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“…We found prophages in Salmonella and VTEC that were most closely related to those of other hosts, such as Klebsiella, Haemophilus and Vibrio. The identification of genetically similar prophages amongst distinct bacteria may broaden the host range when designing future prophage therapies (e.g., engineering broadrange prophage induction agents) against foodborne pathogens (Hu et al, 2021). Furthermore, the discovery of distant hosts with closely-associated clinical outcomes may be attributed to the impact of the host environment in phage-host interactions.…”

Section: General Prophage Characterizationmentioning

confidence: 99%

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Prophage Diversity Across Salmonella and Verotoxin-Producing Escherichia coli in Agricultural Niches of British Columbia, Canada

Fong

Brenner

et al. 2022

Front. Microbiol.

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Prophages have long been regarded as an important contributor to the evolution of Salmonella and Verotoxin-producing E. coli (VTEC), members of the Enterobacteriaceae that cause millions of cases of foodborne illness in North America. In S. Typhimurium, prophages provide many of the genes required for invasion; similarly, in VTEC, the Verotoxin-encoding genes are located in cryptic prophages. The ability of prophages to quickly acquire and lose genes have driven their rapid evolution, leading to highly diversified populations of phages that can infect distantly-related bacterial hosts. To defend against foreign genetic materials (i.e., phages), bacteria have evolved Clustered Regularly Interspaced Short Palindromic Repeats (CRISPR) immunity, consisting of variable spacer regions that match short nucleic acid sequences of invaders previously encountered. The number of spacer regions varies widely amongst Enterobacteriaceae, and there is currently no clear consensus if the accumulation of spacers is linked to genomic prophage abundance. Given the immense prophage diversity and contribution to bacterial host phenotypes, we analyzed the prophage sequences within 118 strains of Salmonella and VTEC, 117 of which are of agricultural origin. Overall, 130 unique prophage sequences were identified and they were found to be remarkably diverse with <50% nucleotide similarity, particularly with the Gifsy-1 group which was identified in several Salmonella serovars and interestingly, a strain of VTEC. Additionally, we identified a novel plasmid-like phage that carried antibiotic resistance and bacteriocin resistance genes. The strains analyzed carried at least six distinct spacers which did not possess homology to prophages identified in the same genome. In fact, only a fraction of all identified spacers (14%) possessed significant homology to known prophages. Regression models did not discern a correlation between spacer and prophage abundance in our strains, although the relatively high number of spacers in our strains (an average of 27 in Salmonella and 19 in VTEC) suggest that high rates of infection may occur in agricultural niches and be a contributing driver in bacterial evolution. Cumulatively, these results shed insight into prophage diversity of Salmonella and VTEC, which will have further implications when informing development of phage therapies against these foodborne pathogens.

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Section: General Prophage Characterizationmentioning

confidence: 99%

“…Prophages may also be employed as antimicrobials (Hu et al, 2021). When environmental triggers inflict stress upon the host cell (e.g., UV light, antibiotic treatment) and induce the bacterial SOS response, prophage induction occurs, where the prophage excises from the genome, ultimately leads to host cell lysis and death (Fu et al, 2019).…”

Section: Introductionmentioning

confidence: 99%

Prophage Diversity Across Salmonella and Verotoxin-Producing Escherichia coli in Agricultural Niches of British Columbia, Canada

Fong

Brenner

et al. 2022

Front. Microbiol.

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“…9). This is particularly evident under MMC-induction, a condition that mimics the Stx-phage induction [190][191][192][193][194][195]. In this context, we note that the definition of pathogenic potential is often skewed by anthropogenic biases, such as fitness factors that are not, per se, accounted for in the virulence inventory and may allow pathogens to access the production foods for human consumption 197].…”

Section: Discussionmentioning

confidence: 99%

Pathogenomes and variations in Shiga toxin production among geographically distinct clones of Escherichia coli O113:H21

et al. 2022

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Infections with globally disseminated Shiga toxin-producing Escherichia coli (STEC) of the O113:H21 serotype can progress to severe clinical complications, such as hemolytic uremic syndrome (HUS). Two phylogeographically distinct clonal complexes have been established by multi locus sequence typing (MLST). Infections with ST-820 isolates circulating exclusively in Australia have caused severe human disease, such as HUS. Conversely, ST-223 isolates prevalent in the US and outside Australia seem to rarely cause severe human disease but are frequent contaminants. Following a genomic epidemiology approach, we wanted to gain insights into the underlying cause for this disparity. We examined the plasticity in the genome make-up and Shiga toxin production in a collection of 20 ST-820 and ST-223 strains isolated from produce, the bovine reservoir, and clinical cases. STEC are notorious for assembly into fragmented draft sequences when using short-read sequencing technologies due to the extensive and partly homologous phage complement. The application of long-read technology (LRT) sequencing yielded closed reference chromosomes and plasmids for two representative ST-820 and ST-223 strains. The established high-resolution framework, based on whole genome alignments, single nucleotide polymorphism (SNP)-typing and MLST, includes the chromosomes and plasmids of other publicly available O113:H21 sequences and allowed us to refine the phylogeographical boundaries of ST-820 and ST-223 complex isolates and to further identify a historic non-shigatoxigenic strain from Mexico as a quasi-intermediate. Plasmid comparison revealed strong correlations between the strains’ featured pO113 plasmid genotypes and chromosomally inferred ST, which suggests coevolution of the chromosome and virulence plasmids. Our pathogenicity assessment revealed statistically significant differences in the Stx2a-production capabilities of ST-820 as compared to ST-223 strains under RecA-induced Stx phage mobilization, a condition that mimics Stx-phage induction. These observations suggest that ST-820 strains may confer an increased pathogenic potential in line with the strain-associated epidemiological metadata. Still, some of the tested ST-223 cultures sourced from contaminated produce or the bovine reservoir also produced Stx at levels comparable to those of ST-820 isolates, which calls for awareness and for continued surveillance of this lineage.

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“…Phages can either undergo a lytic or a lysogenic cycle ( Kannen et al, 2019 ). The lytic infection cycle results in the bacterial lysis and the release of phage copies whereas temperate phages integrates into the host bacterial chromosome (prophages) without causing cell lysis, until a certain stimulator initiates the lytic phase resulting in bacterial cell death ( Hu et al, 2021 ). The antimicrobial activity of phages as modulators of microbial communities is assumed by the virulent or lytic phages whereas temperate phages contribute to the pathogenicity and coexistence of the bacteria in the ecosystem ( Gogokhia et al, 2019 ).…”

Section: Bacteriophagesmentioning

confidence: 99%

Bacteriophage-mediated manipulations of microbiota in gastrointestinal diseases

2022

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Although some gastrointestinal diseases could be managed using various antibiotics regimen, this therapeutic approach lacks precision and damages the microbiota. Emerging literature suggests that phages may play a key role in restoring the gut microbiome balance and controlling disease progression either with exogenous phage intervention or filtered fecal transplantation or even engineered phages. In this review, we will discuss the current phage applications aiming at controlling the bacterial population and preventing infection, inflammation, and cancer progression in the context of gastrointestinal diseases.

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Prophage Activation in the Intestine: Insights Into Functions and Possible Applications

Cited by 37 publications

References 130 publications

Prophage Diversity Across Salmonella and Verotoxin-Producing Escherichia coli in Agricultural Niches of British Columbia, Canada

Prophage Diversity Across Salmonella and Verotoxin-Producing Escherichia coli in Agricultural Niches of British Columbia, Canada

Pathogenomes and variations in Shiga toxin production among geographically distinct clones of Escherichia coli O113:H21

Bacteriophage-mediated manipulations of microbiota in gastrointestinal diseases

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