The role of pseudolysogeny in bacteriophage-host interactions in a natural freshwater environment

Ripp, Steven; Miller, Robert V.

doi:10.1099/00221287-143-6-2065

Cited by 106 publications

(95 citation statements)

References 20 publications

(38 reference statements)

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“…It has been suggested to influence phage survival (Ripp and Miller, 1997), phage-dependent bacterial mortality (Ripp and Miller, 1998) and the virulence of certain bacterial strains (Sakaguchi et al, 2005). Although it has been observed that P. acnes phages can adopt pseudolysogeny (Lood and Collin, 2011), for the first time we revealed that this behavior is largely dependent on the lineages of the host strains and is not a property of the phages.…”

Section: Phage Strainsmentioning

confidence: 67%

“…Pseudolysogeny occurs abundantly in natural environments and is an important part of bacteria-phage interactions (Ripp and Miller, 1997). It has been suggested to influence phage survival (Ripp and Miller, 1997), phage-dependent bacterial mortality (Ripp and Miller, 1998) and the virulence of certain bacterial strains (Sakaguchi et al, 2005).…”

Section: Phage Strainsmentioning

confidence: 99%

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The diversity and host interactions of Propionibacterium acnes bacteriophages on human skin

et al. 2015

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The viral population, including bacteriophages, is an important component of the human microbiota, yet is poorly understood. We aim to determine whether bacteriophages modulate the composition of the bacterial populations, thus potentially playing a role in health or disease. We investigated the diversity and host interactions of the bacteriophages of Propionibacterium acnes, a major human skin commensal implicated in acne pathogenesis. By sequencing 48 P. acnes phages isolated from acne patients and healthy individuals and by analyzing the P. acnes phage populations in healthy skin metagenomes, we revealed that P. acnes phage populations in the skin microbial community are often dominated by one strain. We also found phage strains shared among both related and unrelated individuals, suggesting that a pool of common phages exists in the human population and that transmission of phages may occur between individuals. To better understand the bacterium-phage interactions in the skin microbiota, we determined the outcomes of 74 genetically defined Propionibacterium strains challenged by 15 sequenced phages. Depending on the Propionibacterium lineage, phage infection can result in lysis, pseudolysogeny, or resistance. In type II P. acnes strains, we found that encoding matching clustered regularly interspaced short palindromic repeat spacers is insufficient to confer phage resistance. Overall, our findings suggest that the prey-predator relationship between bacteria and phages may have a role in modulating the composition of the microbiota. Our study also suggests that the microbiome structure of an individual may be an important factor in the design of phage-based therapy.

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Section: Phage Strainsmentioning

confidence: 67%

Section: Phage Strainsmentioning

confidence: 99%

The diversity and host interactions of Propionibacterium acnes bacteriophages on human skin

et al. 2015

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“…Such behaviour suggests that these viruses are fluctuating between states of pseudolysogeny/lysogeny and lytic pathways (Figure 6), behaviour widely documented for environmental phages (Abedon, 2008). This choice of life-cycle has been shown to aid in the regulation of bacterial biomass (Ripp and Miller, 1997), which is not taken into consideration in our calculations of removal. In addition, the extremely high abundance of phages 1 h after incubation with 13 C-labelled E. coli was surprising; however, Zeng and Golding (2011) showed that E. phage lambda can infect, replicate and enter the lysogenic cycle within E. coli after only 80 min.…”

Section: Discussionmentioning

confidence: 99%

Stable-isotope probing and metagenomics reveal predation by protozoa drives E. coli removal in slow sand filters

et al. 2014

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Stable-isotope probing and metagenomics were applied to study samples taken from laboratoryscale slow sand filters 0.5, 1, 2, 3 and 4 h after challenging with 13 C-labelled Escherichia coli to determine the mechanisms and organisms responsible for coliform removal. Before spiking, the filters had been continuously operated for 7 weeks using water from the River Kelvin, Glasgow as their influent source. Direct counts and quantitative PCR assays revealed a clear predator-prey response between protozoa and E. coli. The importance of top-down trophic-interactions was confirmed by metagenomic analysis, identifying several protozoan and viral species connected to E. coli attrition, with protozoan grazing responsible for the majority of the removal. In addition to top-down mechanisms, indirect mechanisms, such as algal reactive oxygen species-induced lysis, and mutualistic interactions between algae and fungi, were also associated with coliform removal. The findings significantly further our understanding of the processes and trophic interactions underpinning E. coli removal. This study provides an example for similar studies, and the opportunity to better understand, manage and enhance E. coli removal by allowing the creation of more complex trophic interaction models.

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“…Like the explanation for differential substrate utilization in different gut compartments, perhaps one explanation for the greater proportion of phages in the ileal metagenomes compared with those of the the large intestine is connected to gut physiology: the ileal microbiota could be subject to cyclic feast or famine conditions, and due to the role of phages in nutrient release (Abedon, 2009), there could be a fitness cost of phage resistance in ileal bacteria. In addition, pseudolysogeny is an unstable state of phage replication that could promote viral survival in nutrient-limited environments (Ripp and Miller, 1997) and yield-increased copies of stalledphage genomes in bacterial cells. Studies of phage ecology in a host-associated environment of limited bacterial richness, such as the ileum, will inform the complex inter-kingdom dynamics in host-associated environments.…”

Section: Gut Microbes Subdivided By Location and Treatment T Looft Et Almentioning

confidence: 99%

Bacteria, phages and pigs: the effects of in-feed antibiotics on the microbiome at different gut locations

Looft

Allen

Cantarel³

et al. 2014

The ISME Journal

330

265

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Disturbance of the beneficial gut microbial community is a potential collateral effect of antibiotics, which have many uses in animal agriculture (disease treatment or prevention and feed efficiency improvement). Understanding antibiotic effects on bacterial communities at different intestinal locations is essential to realize the full benefits and consequences of in-feed antibiotics. In this study, we defined the lumenal and mucosal bacterial communities from the small intestine (ileum) and large intestine (cecum and colon) plus feces, and characterized the effects of in-feed antibiotics (chlortetracycline, sulfamethazine and penicillin (ASP250)) on these communities. 16S rRNA gene sequence and metagenomic analyses of bacterial membership and functions revealed dramatic differences between small and large intestinal locations, including enrichment of Firmicutes and phage-encoding genes in the ileum. The large intestinal microbiota encoded numerous genes to degrade plant cell wall components, and these genes were lacking in the ileum. The mucosaassociated ileal microbiota harbored greater bacterial diversity than the lumen but similar membership to the mucosa of the large intestine, suggesting that most gut microbes can associate with the mucosa and might serve as an inoculum for the lumen. The collateral effects on the microbiota of antibiotic-fed animals caused divergence from that of control animals, with notable changes being increases in Escherichia coli populations in the ileum, Lachnobacterium spp. in all gut locations, and resistance genes to antibiotics not administered. Characterizing the differential metabolic capacities and response to perturbation at distinct intestinal locations will inform strategies to improve gut health and food safety.

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The role of pseudolysogeny in bacteriophage-host interactions in a natural freshwater environment

Cited by 106 publications

References 20 publications

The diversity and host interactions of Propionibacterium acnes bacteriophages on human skin

The diversity and host interactions of Propionibacterium acnes bacteriophages on human skin

Stable-isotope probing and metagenomics reveal predation by protozoa drives E. coli removal in slow sand filters

Bacteria, phages and pigs: the effects of in-feed antibiotics on the microbiome at different gut locations

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