The human gut is host to a dense microbial community that includes a large bacteriophage population. This Review summarizes bacteria and phage dynamics in health and disease, and considers how phages may be harnessed as novel therapeutics to improve disease outcomes. The human gut is host to one of the densest microbial communities known, the gut microbiota, which contains bacteria, archaea, viruses, fungi and other microbial eukaryotes. Bacteriophages in the gut are largely unexplored, despite their potential to regulate bacterial communities and thus human health. In addition to helping us understand gut homeostasis, applying an ecological perspective to the study of bacterial and phage communities in the gut will help us to understand how this microbial system functions. For example, temporal studies of bacteria, phages and host immune cells in the gut during health and disease could provide key information about disease development and inform therapeutic treatments, whereas understanding the regulation of the replication cycles of phages could help harness the gut microbiota to improve disease outcomes. As the most abundant biological entities in our gut, we must consider bacteriophages in our pursuit of personalized medicine.

Menage a trois in the human gut: interactions between host, bacteria and phages

The human intestinal microbiota is one of the most densely populated ecosystems on Earth, containing up to 1013 bacteria/g and in some respects can be considered an organ itself given its role in human health. Bacteriophages (phages) are the most abundant replicating entities on the planet and thrive wherever their bacterial hosts exist. They undoubtedly influence the dominant microbial populations in many ecosystems including the human intestine. Within this setting, lysogeny appears to be the preferred life cycle, presumably due to nutrient limitations and lack of suitable hosts protected in biofilms, hence the predator/prey dynamic observed in many ecosystems is absent. On the other hand, free virulent phages in the gut are more common among sufferers of intestinal diseases and have been shown to increase with antibiotic usage. Many of these phages evolve from prophages of intestinal bacteria and emerge under conditions where their bacterial hosts encounter stress suggesting that prophages can significantly alter the microbial community composition. Based on these observations, we propose the “community shuffling” model which hypothesizes that prophage induction contributes to intestinal dysbiosis by altering the ratio of symbionts to pathobionts, enabling pathobiont niche reoccupation. The consequences of the increased phage load on the mammalian immune system are also addressed. While this is an area of intestinal biology which has received little attention, this review assembles evidence from the literature which supports the role of phages as one of the biological drivers behind the composition of the gut microbiota.

/pdf/movers-and-shakers-influence-of-bacteriophages-in-shaping-2k206bfl1q.pdf

Movers and shakers: influence of bacteriophages in shaping the mammalian gut microbiota.

After ingestion via contaminated food or water, enterohaemorrhagic E. coli colonises the intestinal mucosa and produces Shiga toxins (Stx). No Stx-specific secretion system has been described so far, and it is assumed that Stx are released into the gut lumen after bacterial lysis. Human intestinal epithelium does not express the Stx receptor Gb3 or other Stx binding sites, and it remains unknown how Stx cross the intestinal epithelial barrier and gain access to the systemic circulation. This review summarises current knowledge about the influence of the intestinal environment on Stx production and release, Stx interaction with intestinal epithelial cells and intracellular uptake, and toxin translocation into underlying tissues. Furthermore, it highlights gaps in understanding that need to be addressed by future research.

https://www.mdpi.com/2072-6651/3/6/626/pdf

Shiga toxin interaction with human intestinal epithelium.

Shiga Toxin Producing Escherichia coli.

Within-host competition between parasites is frequently invoked as a major force for parasite evolution, yet quantitative studies on its extent in an organismal group are lacking. Temperate bacteriophages are diverse and abundant parasites of bacteria, distinguished by their ability to enter a facultative dormant state in their host. Bacteria can accumulate multiple phages that may eventually abandon dormancy in response to host stress. Host resources are then converted into phage particles, whose release requires cell death. To study within-host competition between phages, I used the bacterium Escherichia coli and 11 lambdoid phages to construct single and double lysogens. Lysogenic bacterial cultures were then induced and time to host cell lysis and productivity of phages was measured. In double lysogens, this revealed strong competitive interactions as in all cases productivity of at least one phage declined. The outcome of within-host competition was often asymmetrical, and phages were found to vary hierarchically in within-host competitive ability. In double infections, the phage with the shorter lysis time determined the timing of cell lysis, which was associated with a competitive advantage when time differences were large. The results emphasize that within-host competition greatly affects phage fitness and that multiple infections should be considered an integral part of bacteriophage ecology.

/pdf/within-host-competition-determines-reproductive-success-of-17ikgv1wnc.pdf

Within-host competition determines reproductive success of temperate bacteriophages.

Differential efficiency of induction of various lambdoid prophages responsible for production of Shiga toxins in response to different induction agents

Although most Escherichia coli strains occur in the mammalian intestine as commensals, some of them, including enterohemorrhagic E. coli (EHEC), are capable of causing disease in humans. The most notorious virulence factors of EHEC are Shiga toxins, encoded by genes located on genomes of lambdoid prophages. Production and release of these toxins is strongly stimulated after the induction of these prophages. Many antibiotics used to treat bacterial infections stimulate induction of Shiga toxin-converting prophages, enhancing severity of the disease symptoms. Hence, treatment with antibiotics is not recommended if infection with EHEC is confirmed or even suspected. In this light, rapid detection of EHEC is crucial, and understanding the mechanisms of prophage induction and phage development in the human intestine is important to facilitate development of procedures preventing or alleviating Shiga toxin-caused diseases.

Bacteriophages carrying Shiga toxin genes: genomic variations, detection and potential treatment of pathogenic bacteria.

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Differential efficiency of induction of various lambdoid prophages responsible for production of Shiga toxins in response to different induction agents

Bacteriophages carrying Shiga toxin genes: genomic variations, detection and potential treatment of pathogenic bacteria.