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Review
, 4 (1), 4-16

Movers and Shakers: Influence of Bacteriophages in Shaping the Mammalian Gut Microbiota

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Review

Movers and Shakers: Influence of Bacteriophages in Shaping the Mammalian Gut Microbiota

Susan Mills et al. Gut Microbes.

Abstract

The human intestinal microbiota is one of the most densely populated ecosystems on Earth, containing up to 10 ( 13) 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.

Keywords: bacteriophages; community shuffling; gut; induction; microbiota; phages; prophages.

Figures

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Figure 1. Electron micrograph of tailed phages infecting a dividing bacterial cell.
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Figure 2. Electron micrograph images of phage ϕLb338–1 stained with phosphotungstic acid 0.2% (A) and close-up views of Lb338- (B) (reprinted from Gene, Vol. 448, Alemayehu D, Ross RP, O' Sullivan O, Coffey A, Stanton C, Fitzgerald GF, McAuliffe, O., Genome of a virulent bacteriophage Lb338–1 that lyses the probiotic Lactobacillus paracasei cheese strain, 29–39, © 2009, with permission from Elsevier).
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Figure 3. Electron micrographs of intestinal phages (A) Clostridium difficile phage (reprinted from Gene, Vol. 462, Horgan M, O'Sullivan O, Coffey A, Fitzgerald GF, van Sinderen D, McAuliffe O, Ross RP, Genome analysis of the Clostridium difficile phage PhiCD6356, a temperate phage of the Siphoviridae family, 34–43, © 2010, with permission from Elsevier); (B) and (C) Escherichia coli 0157: H7 phages (reprinted from O’ Flynn et al., 2004, © 2004, American Society for Microbiology, Applied and Environmental Microbiology, 70: 3417–3424, DOI: 10.1128/AEM.70.6.3417-3424.2004 and amended with permission from American Society for Microbiology); (D) and (E) Salmonella enterica phages (reprinted from O' Flynn et al., 2006, Journal of Applied Microbiology, Vol. 101, 521–259, John Wiley and Sons, © The Society for Applied Microbiology).
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Figure 4. Model for “community shuffling” hypothesis demonstrating potential consequences of prophage induction among the intestinal microbiota.

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