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Review
.2020 Sep 10:10:481.
doi: 10.3389/fcimb.2020.00481. eCollection 2020.

Shining Light on Human Gut Bacteriophages

Affiliations
Review

Shining Light on Human Gut Bacteriophages

Emma Guerin et al. Front Cell Infect Microbiol..

Abstract

The human gut is a complex environment that contains a multitude of microorganisms that are collectively termed the microbiome. Multiple factors have a role to play in driving the composition of human gut bacterial communities either toward homeostasis or the instability that is associated with many disease states. One of the most important forces are likely to be bacteriophages, bacteria-infecting viruses that constitute by far the largest portion of the human gut virome. Despite this, bacteriophages (phages) are the one of the least studied residents of the gut. This is largely due to the challenges associated with studying these difficult to culture entities. Modern high throughput sequencing technologies have played an important role in improving our understanding of the human gut phageome but much of the generated sequencing data remains uncharacterised. Overcoming this requires database-independent bioinformatic pipelines and even those phages that are successfully characterized only provide limited insight into their associated biological properties, and thus most viral sequences have been characterized as "viral dark matter." Fundamental to understanding the role of phages in shaping the human gut microbiome, and in turn perhaps influencing human health, is how they interact with their bacterial hosts. An essential aspect is the isolation of novel phage-bacteria host pairs by direct isolation through various screening methods, which can transformin silico phages into a biological reality. However, this is also beset with multiple challenges including culturing difficulties and the use of traditional methods, such as plaquing, which may bias which phage-host pairs that can be successfully isolated. Phage-bacteria interactions may be influenced by many aspects of complex human gut biology which can be difficult to reproduce under laboratory conditions. Here we discuss some of the main findings associated with the human gut phageome to date including composition, our understanding of phage-host interactions, particularly the observed persistence of virulent phages and their hosts, as well as factors that may influence these highly intricate relationships. We also discuss current methodologies and bottlenecks hindering progression in this field and identify potential steps that may be useful in overcoming these hurdles.

Keywords: bacteriophage; gut microbiota; microbiome; phage-bacteria interactions; virome.

Copyright © 2020 Guerin and Hill.

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Figures

Figure 1
Figure 1
Overview of bacteriophage lifecycles.(A) Lytic phages hijack host cell machinery to replicate, assemble and produce progeny which are released from the cytoplasm on host cell lysis to initiation further rounds of infection. This phage lifecycle is thought to be the most prevalent in the healthy human gut.(B) Lysogenic phages integrate their genome into the bacterial host genome with which they passively replicate until stress signals trigger their induction and switch to the lytic cycle.(C) Phages that follow a pseudolysogenic lifecycle also passively replicate with the host, but their genome remains independent from that of the host and is maintained in the cytoplasm as an episome.(D) When phages are in a carrier state they can remain attached to the surface of a non-permissive host without infection.(E) During a chronic infection phages produce progeny similarly to that of lytic phages but without host cell lysis.
Figure 2
Figure 2
An overview of factors that influence phage-bacteria interactions in the human gut.(A) To overcome phage predation, bacteria possess an arsenal of defense mechanisms that target one or more stages of phage infection cycles. In retaliation phages have evolved an array of counter-defense mechanisms. This results in a cycle of infection, resistance and counter-resistance that leads to evolution and diversity in the human gut.(B) In the gastrointestinal tract there is significant variation in biotic and abiotic factors both longitudinally and radially. This results in sectional variation in bacterial composition and spatial heterogeneity between phages and their hosts. Anatomical features of the gut such as mucus, crypts and villi create bacterial microhabitats which are inaccessible to phages allowing them to escape predation, gradually seed the lumen and maintain homeostasis.(C) Biotic and abiotic factors can also influence the metabolic state of the bacterial host. This may result in transient phenotypic changes mediated by mechanisms such as phase variation allowing adaptation to stress which includes phage infection. These phenotypic changes may inhibit phage infection and can create isogenic populations consisting of phage permissive and non-permissive host variants allowing the co-existence of phage and bacteria.
Figure 3
Figure 3
A generic overview of key experimental steps important in studying the human gut phageome: from metagenomics, database-independent whole virome analyses,in silico identification of novel phages to isolation and characterization. Linking bioinformatics and lab-based research provides important insights into phageome composition, aids novel phage isolation and characterization of biological properties including interactions with the bacterial and mammalian host.
Figure 4
Figure 4
The crAss-like phage family timeline: fromin silico discovery to anin vitro reality (2014-2020).
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