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Interactions between bacterial and phage communities in natural environments

Abstract

We commonly acknowledge that bacterial viruses (phages) shape the composition and evolution of bacterial communities in nature and therefore have important roles in ecosystem functioning. This view stems from studies in the 1990s to the first decade of the twenty-first century that revealed high viral abundance, high viral diversity and virus-induced microbial death in aquatic ecosystems as well as an association between collapses in bacterial density and peaks in phage abundance. The recent surge in metagenomic analyses has provided deeper insight into the abundance, genomic diversity and spatio-temporal dynamics of phages in a wide variety of ecosystems, ranging from deep oceans to soil and the mammalian digestive tract. However, the causes and consequences of variations in phage community compositions remain poorly understood. In this Review, we explore current knowledge of the composition and evolution of phage communities, as well as their roles in controlling the population and evolutionary dynamics of bacterial communities. We discuss the need for greater ecological realism in laboratory studies to capture the complexity of microbial communities that thrive in natural environments.

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Fig. 1: Canonical phage infection cycles.
Fig. 2: Consequences of co-infection for phage epidemiology and evolution.
Fig. 3: Phage-mediated evolution of bacterial communities.
Fig. 4: Short-term and long-term consequences of phage–bacterium coevolution.

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Acknowledgements

A.C. has received funding from the European Union’s Horizon 2020 research and innovation programme under the Marie Skłodowska-Curie Actions (grant agreement no. 834052, anti-CRISPR). E.R.W. has received funding from the European Research Council (ERC-STG-2016-714478 — EVOIMMECH), the Leverhulme Trust (RPG-2018-380) and the UK Natural Environment Research Council (NE/M018350/1 and NE/S001921/1). S.v.H. has received funding from the UK Biotechnology and Biological Sciences Research Council (BB/S017674/1 and BB/R010781/10).

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A.C. and B.J.P. researched data for the article. A.C. and E.R.W. substantially contributed to discussion of the content. A.C. and B.J.P wrote the manuscript. E.R.W and S.V.H. reviewed and edited the manuscript before submission.

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Correspondence to Anne Chevallereau or Edze R. Westra.

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Nature Reviews Microbiology thanks B. Koskella and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

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Glossary

Mosaicism

The description of a phage genome as composed of gene blocks similar to other phage genomes and flanked by dissimilar sequences. This mosaic genome architecture is due to horizontal transfer of genetic material.

Lysogenic conversion

Phenotypic changes that result from the acquisition and expression of prophage-encoded genes.

Transduction

Transfer of bacterial DNA from one bacterium to another, mediated through phage infection.

Viral dark matter

A viral species (or genome) that has not yet been characterized but for which the existence has been revealed by environmental metagenomic sequencing. More restrictively, viral dark matter can also refer to phage genes that have no assigned functions.

Prophage

Latent form of a phage in which lytic functions are repressed and that is often integrated into the host chromosome.

Lysogeny

Phenomenon where a temperate phage parasitizes a host bacterium (hence called a ‘lysogen’), often by integrating its genetic material into the host DNA, but without producing phage particles or triggering host lysis.

Satellite phages

Phages that lack the ability to replicate autonomously and require the products of infection generated by a helper phage (for example, capsid proteins).

Superinfection

Infection of a host that already accommodates a phage from an earlier infection, which can be engaged either in a lytic or in a lysogenic cycle and integrated as a prophage.

Copiotroph species

Fast-growing organisms found in nutrient-rich environments.

Homoimmunity

Mechanism by which a prophage inhibits the secondary infection of its host by a closely related phage.

Viromes

Ensembles of viral genomes found in an organism or within a given environment.

Temperate phages

Phages that replicate either through a lytic cycle or through a lysogenic cycle.

Virulent phages

Phages that replicate exclusively through a lytic cycle, which ultimately triggers the death of the host cell, releasing new phage particles.

Phageome

Phage fraction of the virome. Phages are generally the main constituents of viromes.

Host range

The range of genetically distinct bacteria in which a phage can replicate. Usually, phages that infect a single or a few genetically close strains are referred to as ‘specialists’, whereas phages that infect many strains of the same species, or even multiple different species or genera, are called ‘generalists’.

Co-infection

Infection where two phages are simultaneously present within the same host cell. This definition therefore widely includes phenomena such as superinfection or polylysogeny.

Lysis inhibition

Delay of the lysis of an infecting phage (this extension of phage latent period results in an increased burst size) induced by secondary adsorptions of additional phages.

Auxiliary metabolic genes

(AMGs). Phage-encoded genes that originate from bacterial cells and can modulate host cell metabolism, likely resulting in improved phage replication.

Virocells

Refers to a concept stating that the reproductive, living form of a virus is the infected cell (called virocell) as opposed to its dissemination form, the virion.

Phase variation

Switch of gene expression from an ‘on’ phase to an ‘off’ phase, generally caused by the introduction of a mutation into a hypermutable DNA region. A secondary mutation in the same region can reactivate gene expression, rendering this phenomenon reversible. Phase variation generates phenotypic diversity in bacterial populations.

Phage-inducible chromosomal islands

Class of mobile genetic elements that specifically exploit (and interfere with) temperate phages for their horizontal transfer.

Fluctuating selection dynamics

Type of phage–bacterium coevolutionary dynamics where phage and host genotype frequencies oscillate over time because of negative frequency-dependent selection.

Arms race dynamics

Type of phage–bacterium coevolutionary dynamics where phage infectivity and host resistance generally increase over time.

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Chevallereau, A., Pons, B.J., van Houte, S. et al. Interactions between bacterial and phage communities in natural environments. Nat Rev Microbiol (2021). https://doi.org/10.1038/s41579-021-00602-y

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