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Revisiting the rules of life for viruses of microorganisms

Abstract

Viruses that infect microbial hosts have traditionally been studied in laboratory settings with a focus on either obligate lysis or persistent lysogeny. In the environment, these infection archetypes are part of a continuum that spans antagonistic to beneficial modes. In this Review, we advance a framework to accommodate the context-dependent nature of virus–microorganism interactions in ecological communities by synthesizing knowledge from decades of virology research, eco-evolutionary theory and recent technological advances. We discuss that nuanced outcomes, rather than the extremes of the continuum, are particularly likely in natural communities given variability in abiotic factors, the availability of suboptimal hosts and the relevance of multitrophic partnerships. We revisit the ‘rules of life’ in terms of how long-term infections shape the fate of viruses and microbial cells, populations and ecosystems.

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Fig. 1: The viral infection continuum.
Fig. 2: Viral transmission strategies and ecological context.
Fig. 3: Examples of temperate phage–bacterium mutualisms.

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Acknowledgements

Stimulating discussions at a Canadian Institute for Advanced Research–Gordon and Betty Moore Foundation workshop entitled “Continuum of Persistence – Ecology and Function of Persistent Virus Infections” contributed to the initial motivation for and direction of this work. An American Association for the Advancement of Science (AAAS) special session entitled “Viruses, Microbes and Their Entangled Fates” facilitated discussions and ultimately led to this Review, and AAAS is acknowledged for travel support provided to A.M.S.C. Funding that supported this synthesis was provided by the NSF Biological Oceanography Program (OCE#1635798 and OCE#1928609 to A.M.S.C., OCE#1829831 to M.B.S., OCE#1829640 to M.B.S. and OCE#1829636 to J.S.W. and OCE#1737237 to A.B.), an Early-Career Research Fellowship (#2000009651) from the Gulf Research Program of the US National Academies of Sciences to A.M.S.C., the Gordon and Betty Moore Foundation (#3790 to M.B.S.) and the Simons Foundation (SCOPE Award ID 329108 and Award ID 722153 to J.S.W and Award ID 735083 to A.B.).

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A.M.S.C., A.B., M.B.S. and J.S.W. conceptualized the Review. All authors contributed to all aspects of manuscript development, including research, writing and editing.

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Correspondence to Adrienne M. S. Correa or Alison Buchan or Matthew B. Sullivan or Joshua S. Weitz.

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Glossary

Viral shunt

Prevention of dissolved and particulate carbon from being incorporated into consumers at higher trophic levels due to the release of this carbon from infected host cells via viral lysis.

Lytic infections

Infections involving the reproduction of viral genetic material, packing of viral genetic material into capsids and release of virus particles into the environment following the lysis (that is, rupture) and death of the host cell.

Bacteriophages (or phages)

Viruses that exclusively infect bacterial cells.

Lysogenic infections

A viral infection state in which the viral genome is integrated into that of the host cellular genome and can be replicated during division without lysing the cell.

Chronic infections

Infections in which viral progeny are released from the host cell into the environment but lysis and death of that infected cell do not necessarily occur.

Inefficient lytic infections

Infections by a virulent virus that may be stalled or terminated at one or multiple stages of the infection cycle, from adsorption to the host cell through to cell lysis.

Latent infection

A state of reduced lytic activity, which includes lysogeny (that is, the viral genome is integrated into the host genome), chronic infection and other infection states (including otherwise lytic viruses that infect hosts during non-optimal conditions).

Temperate phages

Viruses that can establish a lytic cycle or a lysogenic cycle.

Prophage

An integrated genome of a temperate phage inside a lysogen.

Cellular multiplicity of infection

The discrete number of viruses that have infected a given cell. ‘Cellular multiplicity of infection’ is distinct from the commonly used term ‘multiplicity of infection’ (that is, the population-level ratio of the number of virus particles to the number of cells).

Adsorption

Viral attachment to a host cell.

Lysogens

Cells with a prophage, which is either integrated into the cellular genome or is extrachromosomal.

Virocell

A cell infected by a virus that reshapes cellular physiology so that it is controlled by viral genetic programmes.

Heteroimmunity

Denoting when two phages have heterotypic (unrelated) genetic elements (that is, repressor and cognate operator) to control the lytic cycle and, as a consequence, neither prophage is able to prevent infection of the host by the other virus.

Superinfection

Viral infection of a cell harbouring another virus.

Cytoplasmic incompatibility

Caused by maternally inherited bacteria, a situation in which factors in the cytoplasm of two gametes are not compatible, preventing the formation of viable offspring.

Co-infection

The simultaneous infection of a cell by more than one virus; the viruses need not be closely related.

Homoimmunity

Denoting when a prophage confers immunity against infection by similar viruses because both the resident prophage and the incoming virus contain homotypic (identical or nearly identical) genetic elements (that is, repressor and cognate operator) to control the lytic cycle.

Carrier states

Cells that are considered to have a chronic infection.

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Correa, A.M.S., Howard-Varona, C., Coy, S.R. et al. Revisiting the rules of life for viruses of microorganisms. Nat Rev Microbiol 19, 501–513 (2021). https://doi.org/10.1038/s41579-021-00530-x

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