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  • Review Article
  • Published:

Virus–host interactions and their roles in coral reef health and disease

Nature Reviews Microbiology volume 15, pages 205–216 (2017)Cite this article

Subjects

Key Points

  • Over the past 15 years, coral reef virology has identified diverse and dynamic viral consortia that are associated with different reef zones and hosts.

  • We hypothesize that viruses of bacteria and eukaryotes dynamically interact with their hosts in the water column and with scleractinian (stony) corals to influence microbial-community dynamics, coral bleaching and disease, and reef biogeochemical cycling.

  • Beyond directly affecting host health and survival, coral reef viruses are hypothesized to indirectly have an effect on reef ecosystem function by triggering the release and movement of nutrients.

  • Anthropogenic drivers of viral production, such as eutrophication and thermal anomalies, can trigger the transfer of nutrients from coral colonies to water column microbial communities and then back to benthic communities, ultimately leading to coral disease and mortality. We call this feedback loop the 'virus-mediated vortex of coral reef decline'.

Abstract

Coral reefs occur in nutrient-poor shallow waters, constitute biodiversity and productivity hotspots, and are threatened by anthropogenic disturbance. This Review provides an introduction to coral reef virology and emphasizes the links between viruses, coral mortality and reef ecosystem decline. We describe the distinctive benthic-associated and water-column- associated viromes that are unique to coral reefs, which have received less attention than viruses in open-ocean systems. We hypothesize that viruses of bacteria and eukaryotes dynamically interact with their hosts in the water column and with scleractinian (stony) corals to influence microbial community dynamics, coral bleaching and disease, and reef biogeochemical cycling. Last, we outline how marine viruses are an integral part of the reef system and suggest that the influence of viruses on reef function is an essential component of these globally important environments.

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Figure 1: Transmission electron microscopy images of several types of coral-associated viruses.
Figure 2: The core coral virome in the benthic compartment of shallow-water tropical coral reefs.
Figure 3: Viruses in the water column of tropical reefs.
Figure 4: Changes in the relative abundance of members of the core coral virome with coral health state.
Figure 5: Overview of the virus-mediated vortex of coral reef decline.

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Acknowledgements

Work in the authors' laboratories was supported by the US National Science Foundation (OCE-0960937 and OCE-1341195 to R.V.T. and OCE-1635913 to R.V.T., A.R.T. and A.M.S.C.) and the Institute for Pacific Coral Reefs (to J.P.P.).

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Authors and Affiliations

  1. Department of Microbiology, Oregon State University, Corvallis, 97331, Oregon, USA

    Rebecca Vega Thurber, Jérôme P. Payet & Andrew R. Thurber

  2. College of Earth, Ocean, and Atmospheric Science, Oregon State University, Corvallis, 97331, Oregon, USA

    Jérôme P. Payet & Andrew R. Thurber

  3. BioSciences Department, Rice University, 6100 Main Street, Houston, 77005, Texas, USA

    Adrienne M. S. Correa

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  1. Rebecca Vega Thurber
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PowerPoint slides

Glossary

Top-down effects

The ecological concept that organismal growth and abundance are primarily regulated by predation (for example, grazing and viral infection) as opposed to resource limitation.

Benthic

Related to the seafloor habitat, including the objects and organisms that are associated within or on it.

Eukaryotic viruses

Viruses that infect eukaryotic organisms.

Microbial communities

Assemblages of populations of interacting microscopic species, potentially including representatives from all three domains (bacteria, archaea and microscopic eukaryotes) that occupy the same space at a particular time.

Symbiodinium

A genus of photosynthetic dinoflagellate algae that lives inside the tissues of corals and other marine hosts and provides them with fixed carbon. When lost en masse from a host, that host individual experiences diminished health and appears white or 'bleached'.

Coral holobiont

A host organism and all of the symbiotic microbial communities and viral consortia that live in and on it.

Coral surface microlayer

(CSM). A thin layer (several millimetres thick) at the interface between a coral colony and the external environment, which is rich in mucus and heavily colonized by bacteria and bacteriophages.

Viral shunt

A process in which viruses release dissolved organic matter and inorganic nutrients through the infection and lysis of microorganisms, making them available to other nearby microorganisms. This reduces energy transfer to higher trophic levels and increases microbial activity and growth through the recycling of key elements.

Cnidarian

Related to a basal animal phylum that contains the stony corals and other closely related taxa that are united by the possession of stinging cells. Examples include soft corals, anemones, hydra and jellies.

Viromes

The ensembles of viruses in specific samples.

Nucleocytoplasmic large DNA viruses

(NCLDVs). A monophyletic group of ten virus families that have a common virion and genomic structure and replicate in the nucleus of their hosts, but their particles form in the host cytoplasm.

Phycodnavirus

One of a family of nucleocytoplasmic large DNA viruses that commonly infects marine phytoplankton and coral holobionts. Phycodnaviruses are also known as phycoviruses.

Megaviruses

A proposed order of monophyletic viruses that is relatively large in terms of physical size and genome length.

Bacterial standing stock

The number of bacterial cells in a region at any one time.

Bacterial turnover

The time it takes for bacterial standing stock to be replaced through production and predation.

Temperate viruses

Viruses that integrate their genome into the chromosome of their host as a prophage and replicate silently along with their host.

Microbialization

The hypothesis that a habitat that experiences various stressors is altered through shifts in carbon to lower (microbial) trophic levels.

Horizontal gene transfer

The movement of genes between or among organisms in the absence of reproduction that occurs through several mechanisms, including phage infection.

Transduction

The transfer of genetic material between bacteria through phage infection.

Viral production

The release of new virus particles following host cell lysis due to viral infection.

Eutrophication

An increase of inorganic or organic nutrients (for example, nitrate, phosphate or sewage) in a habitat that results in negative ecosystem effects.

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Thurber, R., Payet, J., Thurber, A. et al. Virus–host interactions and their roles in coral reef health and disease. Nat Rev Microbiol 15, 205–216 (2017). https://doi.org/10.1038/nrmicro.2016.176

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