Metabolic and biogeochemical consequences of viral infection in aquatic ecosystems

Abstract

Ecosystems are controlled by ‘bottom-up’ (resources) and ‘top-down’ (predation) forces. Viral infection is now recognized as a ubiquitous top-down control of microbial growth across ecosystems but, at the same time, cell death by viral predation influences, and is influenced by, resource availability. In this Review, we discuss recent advances in understanding the biogeochemical impact of viruses, focusing on how metabolic reprogramming of host cells during lytic viral infection alters the flow of energy and nutrients in aquatic ecosystems. Our synthesis revealed several emerging themes. First, viral infection transforms host metabolism, in part through virus-encoded metabolic genes; the functions performed by these genes appear to alleviate energetic and biosynthetic bottlenecks to viral production. Second, viral infection depends on the physiological state of the host cell and on environmental conditions, which are challenging to replicate in the laboratory. Last, metabolic reprogramming of infected cells and viral lysis alter nutrient cycling and carbon export in the oceans, although the net impacts remain uncertain. This Review highlights the need for understanding viral infection dynamics in realistic physiological and environmental contexts to better predict their biogeochemical consequences.

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Fig. 1: Remodelling of host metabolic pathways during viral infection.
Fig. 2: Relationships between viral productivity and host physiology or environment.
Fig. 3: The role of viruses in marine carbon and nutrient cycling.

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Acknowledgements

This work was supported by the Gordon & Betty Moore Foundation Marine Microbiology Initiative (Award 3305). Additional support was provided by the National Science Foundation Division of Ocean Sciences (NSF-OCE) (Awards 1536989 and 1829831 to M.B.S.), the Simons Foundation (Awards 32910 to S.J. and 402971 to J.R.W.) and the Gordon & Betty Moore Foundation (Awards 3788 to A.Z.W. and 3790 to M.B.S.).

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Glossary

Transparent exopolymer particle

(TEP). A sticky, gel-like particle consisting predominantly of acidic polysaccharides that originate from microorganisms and can enhance the aggregation of non-sticky particles in marine and aquatic ecosystems.

Core reaction centre

A membrane complex of several proteins, pigments and other cofactors that performs the principal energy conversion reactions of photosynthesis, capturing light energy and converting it into redox potential energy for ATP synthesis and reducing power for reduction of CO2; also known as the photosynthetic reaction centre.

Phycobilin

Photosynthetic pigments found in cyanobacteria and the chloroplasts of red algae and glaucophytes that aid in absorption of light energy, particularly at wavelengths that are not well absorbed by chlorophylls or carotenoids.

Euphotic zone

The uppermost layer of water in a lake or ocean characterized by enough sunlight to support photosynthetic carbon fixation.

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Zimmerman, A.E., Howard-Varona, C., Needham, D.M. et al. Metabolic and biogeochemical consequences of viral infection in aquatic ecosystems. Nat Rev Microbiol 18, 21–34 (2020). https://doi.org/10.1038/s41579-019-0270-x

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