Rising to the challenge: accelerated pace of discovery transforms marine virology

Key Points

  • A newly available quantitative metagenomic pipeline for double-stranded DNA (dsDNA) viruses has facilitated the generation of large-scale, systematic data sets with which to explore marine viral ecology at the gene, population and community levels.

  • The use of protein clusters and shared k-mer-based analyses, including social networks, enables examination of gene diversity and viral ecology, despite the dominance of 'unknown' sequences in marine viromes.

  • Viral auxiliary metabolic genes (AMGs) encompass a wide range of metabolic functions, indicating that viruses can substantially augment marine ecosystem function by altering the metabolism of their hosts. These AMGs are also major contributors to niche differentiation in marine viral communities.

  • Viruses that infect dominant and widespread marine microorganisms have been identified using cultivation-dependent and cultivation-independent techniques, which is expanding our understanding of marine viral diversity.

  • Several cultivation-independent techniques are now available to link viruses to their hosts in complex environments, which is facilitating the exploration of virus–host interactions in nature. Notably, viral tagging suggests that wild marine cyanophages comprise discrete populations, facilitating the application of population-based viral ecology for which decades of existing ecological and evolutionary theory can be leveraged.

  • Phage–bacteria infection networks and quantitative host range analyses help to advance the field towards a more predictive understanding of 'who infects whom?'

  • The main challenges and areas for future research in marine virology are outlined.

Abstract

Marine viruses have important roles in microbial mortality, gene transfer, metabolic reprogramming and biogeochemical cycling. In this Review, we discuss recent technological advances in marine virology including the use of near-quantitative, reproducible metagenomics for large-scale investigation of viral communities and the emergence of gene-based viral ecology. We also describe the reprogramming of microbially driven processes by viral metabolic genes, the identification of novel viruses using cultivation-dependent and cultivation-independent tools, and the potential for modelling studies to provide a framework for studying virus–host interactions. These transformative advances have set a rapid pace in exploring and predicting how marine viruses manipulate and respond to their environment.

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Figure 1: Overview of sequence-based approaches to examine viral ecology at the levels of genes, populations and communities.
Figure 2: Identification of 'core' protein clusters in the Pacific Ocean Virome data set can be used to assess niche differentiation among photic and aphotic marine viruses, as well as the vertical flux of viruses from the photic to aphotic zone.
Figure 3: An overview of the new methods that are available for linking viruses and microbial hosts in natural communities.

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Acknowledgements

The authors thank their colleagues R. Amann, M. Breitbart, P. Chisholm, M. Clokie, M. Coleman, A. Culley, J. Fuhrman, S. Giovannoni, S. Hallam, P. Hugenholtz, D. Karl, D. Lindell, V. Rich, F. Rohwer, A. Segall, G. Steward, J. Weitz, M. Young and members of the Tucson Marine Phage Laboratory (TMPL) for years of engaging discussions on viral ecology, and the US Department of Energy Joint Genome Institute Community Sequencing Program for their long-term support of sequence-based viral ecology. This publication and generous opportunities to innovate were funded in part by Gordon and Betty Moore Foundation grants GBMF2631, GBMF3305 and GBMF3790 to M.B.S..

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Glossary

Phytoplankton blooms

Temporally limited increases in phytoplankton abundances, which are often dominated by one phytoplankton species.

Microbial loop

The flow of materials (for example, organic matter and nutrients) and energy within a microbial community, including the recycling of materials by heterotrophic microorganisms.

Viral shunt

Refers to the role of viral lysis in the conversion of living microbial biomass into dissolved organic matter, which can be consumed by heterotrophic microorganisms.

Kill the Winner hypothesis

(KtW hypothesis). This refers to the ability of predators to exert top-down control on the abundance of their hosts. In the context of this Review, the hypothesis refers to the ability of viruses to prevent their microbial hosts from becoming dominant through increased viral-induced mortality of the most proliferative hosts (the 'winners').

Genome fingerprinting

An electrophoresis-based method to quantify the distribution of viruses with varying genome sizes in a sample.

Viromes

The metagenomes of all viruses present in a specific sample.

Iron chloride flocculation

A method to concentrate viruses from aquatic samples by binding viruses to iron flocs that can then be captured by filtration and dissolved to release the viruses.

Tangential flow filtration

A method to concentrate viruses from aquatic samples, in which the sample is passed at pressure across a filter membrane of defined size to retain viruses and remove smaller materials.

Linker amplification

A method to amplify DNA using ligated primers to obtain sufficient quantities of genomic material for downstream applications, such as metagenomic sequencing.

Multiple displacement amplification

A method to amplify DNA using the phi29 polymerase in order to obtain sufficient quantities of genomic material for downstream applications, such as metagenomic sequencing.

Rarefaction curves

Assessment of a community richness metric (for example, the total number of species, populations or protein clusters) versus the number of samples examined.

Contig spectra

The number of contigs (overlapping sequences) per size of contig (the number of sequences in each contig) after assembly of metagenomic sequences.

Aphotic zone

The region of the ocean that is not illuminated by sunlight.

Particle biology

The study of the composition and activity of microbial communities on particulate matter in the ocean.

k-mer

A fragment of a genomic sequence with a specific length 'k' (number of base pairs).

Social network analysis

Quantitative measurement of the relationships between defined groups or samples using network theory.

Oxygen minimum zone

(OMZ). Region of the ocean in which little or no dissolved oxygen is present.

Gene transfer agents

(GTAs). Phage-like entities that package cellular DNA at random and facilitate horizontal gene transfer.

Membrane vesicles

Fluid-filled, membrane-bound sacs containing proteins and other molecules, which are formed by 'pinching off' from the outer membrane of a cell.

Fosmids

Cloning vectors derived from the bacterial F plasmid in which large genomic segments (40 kb) are stably maintained. These are used to identify genes or genomes of interest by end-sequencing or hybridization.

Single amplified genomes

(SAGs). Amplified genomic sequences obtained from a single cell that has been separated from other cells by flow cytometry. These sequences can be mined to identify the presence of viral DNA.

Microfluidic digital PCR

PCR-based amplification of individual genes from organisms that are trapped in microfluidic chambers.

phageFISH

An epifluorescence microscopy-based method to determine the colocalization of viral and host gene markers by fluorescence in situ hybridization (FISH), which enables the visualization of specific types of intracellular and extracellular viruses.

Viral tagging

A flow cytometry method in which fluorescently labelled viruses are used as probes to detect and obtain wild viruses associated with cultivated cells.

Quantitative host range analysis

(qHR analysis). A method for evaluating the magnitude of viral proliferation when individual cultivated virus types encounter individual cultivated microbial hosts in a laboratory setting.

King of the Mountain hypothesis

(KoM hypothesis). This hypothesis describes the influence of increased recombination rates that enable particular microorganisms to dominate a community.

NPZ-type ecosystem models

Numerical models that describe oceanic plankton dynamics using the three state variables of nutrient concentration (often nitrogen), phytoplankton abundance and zooplankton abundance.

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Brum, J., Sullivan, M. Rising to the challenge: accelerated pace of discovery transforms marine virology. Nat Rev Microbiol 13, 147–159 (2015). https://doi.org/10.1038/nrmicro3404

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