Microbial oceanography

Viral strategies at sea

The finding that marine environments with high levels of host microbes have fewer viruses per host than when host abundance is low challenges a theory on the relative roles of lysogenic and lytic viral-survival strategies. See Article p.466

Lysogeny is the process by which viral DNA is incorporated into the genome of the host organism, and it has long been thought that this ensures virus survival through periods of low host abundance. In this issue, Knowles et al.1 (page 466) use viral and bacterial host-abundance and genomic data to suggest the opposite: that lysogeny is associated with high host abundances. The authors call this a 'piggyback-the-winner' strategy, as opposed to the conventional view, which they paraphrase as 'piggyback-the-loser'.

It is more than 25 years since the realization2,3 that viruses are such abundant players in aquatic and other ecosystems that they are probably the most numerous biological entities on Earth4 (Fig. 1). Over this time, virus ecology has grown into a key discipline of microbial ecology, opening our eyes to an amazingly diverse component of natural ecosystems4,5. Yet despite vast progress in the description of host–virus biomes, our understanding of the connections between host–virus systems and the ecosystems in which they are embedded remains vague.

Figure 1: Marine microbes and their viruses.
figure1

Gunnar Bratbak

This fluorescence-microscopy image of marine microorganisms shows bacteria (oval or rod-shaped green bodies) and viruses (small dots) surrounding a diatom algal cell (red and yellow). Aquatic environments typically have a ratio between free virus and potential hosts of around 10 to 1. Invisible with this technique are lysogenic viruses, whose viral DNA is incorporated into the host genome. Knowles et al.1 present data that challenge conventional ideas of when and why lysogeny occurs in nature. (Scale bar, 20 micrometres.)

The host–virus systems we observe today can be seen as the products of antagonistic arms races, in which both hosts and viruses have evolved strategies to ensure their survival and propagation not only during resource-rich periods of rapid growth, but also in leaner times. Like all specialized predators and parasites, virus lineages face the evolutionary dilemma that too much success is a potential disaster: an organism that drives its prey or hosts to extinction does not survive. This could be a particular challenge in variable environments in which 'too efficient' is a condition that changes continuously.

Phages — viruses that infect bacterial hosts — have developed two main life strategies, lysis and lysogeny. Lytic phages (also known as virulent phages) reproduce in their hosts to produce progeny that are released as the host cell bursts (lyses). Maintaining a population of lytic viruses requires that, on average, at least one of the viruses released in a lytic event finds and successfully infects a new host before the virus itself is inactivated. This requirement is obviously problematic if hosts become rare. Lysogenic phages (also known as temperate phages) incorporate their DNA into the host's genome, such that their DNA is copied together with that of the host cell as the cell grows and multiplies. Generations later, the phage DNA may reactivate to produce progeny viruses. Lysogeny has typically been argued to ensure not only that the phages survive without killing their hosts when hosts are few, but also that they are in the same place as the hosts when growth conditions improve. These arguments lead to an expectation of increased importance of lysogeny in oligotrophic (nutrient-poor) environments, as confirmed by some investigations6.

The ecological consequences of the lytic and lysogenic strategies are different. By causing host-cell lysis, lytic viruses shunt energy and material out of the food chain, whereas lysogenic viruses have the potential to move genes between hosts in a process called transduction. The balance between lysis and lysogeny, and the environmental conditions that influence this balance, are therefore thought to have major consequences for how marine ecosystems work.

Knowles et al. present data that challenge the established view that low host abundance is a primary driver for a shift from lytic to lysogenic behaviour. When host abundance is high, the probability of a host–virus collision increases and one might expect an increasing role for lytic viruses, reflected in an increasing virus-to-microbe ratio. However, both in their own data from coral reefs and in a meta-analysis from a broad set of environments, Knowles et al. find the opposite: the ratio between virus and microbe abundance tends to decrease at high microbe abundances. They hypothesize that this is caused by an increasing tendency towards lysogeny at high host abundance.

However, other situations might produce a similar decreasing trend in the virus-to-microbe ratio. One example is a model7 in which high-abundance-host communities are dominated by slow-growing, defensive host strains with low associated virus production, and in which viruses primarily attack more-competitive, fast-growing strains. The two models are not mutually exclusive, but Knowles and colleagues use metagenomic data (the combined genomes of an ecological community) to show that a set of DNA sequences associated with defence against viruses shows no correlation with microbial abundance, which argues against the defence hypothesis. By contrast, genes associated with the integration and excision of lysogenic viruses increase, supporting the authors' lysogeny hypothesis.

The metagenomic data sets now available8 suggest that the gap between observed microbial diversity in the ocean and what we can explain theoretically is probably even larger than was recognized when this discrepancy was first pointed out more than 50 years ago9. Biodiversity theory thus remains one of the major challenges in marine microbial ecology. Viral lysis is thought to generate and maintain parts of host diversity7, whereas lysogenic viruses could, theoretically, exist independently of diversity in the host community. Lytic and lysogenic viral strategies sit at the hub of a story that connects microbial diversity, activity, evolution and ecosystem function, yet the story is unfinished. Although lysogeny has so far played a modest part as a survival strategy, Knowles and colleagues' work suggests a more central role for this process in dynamic ecosystems. If confirmed by future work, this implies a reshuffling of key pieces of the puzzle that would have consequences for our understanding of the role of host–virus biology in structuring the microbial part of ocean ecosystems.

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Correspondence to T. Frede Thingstad.

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Thingstad, T., Bratbak, G. Viral strategies at sea. Nature 531, 454–455 (2016). https://doi.org/10.1038/nature17303

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