Selina Våge

A theoretical analysis of how strain-specific viruses can control microbial species diversity.

Significance This work presents the first detailed analysis to the authors’ knowledge of how species-level diversity is a property emerging from competitive and defensive abilities at the organism level in a microbial system where the diversity-generating mechanism is strain-specific viral lysis. The theoretical analysis constitutes a general case treatment of the important special case question of what properties may make SAR11, a subphylum within the Alphaproteobacteria, so dominant in the pelagic environment. The resulting conceptual framework connects differences in the molecular defense mechanism to ecosystem-level properties such as diversity and activity. It also suggests a reinterpretation of the concept of dormancy in aquatic microbial communities. Pelagic prokaryote communities are often dominated by the SAR11 clade. The recent discovery of viruses infecting this clade led to the suggestion that such dominance could not be explained by assuming SAR11 to be a defense specialist and that the explanation therefore should be sought in its competitive abilities. The issue is complicated by the fact that prokaryotes may develop strains differing in their balance between competition and viral defense, a situation not really captured by present idealized models that operate only with virus-controlled “host groups.” We here develop a theoretical framework where abundance within species emerges as the sum over virus-controlled strains and show that high abundance then is likely to occur for species able to use defense mechanisms with a low trade-off between competition and defense, rather than by extreme investment in one strategy or the other. The J-shaped activity–abundance community distribution derived from this analysis explains the high proportion low-active prokaryotes as a consequence of extreme defense as an alternative to explanations based on dormancy or death due to nutrient starvation.

SAR11 viruses and defensive host strains.

arising from Y. Zhao et al. 494, 357–360 (2013)10.1038/nature11921The recent findings of abundant SAR11 viruses by Zhao et al. are intriguing, and add new insight into the on-going discussion of why SAR11 bacteria are highly successful in the pelagic ocean. On the basis of high SAR11 virus abundance, Zhao et al. claim that SAR11 bacteria are competition specialists. Alternatively, we show here how their findings could be consistent with a dominance of defensive SAR11 strains. Considering their high abundance, understanding why SAR11 bacteria are so successful has important implications for the study of the pelagic ecosystem. There is a Reply to this Brief Communication Arising by Giovannoni, S., Temperton, B. & Zhao, Y. Nature 499, http://dx.doi.org/10.1038/nature12388 (2013).

What difference does it make if viruses are strain-, rather than species-specific?

Theoretical work has suggested an important role of lytic viruses in controlling the diversity of their prokaryotic hosts. Yet, providing strong experimental or observational support (or refutation) for this has proven evasive. Such models have usually assumed “host groups” to correspond to the “species” level, typically delimited by 16S rRNA gene sequence data. Recent model developments take into account the resolution of species into strains with differences in their susceptibility to viral attack. With strains as the host groups, the models will have explicit viral control of abundance at strain level, combined with explicit predator or resource control at community level, but the direct viral control at species level then disappears. Abundance of a species therefore emerges as the combination of how many strains, and at what abundance, this species can establish in competition with other species from a seeding community. We here discuss how species diversification and strain diversification may introduce competitors and defenders, respectively, and that the balance between the two may be a factor in the control of species diversity in mature natural communities. These models can also give a dominance of individuals from strains with high cost of resistance; suggesting that the high proportion of “dormant“ cells among pelagic heterotrophic prokaryotes may reflect their need for expensive defense rather than the lack of suitable growth substrates in their environment.

Optimal defense strategies in an idealized microbial food web under trade-off between competition and defense

Trophic mechanisms that can generate biodiversity in food webs include bottom-up (growth rate regulating) and top-down (biomass regulating) factors. The top-down control has traditionally been analyzed using the concepts of “Keystone Predation” (KP) and “Killing-the-Winner” (KtW), predominately occuring in discussions of macro- and micro-biological ecology, respectively. Here we combine the classical diamond-shaped food web structure frequently discussed in KP analyses and the KtW concept by introducing a defense strategist capable of partial defense. A formalized description of a trade-off between the defense-strategists competitive and defensive ability is included. The analysis reveals a complex topology of the steady state solution with strong relationships between food web structure and the combination of trade-off, defense strategy and the systems nutrient content. Among the results is a difference in defense strategies corresponding to maximum biomass, production, or net growth rate of invading individuals. The analysis thus summons awareness that biomass or production, parameters typically measured in field studies to infer success of particular biota, are not directly acted upon by natural selection. Under coexistence with a competition specialist, a balance of competitive and defensive ability of the defense strategist was found to be evolutionarily stable, whereas stronger defense was optimal under increased nutrient levels in the absence of the pure competition specialist. The findings of success of different defense strategies are discussed with respect to SAR11, a highly successful bacterial clade in the pelagic ocean.

Successful strategies in size structured mixotrophic food webs

This study investigates how food web structures in aquatic microbial communities emerge based on different mixotrophic life strategies. Unicellular mixotrophic organisms that combine osmotrophy and primary production with phagotrophy account for significant amounts of primary production and bacterivory in marine environments, yet mixotrophs are still usually absent in large-scale biogeochemical models. We here present for the first time a thorough analysis of a food web model with a finely resolved structure in both cell size and foraging mode, where foraging mode is a strategy ranging from pure osmotrophy to pure phagotrophy. A trade-off for maximum uptake rates of mixotrophs is incorporated. We study how different factors determine the food web structure, here represented by the topology of the distribution of given amounts of total phosphorous over the cell size-foraging mode plane. We find that mixotrophs successfully coexist with foraging specialists (pure osmo- and phagotrophs) for a wide range of conditions, a result consistent with the observed prevalence of mixotrophs in recent oceanographic surveys. Mixotrophy trade-off and size-dependent parameters have a strong effect on the emerging community structure, stressing the importance of foraging mode and size considerations when working with microbial diversity and food web dynamics. The proposed model may be used to develop timely representations of mixotrophic strategies in larger biogeochemical ocean models.

Oceanic protists with different forms of acquired phototrophy display contrasting biogeographies and abundance

This first comprehensive analysis of the global biogeography of marine protistan plankton with acquired phototrophy shows these mixotrophic organisms to be ubiquitous and abundant; however, their biogeography differs markedly between different functional groups. These mixotrophs, lacking a constitutive capacity for photosynthesis (i.e. non-constitutive mixotrophs, NCMs), acquire their phototrophic potential through either integration of prey-plastids or through endosymbiotic associations with photosynthetic microbes. Analysis of field data reveals that 40–60% of plankton traditionally labelled as (non-phototrophic) microzooplankton are actually NCMs, employing acquired phototrophy in addition to phagotrophy. Specialist NCMs acquire chloroplasts or endosymbionts from specific prey, while generalist NCMs obtain chloroplasts from a variety of prey. These contrasting functional types of NCMs exhibit distinct seasonal and spatial global distribution patterns. Mixotrophs reliant on ‘stolen’ chloroplasts, controlled by prey diversity and abundance, dominate in high-biomass areas. Mixotrophs harbouring intact symbionts are present in all waters and dominate particularly in oligotrophic open ocean systems. The contrasting temporal and spatial patterns of distribution of different mixotroph functional types across the oceanic provinces, as revealed in this study, challenges traditional interpretations of marine food web structures. Mixotrophs with acquired phototrophy (NCMs) warrant greater recognition in marine research.

The Response of Heterotrophic Prokaryote and Viral Communities to Labile Organic Carbon Inputs Is Controlled by the Predator Food Chain Structure

Factors controlling the community composition of marine heterotrophic prokaryotes include organic-C, mineral nutrients, predation, and viral lysis. Two mesocosm experiments, performed at an Arctic location and bottom-up manipulated with organic-C, had very different results in community composition for both prokaryotes and viruses. Previously, we showed how a simple mathematical model could reproduce food web level dynamics observed in these mesocosms, demonstrating strong top-down control through the predator chain from copepods via ciliates and heterotrophic nanoflagellates. Here, we use a steady-state analysis to connect ciliate biomass to bacterial carbon demand. This gives a coupling of top-down and bottom-up factors whereby low initial densities of ciliates are associated with mineral nutrient-limited heterotrophic prokaryotes that do not respond to external supply of labile organic-C. In contrast, high initial densities of ciliates give carbon-limited growth and high responsiveness to organic-C. The differences observed in ciliate abundance, and in prokaryote abundance and community composition in the two experiments were in accordance with these predictions. Responsiveness in the viral community followed a pattern similar to that of prokaryotes. Our study provides a unique link between the structure of the predator chain in the microbial food web and viral abundance and diversity.

Fractal Hypothesis of the Pelagic Microbial Ecosystem-Can Simple Ecological Principles Lead to Self-Similar Complexity in the Pelagic Microbial Food Web?

Trophic interactions are highly complex and modern sequencing techniques reveal enormous biodiversity across multiple scales in marine microbial communities. Within the chemically and physically relatively homogeneous pelagic environment, this calls for an explanation beyond spatial and temporal heterogeneity. Based on observations of simple parasite-host and predator-prey interactions occurring at different trophic levels and levels of phylogenetic resolution, we present a theoretical perspective on this enormous biodiversity, discussing in particular self-similar aspects of pelagic microbial food web organization. Fractal methods have been used to describe a variety of natural phenomena, with studies of habitat structures being an application in ecology. In contrast to mathematical fractals where pattern generating rules are readily known, however, identifying mechanisms that lead to natural fractals is not straight-forward. Here we put forward the hypothesis that trophic interactions between pelagic microbes may be organized in a fractal-like manner, with the emergent network resembling the structure of the Sierpinski triangle. We discuss a mechanism that could be underlying the formation of repeated patterns at different trophic levels and discuss how this may help understand characteristic biomass size-spectra that hint at scale-invariant properties of the pelagic environment. If the idea of simple underlying principles leading to a fractal-like organization of the pelagic food web could be formalized, this would extend an ecologists mindset on how biological complexity could be accounted for. It may furthermore benefit ecosystem modeling by facilitating adequate model resolution across multiple scales.

Linking internal and external bacterial community control gives mechanistic framework for pelagic virus-to-bacteria ratios

Summary For more than 25 years, virus‐to‐bacteria ratios (VBR) have been measured and interpreted as indicators of the importance of viruses in aquatic ecosystems, yet a generally accepted theory for understanding mechanisms controlling VBR is still lacking. Assuming that the denominator (total bacterial abundance) is primarily predator controlled, while viral lysis compensates for host growth rates exceeding this grazing loss, the numerator (viral abundance) reflects activity differences between prokaryotic hosts. VBR is then a ratio between mechanisms generating structure within the bacterial community and interactions between different plankton functional types controlling bacterial community size. We here show how these arguments can be formalized by combining a recently published model for co‐evolutionary host‐virus interactions, with a previously published “minimum” model for the microbial food web. The result is a framework where viral lysis links bacterial diversity to microbial food web structure and function, creating relationships between different levels of organization that are strongly modified by organism‐level properties such as cost of resistance.

Quantifying Tradeoffs for Marine Viruses

The effects of viruses on marine microbial communities are myriad. The high biodiversity of viruses and their complex interactions with diverse hosts makes it a challenge to link modeling work with experimental work. In various trophic groups, trait-based approaches have helped to simplify this complexity, as traits describe organism properties in terms of taxon-transcending units, allowing for easier identification of generic, underlying principles. By predicting large-scale biogeography of different plankton functional types based on key sets of traits and their associated tradeoffs, these approaches have made major contributions to our understanding of global biogeochemistry and ecology. This review addresses the question of how a trait-based approach can make contributions toward understanding marine virus ecology. We review and synthesize current knowledge on virus traits with a focus on quantifying the associated tradeoffs. We use three case studies--virulence, host range, and cost of resistance--to illustrate how quantification of tradeoffs can help to explain observed patterns, generate hypotheses, and improve our theoretical understanding of virus ecology. Using a nutrient-susceptible-infected-virus model as a framework, we discuss tradeoffs as a link between model building (theory) and experimental design (practice). Finally, we address how insights from virus ecology can contribute back to the trait-based ecology community.