Host-virus-predator coexistence in a grey-box model with dynamic optimization of host fitness.

Lytic viruses are believed to affect both flow patterns and host diversity in microbial food webs. Models resolving host and virus communities into subgroups can represent both aspects. However, when flow pattern is the prime interest, such models may seem unnecessary complex. This has led to proposals of black-box models using only total community sizes as state variables. This simplification creates a coexistence problem, however, since predator and virus communities then compete for the same, shared, prey = host community. Mathematically, this problem can be solved by introducing feedbacks allowing community-level properties to adapt. The different mathematical alternatives for such feedback represent different ecological assumptions and thus different hypotheses for how the balance between predators and viruses is controlled in nature. We here explore a model where the feedback works through an increase in host community resistance in response to high virus abundances, thereby reducing virus production. We use a dynamic "strategy" index S to describe the balance between defensive and competitive abilities in the host community, and assume the rate of change in S to be proportional to the local slope of the per capita fitness gradient for the host. We explore how such a "grey-box" model can allow stable coexistence of viruses and predators, and how equilibrium food web structure, virus-to-host ratio, and partitioning of host production varies; both as functions of host community traits, and as functions of external bottom-up and top-down drivers.

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.

Effects of differences in organic supply on bacterial diversity subject to viral lysis.

Bacterial diversity is believed to be controlled both by bottom-up and top-down mechanisms such as nutrient competition, predation and viral lysis. We hypothesise that lytic viruses create trophic niches within bacterial communities, and thus primarily control richness and evenness, while substrate composition primarily controls community composition, that is, the inhabitants of these niches. To investigate this, we studied diversity of mixed bacterial communities subject to viruses under different regimes of organic matter supply. From a predator-free inoculum, bacterial communities were allowed to develop in batch cultures where the organic substrate was either a single compound [glucose (G)] or more complex mixtures produced by phytoplankton [Phaeocystis pouchetii (P) or Thalassiosira sp. (T)]. Throughout the experiment, c. 98% of the sequences in treatment G belonged to the Gammaproteobacteria class, which dominated also in the initial phase of the other treatments [T (c. 87%) and P (62%)]. In treatment T, the composition shifted to a dominance of Alphaproteobacteria (c. 37%), while in P, the proportion of Gammaproteobacteria remained stable. Richness increased with increasing substrate complexity, while evenness remained similar in the different treatments. The results suggest that both substrate composition (bottom-up) and viral lysis (top-down) operate simultaneously in the control of bacterial diversity. Despite the reduction in factors supposed to influence prokaryote diversity, the system was still complex if taken into account the potential synergistic interactions within and between the remaining factors.

Viral and microbial community dynamics in four aquatic environments.

The species composition and metabolic potential of microbial and viral communities are predictable and stable for most ecosystems. This apparent stability contradicts theoretical models as well as the viral-microbial dynamics observed in simple ecosystems, both of which show Kill-the-Winner behavior causing cycling of the dominant taxa. Microbial and viral metagenomes were obtained from four human-controlled aquatic environments at various time points separated by one day to >1 year. These environments were maintained within narrow geochemical bounds and had characteristic species composition and metabolic potentials at all time points. However, underlying this stability were rapid changes at the fine-grained level of viral genotypes and microbial strains. These results suggest a model wherein functionally redundant microbial and viral taxa are cycling at the level of viral genotypes and virus-sensitive microbial strains. Microbial taxa, viral taxa, and metabolic function persist over time in stable ecosystems and both communities fluctuate in a Kill-the-Winner manner at the level of viral genotypes and microbial strains.

Prokaryotic diversity--magnitude, dynamics, and controlling factors.

There are probably millions of species in the microorganismal domains Bacteria and Archaea (the prokaryotes), and we are only just beginning to work out the basic principles governing their distribution and abundance in natural environments. One characteristic that has become clear is that prokaryote diversity in aquatic environments is orders of magnitude less than in sediments and soils. Hypotheses and models explaining such differences are under development and are beginning to offer promising insights into the mechanisms governing prokaryote diversity and ecosystem function.