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Pelagic microbial food web organization: Extending the theory for structure and diversity generating mechanisms based on life strategy trade-offs

Pelagic microbial food web organization: Extending the theory for structure and diversity generating mechanisms based on life strategy trade-offs
Selina Våge

2014

Department of Biology, University of Bergen, 5007 Bergen, NORWAY.

ABSTRACT

This dissertation explores food web interactions controlling structure and biodiversity in the pelagic microbial community. Through a theoretical approach, mathematical models of simplified microbial food webs are used to investigate when particular microbial life strategies are successful in the pelagic ocean, to what extent the success is dependent on life-strategy trade-offs, and how different life strategies influence the biogeochemical functioning of the marine ecosystem. Trade-offs between competition, defense, predation and different foraging modes are found to strongly influence the structure and functioning of the microbial community.

A steady-state 3-population model with a predator, a competition specialist and a defense specialist partially defended against the predator is analyzed with respect to defense strategy and trade-off between competition and defense (Paper I). The food web structure is found to intricately depend on the functional shape of this trade-off, the investment of the defense specialist into defense and the system's nutrient content. High defense results in high biomass of the defense strategist, whereas low defense increases production, and strategies corresponding to maximum biomass or production are generally different from evolutionary stable strategies. Through its diamond-shaped food-web structure, this study links the 'Killing-the-Winner' concept known in microbial ecology to the classical macroecological principle of 'Keystone Predation'.

Using a dynamic model with high resolution in foraging mode and cell size, food web structures are investigated as emergent features of basic ecological interactions such as size-selective predation, allometric uptake kinetics and trade-offs between different nutritional modes (Paper II). Mixotrophy (a combination between osmotrophic and phagotrophic foraging) is found to be a successful strategy under different environmental conditions, even at high costs relative to specialized foraging (pure osmotrophy and pure phagotrophy). Furthermore, the emergent food web structure is found to be highly sensitive to size-dependent model parameters.

Coexistence and diversity within the prokaryote community are analyzed at steady state in a virus-host community model (Paper III). A trade-off between competitive and defensive abilities in hosts is found to potentially explain inverse rank abundance curves of host groups and their associated viruses in the pelagic ocean. Cost of resistance (COR) and viral control of fast growing competition specialists is proposed as an explanation for the dominance of slow growing bacteria in the oligotrophic ocean, rather than dormancy due to a lack of resources. Paper IV extends the ongoing discussion of why the abundant bacterial clade SAR11 may be so successful in the pelagic ocean. When interpreting host groups in the virus-host community model of Paper III as strains of different species, the model provides an alternative and counterintuitive explanation for high viral abundances in connection with host populations that may be dominated by defense specialists.

Paper V takes this discussion one step further and resolves host groups at the level of species and strains of species. In an idealized host-virus arms race model, control of prokaryote abundance and diversity is analyzed under the influence of lytic viruses in a chemostat environment. A COR for host strains as well as potential reductions of viral abilities to infect ancient strains is incorporated. Competitive traits of the strains are found to determine the number of strains each species can establish, whereas defensive traits of the strains determine the number of individuals in each strain. High numerical abundance at the species level, such as obtained by SAR11, thus seems dependent on a successful combination of competitive and defensive skills on the strain level.

The dissertation and papers therein extend our conceptual understanding of how ecological trade-offs are fundamental in structuring the pelagic microbial community across different levels, and encourage experimental studies to quantify and gain a mechanistic understanding of these trade-offs. The presence of a generic mechanism allowing coexistence of competition and defense specialists at different trophic levels motivates the formulation of a fractal hypothesis of the pelagic food web, where trade-offs acting repeatedly at different trophic levels may give rise to a self-similar organization of the pelagic microbial food web.