T. Frede Thingstad

Explaining microbial population genomics through phage predation

The remarkable differences that have been detected by metagenomics in the genomes of strains of the same bacterial species are difficult to reconcile with the widely accepted paradigm that periodic selection within bacterial populations will regularly purge genomic diversity by clonal replacement. We have found that many of the genes that differ between strains affect regions that are potential phage recognition targets. We therefore propose the constant-diversity dynamics model, in which the diversity of prokaryotic populations is preserved by phage predation. We provide supporting evidence for this model from metagenomics, mathematical analysis and computer simulations. Periodic selection and phage predation dynamics are not mutually exclusive; we compare their predictions to shed light on the ecological circumstances under which each type of dynamics could predominate.

Trade-Offs between Competition and Defense Specialists among Unicellular Planktonic Organisms: the “Killing the Winner” Hypothesis Revisited

SUMMARY A trade-off between strategies maximizing growth and minimizing losses appears to be a fundamental property of evolving biological entities existing in environments with limited resources. In the special case of unicellular planktonic organisms, the theoretical framework describing the trade-offs between competition and defense specialists is known as the “killing the winner” hypothesis (KtW). KtW describes how the availability of resources and the actions of predators (e.g., heterotrophic flagellates) and parasites (e.g., viruses) determine the composition and biogeochemical impact of such organisms. We extend KtW conceptually by introducing size- or shape-selective grazing of protozoans on prokaryotes into an idealized food web composed of prokaryotes, lytic viruses infecting prokaryotes, and protozoans. This results in a hierarchy analogous to a Russian doll, where KtW principles are at work on a lower level due to selective viral infection and on an upper level due to size- or shape-selective grazing by protozoans. Additionally, we critically discuss predictions and limitations of KtW in light of the recent literature, with particular focus on typically neglected aspects of KtW. Many aspects of KtW have been corroborated by in situ and experimental studies of isolates and natural communities. However, a thorough test of KtW is still hampered by current methodological limitations. In particular, the quantification of nutrient uptake rates of the competing prokaryotic populations and virus population-specific adsorption and decay rates appears to be the most daunting challenge for the years to come.

Global-scale processes with a nanoscale drive: the role of marine viruses

Viruses, the smallest and most numerous of all biotic agents, represent the planets largest pool of genetic diversity. The sheer abundance of oceanic viruses results in ~1029 viral infections per day, causing the release of 108–109 tonnes of carbon per day from the biological pool (Suttle, 2007). Still, how and to what extent virus-mediated nanoscale processes are linked to global-scale biodiversity and biogeochemistry is poorly defined.

Conceptual models for the biogeochemical role of the photic zone microbial food web, with particular reference to the Mediterranean Sea

Abstract Observations are reviewed which indicate that not only phytoplankton, but also heterotrophic bacteria are P-limited during those seasons when there is stratification in the Mediterranean. It is discussed how these observations fit into a general concept of a size-structured food chain where the structure is a result of combined top-down control from size-selective predators and size-dependent competition for phosphate. It is argued that, conceptually, labile DOC and silicate have symmetrical roles in potentially controlling the flux of P through the ‘microbial’ and ‘classical’ sides, respectively, of this food web. The resulting concept provides a model linking C, P, and Si fluxes to the size spectrum of biogenic particles in the photic zone.

Impact of changing ice cover on pelagic productivity and food web structure in Disko Bay, West Greenland: a dynamic model approach

Abstract A rise in global temperatures could potentially lead to less ice in the Arctic, including a reduction in the ice-covered period. The consequence of a changing ice cover on the food web structure and production in Disko Bay, Western Greenland, is analysed through application of a dynamical model for the planktonic food web. The model is successfully calibrated and tested for sensitivity, using a detailed data set for 1996–1997. Model scenarios are (1) extended ice cover and (2) no ice. These scenarios are compared to model runs with measured ice cover in two normal years. In the extended ice scenario, assuming unchanged copepod behaviour, copepods are starving or feeding in the ice/water interface from the time they ascend to the surface layer from over-wintering depths until the ice break-up in June. The total annual primary production reaches the same level as it does in the average year, but copepod ingestion and, as a consequence, vertical carbon export is reduced by app. 40%. In the ice-free situation, an early diatom bloom is initiated by stratification of the water in March, before the copepods ascend. The diatom bloom is grazed upon by protozooplankton, which reach a high biomass before the copepods ascend in April. Annual primary production increases by 52% while copepod ingestion and vertical loss of carbon is reduced by 57%. This study illustrates how a change in the ice cover in Arctic areas can potentially create a mismatch between spring primary production and copepod grazers. The result may be a planktonic food web dominated by protozooplankton, resulting in lower export of organic material out of the photic zone despite increased primary productivity, or alternatively lead to changes in species composition or behaviour.

A theoretical approach to structuring mechanisms in the pelagic food web

In the literature there is a commonly used idealized concept of the foodweb structure in the pelagic photic zone food web, based to a large extenton size dependent relationships. An outline is here given of how theelementary size-related physical laws of diffusion and sinking, combinedwith the assumption of predators being size selective in their choice ofprey, give a theoretical foundation for this type of structure. It is shownhow such a theoretical fundament makes it possible to relate a broad specterof phenomena within one generic and consistent framework. Phenomena such asHutchinson‘s and Goldman‘s paradoxes, the influence of nutrients and watercolumn stability on the balance between microbial and classical food webs,bacterial carbon consumption, new production and export of DOC and POC tothe aphotic zone, eutrophication and diversity, can all be approached fromthis perspective. By including host-specific viruses, this approach gives ahierarchical structure to the control of diversity with nutrient contentcontrolling the maximum size of the photic zone community, size selectivityof predators regulating how the nutrient is distributed between size-groupsof osmotrophic and phagotrophic organisms, and viral host specificityregulating how the nutrients within a size group is distributed between hostgroups. I also briefly discuss how some biological strategies may besuccessful by not conforming to the normal rules of such a framework.Analyzing the behavior of these idealized systems is thus claimed tofacilitate our understanding of the behavior of complex natural food webs.In the literature there is a commonly used idealized concept of the foodweb structure in the pelagic photic zone food web, based to a large extenton size dependent relationships. An outline is here given of how theelementary size-related physical laws of diffusion and sinking, combinedwith the assumption of predators being size selective in their choice ofprey, give a theoretical foundation for this type of structure. It is shownhow such a theoretical fundament makes it possible to relate a broad specterof phenomena within one generic and consistent framework. Phenomena such asHutchinson‘s and Goldman‘s paradoxes, the influence of nutrients and watercolumn stability on the balance between microbial and classical food webs,bacterial carbon consumption, new production and export of DOC and POC tothe aphotic zone, eutrophication and diversity, can all be approached fromthis perspective. By including host-specific viruses, this approach gives ahierarchical structure to the control of diversity with nutrient contentcontrolling the maximum size of the photic zone community, size selectivityof predators regulating how the nutrient is distributed between size-groupsof osmotrophic and phagotrophic organisms, and viral host specificityregulating how the nutrients within a size group is distributed between hostgroups. I also briefly discuss how some biological strategies may besuccessful by not conforming to the normal rules of such a framework.Analyzing the behavior of these idealized systems is thus claimed tofacilitate our understanding of the behavior of complex natural food webs.

A multitrophic model to quantify the effects of marine viruses on microbial food webs and ecosystem processes

Viral lysis of microbial hosts releases organic matter that can then be assimilated by nontargeted microorganisms. Quantitative estimates of virus-mediated recycling of carbon in marine waters, first established in the late 1990s, were originally extrapolated from marine host and virus densities, host carbon content and inferred viral lysis rates. Yet, these estimates did not explicitly incorporate the cascade of complex feedbacks associated with virus-mediated lysis. To evaluate the role of viruses in shaping community structure and ecosystem functioning, we extend dynamic multitrophic ecosystem models to include a virus component, specifically parameterized for processes taking place in the ocean euphotic zone. Crucially, we are able to solve this model analytically, facilitating evaluation of model behavior under many alternative parameterizations. Analyses reveal that the addition of a virus component promotes the emergence of complex communities. In addition, biomass partitioning of the emergent multitrophic community is consistent with well-established empirical norms in the surface oceans. At steady state, ecosystem fluxes can be probed to characterize the effects that viruses have when compared with putative marine surface ecosystems without viruses. The model suggests that ecosystems with viruses will have (1) increased organic matter recycling, (2) reduced transfer to higher trophic levels and (3) increased net primary productivity. These model findings support hypotheses that viruses can have significant stimulatory effects across whole-ecosystem scales. We suggest that existing efforts to predict carbon and nutrient cycling without considering virus effects are likely to miss essential features of marine food webs that regulate global biogeochemical cycles.

Viral control of bacterial biodiversity - evidence from a nutrient-enriched marine mesocosm experiment

We demonstrate here results showing that bottom-up and top-down control mechanisms can operate simultaneously and in concert in marine microbial food webs, controlling prokaryote diversity by a combination of viral lysis and substrate limitation. Models in microbial ecology predict that a shift in the type of bacterial growth rate limitation is expected to have a major effect on species composition within the community of bacterial hosts, with a subsequent shift in the composition of the viral community. Only moderate effects would, however, be expected in the absolute number of coexisting virus-host pairs. We investigated these relationships in nutrient-manipulated systems, under simulated in situ conditions. There was a strong correlation in the clustering of the viral and bacterial community data supporting the existence of an important link between the bacterial and viral communities. As predicted, the total number of viral populations was the same in all treatments, while the composition of the viral community varied. Our results support the theoretical prediction that there is one control mechanism for the number of niches for coexisting virus-host pairs (top-down control), and another mechanism that controls which virus-host pairs occupy these niches (bottom-up control).

Specific Affinity for Phosphate Uptake and Specific Alkaline Phosphatase Activity as Diagnostic Tools for Detecting Phosphorus-limited Phytoplankton and Bacteria

We analyzed responses of soluble reactive phosphorus (SRP), bioavailable phosphate (PO4), particulate phosphorus, turnover time of orthophosphate (Tt), and alkaline phosphatase activity (APA) to varying degrees of nutrient stress. The nutrient stress was evoked by different treatments in concentration and combination of inorganic nitrogen (N) and phosphorus (P), and labile organic carbon (glucose) to mesocosms in experiments carried out in eutrophic southern (Odense Fjord, Denmark) and northern (Tvärminne Archipelago, Finland) coastal zones of the Baltic Sea. Despite seasonal and geographical differences, similar responses were observed in both experiments. Low SRP (<100 nmol l−1), shortTt (<10 h), and increased levels of APA were observed in both N+P balanced and P deficient treatments, while the opposite trend was observed in P replete treatments. The shortestTt and the highest APA were found when glucose was combined with N treatment. Bioavailable PO4 was estimated usingTt and P uptake rates as derived from stoichiometric conversion of carbon based primary and bacterial production. With shorterTt, the PO4 pool declined to <1 nmol-P l−1, whereas the SRP background pool (difference between SRP and PO4) remained relatively constant (c. 50 nmol l−1). APA was inversely related to PO4 but not to SRP. Responses of specific APA and specific affinity for PO4 uptake, which are APA and PO4 uptake rates (inverse ofTt), respectively, normalized to the summed P biomass of phytoplankton and bacteria, responded consistently to the pattern and magnitude of nutrient limitation evoked in our experiments. Our results, together with a literature survey, suggest that both parameters can be useful in examining PO4 availability for the natural phytoplankton and bacteria community in P starved aquatic systems.

An Emiliania huxleyi dominated subsurface bloom in Samnangerfjorden, western Norway. Importance of hydrography and nutrients

Abstract Samnangerfjorden is a narrow and sheltered fjord with a pronounced low salinity phosphate- depleted surface layer. The coccolithophorid Emiliania huxleyi (Lohmann) Hay et Mohler bloomed in a nitrate-depleted intermediate layer below the phosphate-depleted surface layer in the inner part of the fjord in May 1992. Maximum cell density was 7 × 106 cells 1−1, and E. huxleyi accounted for 30 % of autotrophic biomass. Both cell density and the calcification rate decreased towards the mouth of the fjord. Production was P-limited in the inner part of the surface layer, while production in the intermediate layer was light-limited. The growth of E. huxleyi in the surface layer was greatly reduced by the low salinity.