Mechanisms Generating Dichotomies in the Life Strategies of Heterotrophic Marine Prokaryotes

Understanding the mechanisms that generate and maintain diversity in marine prokaryotic communities is one of the main challenges for contemporary marine microbiology. We here review how observational, experimental, and theoretical evidence converge on the conclusion that the marine pelagic community of heterotrophic prokaryotes consists of organisms with two main types of life strategies. We illustrate this dichotomy by SAR11 and Vibrio spp. as typical representatives of the two strategies. A theory for life strategy dichotomy exists in classical r/K-selection. We here discuss an additional dichotomy introduced by what we term S/L-selection (for Small and Large, respectively). While r/K-selection focuses on the role of environmental disturbances, steady-state models suggest that high abundance at species level should be closely related to a low trade-off between competition and defense. We summarize literature indicating that the high availability of organic C is an essential environmental factor favoring Vibrio spp. and suggest that the essence of the generalized L-strategy is to reduce the competition-predator defense trade-off by using non-limiting organic C to increase size. The “streamlining” theory that has been suggested for the S-strategist SAR11 proposes the opposite: that low trade-off is achieved by a reduction in size. We show how this apparent contradiction disappears when the basic assumptions of diffusion-limited uptake are considered. We propose a classification scheme that combines S/L and r/K-selection using the two dimensions of organic C availability and environmental disturbance. As organic C in terrestrial runoff and size of the oligotrophic oceanic gyres are both changing, habitat size for both S- and L-strategists are affected by global change. A theory capturing the main aspects of prokaryote life strategies is therefore crucial for predicting responses of the marine microbial food web to climate change and other anthropogenic influences.publishedVersio

Explaining microbial population genomics through phage predation

The remarkable diversity of genes within the pool of prokaryotic genomes belonging to the same species or pan-genome is difficult to reconcile with the widely accepted paradigm which asserts that periodic selection within bacterial populations would regularly purge genomic diversity by clonal replacement. Recent evidence from metagenomics indicates that even within a single sample a large diversity of genomes can be present for a single species. We have found that much of the differential gene content affects regions that are potential phage recognition targets. We therefore propose the operation of Constant-Diversity dynamics 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 indicate under which ecological circumstances each dynamics could predominate

Winter−spring transition in the subarctic Atlantic: microbial response to deep mixing and pre-bloom production

In temperate, subpolar and polar marine systems, the classical perception is that diatoms initiate the spring bloom and thereby mark the beginning of the productive season. Contrary to this view, we document an active microbial food web dominated by pico- and nanoplankton prior to the diatom bloom, a period with excess nutrients and deep convection of the water column. During repeated visits to stations in the deep Iceland and Norwegian basins and the shallow Shetland Shelf (26 March to 29 April 2012), we investigated the succession and dynamics of photosynthetic and heterotrophic microorganisms. We observed that the early phytoplankton production was followed by a decrease in the carbon:nitrogen ratio of the dissolved organic matter in the deep mixed stations, an increase in heterotrophic prokaryote (bacteria) abundance and activity (indicated by the high nucleic acid:low nucleic acid bacteria ratio), and an increase in abundance and size of heterotrophic protists. The major chl a contribution in the early winter-spring transition was found in the fraction 50 µm) were stimulated by deep mixing later in the period, while picophytoplankton were unaffected by mixing; both physical and biological reasons for this development are discussed herein

Linking bacterial community structure to advection and environmental impact along a coast-fjord gradient of the Sognefjord, western Norway

publishedVersio

Temperate infection in a virus–host system previously known for virulent dynamics

The blooming cosmopolitan coccolithophore Emiliania huxleyi and its viruses (EhVs) are a model for density-dependent virulent dynamics. EhVs commonly exhibit rapid viral reproduction and drive host death in high-density laboratory cultures and mesocosms that simulate blooms. Here we show that this system exhibits physiology-dependent temperate dynamics at environmentally relevant E. huxleyi host densities rather than virulent dynamics, with viruses switching from a long-term non-lethal temperate phase in healthy hosts to a lethal lytic stage as host cells become physiologically stressed. Using this system as a model for temperate infection dynamics, we present a template to diagnose temperate infection in other virus–host systems by integrating experimental, theoretical, and environmental approaches. Finding temperate dynamics in such an established virulent host–virus model system indicates that temperateness may be more pervasive than previously considered, and that the role of viruses in bloom formation and decline may be governed by host physiology rather than by host–virus densities

Competition–defense trade-offs in the microbial world

publishedVersio

How trophic cascades and photic zone nutrient content interact to generate basin-scale differences in the microbial food web

In linear food chains, resource and predator control produce positive and negative correlations, respectively, between biomass at adjacent trophic levels. These simple relationships become more complex in food webs that contain alternative food chains of unequal lengths. We have used a “minimum” model for the microbial part of the pelagic food web that has three such food chains connecting free mineral nutrients to copepods: via diatoms, autotrophic flagellates, and heterotrophic bacteria. Trophic cascades from copepods strongly modulates the balance between the three pathways and, therefore, the functionality of the microbial food web in services such as food production for higher trophic levels, DOM degradation, and ocean carbon sequestration. The result is a theoretical framework able to explain, not only apparent conflicts in Arctic mesocosm experiments, but also biogeochemical features of the Mediterranean. Here, the fundamental difference between Arctic and Mediterranean microbial food webs is the way they are predator driven by seasonal migration of large copepods in the Arctic, but resource driven due to the anti-estuarine circulation in the Mediterranean. In this framework, global change effects on microbial ecosystem functions are more like to come indirectly through changes in these drivers than through direct temperature effects on the microbes

Are bacteria active in the cold pelagic ecosystem of the Barents Sea?

Bacterial biomass and activity indicators have been studied at low water temperatures (?1.9 to +4°C) in Barents Sea. Strong responses by indicators of bacterial activity, such as hydrolytic enzyme and substrate uptake potentials, were observed in association with the development of phytoplankton blooms. At late successional stages of blooms, observation by epifluorescence microscopy revealed heavy bacterial colonisation of detrital matter, in particular of senescent colonies of Phaeocystis pouchetii. Based on the retention of bacteria on filters of 1 ?m pore size, up to 55% of the bacterial population was estimated to be attached to organic aggregates in some cases. Based on thymidine incorporation and a conventional conversion factor, bacterial generation times as short as one day were estimated at temperatures below zero. Changes in substrate availability governed by the successional stages of the planktonic ecosystem seem to be more important as controlling factors for bacterial growth than the low temperatures of the Barents Sea

Mechanisms Generating Dichotomies in the Life Strategies of Heterotrophic Marine Prokaryotes

Understanding the mechanisms that generate and maintain diversity in marine prokaryotic communities is one of the main challenges for contemporary marine microbiology. We here review how observational, experimental, and theoretical evidence converge on the conclusion that the marine pelagic community of heterotrophic prokaryotes consists of organisms with two main types of life strategies. We illustrate this dichotomy by SAR11 and Vibrio spp. as typical representatives of the two strategies. A theory for life strategy dichotomy exists in classical r/K-selection. We here discuss an additional dichotomy introduced by what we term S/L-selection (for Small and Large, respectively). While r/K-selection focuses on the role of environmental disturbances, steady-state models suggest that high abundance at species level should be closely related to a low trade-off between competition and defense. We summarize literature indicating that the high availability of organic C is an essential environmental factor favoring Vibrio spp. and suggest that the essence of the generalized L-strategy is to reduce the competition-predator defense trade-off by using non-limiting organic C to increase size. The “streamlining” theory that has been suggested for the S-strategist SAR11 proposes the opposite: that low trade-off is achieved by a reduction in size. We show how this apparent contradiction disappears when the basic assumptions of diffusion-limited uptake are considered. We propose a classification scheme that combines S/L and r/K-selection using the two dimensions of organic C availability and environmental disturbance. As organic C in terrestrial runoff and size of the oligotrophic oceanic gyres are both changing, habitat size for both S- and L-strategists are affected by global change. A theory capturing the main aspects of prokaryote life strategies is therefore crucial for predicting responses of the marine microbial food web to climate change and other anthropogenic influences

Stepwise building of plankton functional type (PFT) models: A feasible route to complex models?

We discuss the strategy of building models of the lower part of the planktonic food web in a stepwise manner: starting with few plankton functional types (PFTs) and adding resolution and complexity while carrying along the insight and results gained from simpler models. A central requirement for PFT models is that they allow sustained coexistence of the PFTs. Here we discuss how this identifies a need to consider predation, parasitism and defence mechanisms together with nutrient acquisition and competition. Although the stepwise addition of complexity is assumed to be useful and feasible, a rapid increase in complexity strongly calls for alternative approaches able to model emergent system-level features without a need for detailed representation of all the underlying biological detail