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  • Review Article
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Predation on prokaryotes in the water column and its ecological implications

A Corrigendum to this article was published on 01 September 2005

Key Points

  • The high prokaryotic mortality in pelagic habitats is caused by both viral lysis and predation by ciliated and flagellated protists. Viral lysis is thought to have the greatest effect on prokaryotic community diversity. By contrast, protistan predation might be most influential in limiting the total bacterial abundance and biomasses in the water column, but it also leaves its mark on microbial community composition. This article focuses on the role of protist predation.

  • What does protistan predation contribute to the 'microbial loop' in pelagic habitats? According to the microbial loop concept, dissolved organic material that is produced during the flux of particulate matter towards larger organisms is reincorporated by heterotrophic bacteria and archaea. Bacterivorous nanoflagellates form a bridge between those planktonic organisms (the picoplankton) that consume dissolved organic matter and those that can only feed on cells >3–5 mm in diameter. Another point of entry for protists is herbivory, that is, direct feeding on bacterial primary producers, as well as feeding on detritus and competing with bacteria for dissolved organic material. Furthermore, grazing by protists is an important mechanism of nutrient regeneration.

  • It is still unclear whether the biomass of prokaryotes in the water column is limited primarily by protistan predation ('top-down control') or by competition for organic carbon and nutrients ('bottom-up control'). However, empirical observations and theoretical models indicate that the mode of control might be influenced by the overall productivity in marine systems. In fresh water, the situation seems to be more complex.

  • A significant proportion of microbial activity in pelagic habitats occurs on, or near, particles known as marine snow or lake snow. Bacteria on such aggregates cannot escape from protistan predation; in fact, protists are more efficient in collecting suspended bacteria if they are attached to a surface than if they are free-living.

  • Not all members of the bacterioplankton are equal in the eyes of their protistan predators. The selective grazing pressure that protistan predators can exert on mixed bacterial assemblages at high particle concentrations is a function of both selective uptake and differential digestion (for example, it is more time-consuming to digest a Gram-positive cell than a Gram-negative cell). At low bacterial concentrations, feeding selectivity decreases.

  • Owing to this selective foraging, protistan predation represents another mechanism (besides viral lysis) that can shape the structure of microbial communities in pelagic habitats.

  • The grazing pressure exerted by protists has not 'gone unnoticed' by their microbial prey. Aquatic bacteria have evolved various anti-predator strategies, which include exopolymer secretion, filament formation, high-speed motility, cell miniaturization and toxin production. It is therefore conceivable that bacterivory by protists has shaped microbial evolution as profoundly as, for example, oxygenic photosynthesis.

Abstract

The oxic realms of freshwater and marine environments are zones of high prokaryotic mortality. Lysis by viruses and predation by ciliated and flagellated protists result in the consumption of microbial biomass at approximately the same rate as it is produced. Protist predation can favour or suppress particular bacterial species, and the successful microbial groups in the water column are those that survive this selective grazing pressure. In turn, aquatic bacteria have developed various antipredator strategies that range from simply 'outrunning' protists to the production of highly effective cytotoxins. This ancient predator–prey system can be regarded as an evolutionary precursor of many other interactions between prokaryotic and eukaryotic organisms.

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Figure 1: Two models that address the relative importance of predation in oligotrophic and eutrophic conditions.
Figure 2: Phenotypic properties of aquatic bacteria that might provide protection from predation by heterotrophic protists.
Figure 3: The effect of predation on microbial community structure.
Figure 4: 'Killing the winner' by predation.
Figure 5: A simple conceptual model that relates changes in microbial species composition to community-level growth and loss.

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Acknowledgements

I thank my students and colleagues for the inspiring discussions and bitter controversies that have helped to shape my understanding of aquatic microbial food webs. Valuable suggestions by three reviewers have greatly improved the text. This work was supported by the European Union and by the Max-Planck Society.

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Glossary

PELAGIC HABITAT

The parts of a lake, river and ocean that make up the water column.

OLIGOTROPHIC

An aquatic environment that has low levels of nutrient and algal photosynthetic production (for example, high mountain lakes).

PHAGOTROPHY

The uptake of particles by eukaryotic cells.

BACTERIOPLANKTON

Bacteria that inhabit the water column of lakes and oceans, either freely suspended or attached to particles.

OMNIVORY

Ability of animals to feed on different types of prey.

HETEROTROPHY

The acquisition of metabolic energy by consumption of particulate or dissolved organic matter.

BACTERIVOROUS NANOFLAGELLATES

Small, flagellated protists that range in size from 3 to 15 mm and that can feed on bacteria.

PICOPLANKTON

Organisms suspended in the water column that are less than 2 mm in size.

DETRITAL PARTICLES

Dead organic material suspended in the water column.

PRIMARY PRODUCERS

Organisms that are the original source of organic material in an ecosystem — plants, algae or chemosynthetic microorganisms.

AUTOTROPHY

The acquisition of metabolic energy from the fixation of inorganic carbon, for example, by photo- or chemosynthesis.

EUPHOTIC ZONE

Upper realms of the oceans that are penetrated by sufficient amounts of light for the growth of photosynthetic organisms.

HERBIVORY

The consumption of plants.

NUTRIENT REGENERATION

Processes by which nutrients that are bound in organismic biomass are retransformed into their inorganic form.

TOP-DOWN CONTROL

Ecological scenario in which the abundance or biomass of organisms is mainly determined by mortality owing to predation.

BOTTOM-UP CONTROL

Ecological scenario in which the abundance or biomass of organisms is mainly determined by a lack of resources and mortality owing to starvation.

EUTROPHIC

Aquatic systems with high availability of dissolved organic matter from photosynthetic production or other sources. Examples include shallow lowland lakes and coastal estuaries.

CHEMOSPHERE

Zone of elevated concentration of organic molecules that diffuse from the surface of a suspended particle.

CHEMOTAXIS

Ability of microorganisms to follow a chemical gradient.

FILTER FEEDING

Feeding mode that filters particles from the water by means of a sieving structure. Usually the prey is very small compared with the predator.

INTERCEPTION FEEDING

The capture of individual bacteria or particles by direct random contact with a protistan cell. Usually the sizes of the predator and prey are similar.

PHOTOTROPHS

Organisms that fix inorganic carbon using light energy.

MIXOTROPHS

Organisms that are part autotrophic and part heterotrophic, for example, carnivorous plants.

ULTRAMICROBACTERIA

Bacteria that maintain cell volumes of <0.1 mm3 even during exponential growth on rich media.

QUORUM SENSING

Bacterial communication system based on the secretion and detection of a quorum, which is a substance that increases with population density and that induces expression of specific genes in the population above a threshold concentration.

APOPTOTIC RESPONSE

Phenotypic changes that occur during programmed cell death in eukaryotic cells, for example, cell shrinkage.

SPECIES RICHNESS

Number of species that are present in a community.

COMMUNITY EVENNESS

Balance of the respective number of individuals in each species of a community.

FEAST OR FAMINE

Growth strategy of microorganisms that rapidly proliferate if conditions are optimal and that can survive extended periods of starvation.

ECOPHYSIOLOGICAL APPROACHES

Determination of protistan physiological properties under field conditions, for example, of feeding rates through uptake of surrogate particles.

MOLECULAR BIOLOGICAL APPROACHES

Cultivation-independent identification of protists in environmental samples by sequencing of rRNA genes and fluorescence in situ hybridization with rRNA-targeted probes.

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Pernthaler, J. Predation on prokaryotes in the water column and its ecological implications. Nat Rev Microbiol 3, 537–546 (2005). https://doi.org/10.1038/nrmicro1180

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