Fate of heterotrophic microbes in pelagic habitats: focus on populations

Abstract

Major biogeochemical processes in the water columns of lakes and oceans are related to the activities of heterotrophic microbes, e.g., the mineralization of organic carbon from photosynthesis and allochthonous influx or its transport to the higher trophic levels. During the last 15 years, cultivation-independent molecular techniques have substantially contributed to our understanding of the diversity of the microbial communities in different aquatic systems. In parallel, the complexity of aquatic habitats at a microscale has inspired research on the ecophysiological properties of uncultured microorganisms that thrive in a continuum of dissolved to particulate organic matter. One possibility to link these two aspects is to adopt a"Gleasonian" perspective, i.e., to study aquatic microbial assemblages in situ at the population level rather than looking at microbial community structure, diversity, or function as a whole. This review compiles current knowledge about the role and fate of different populations of heterotrophic picoplankton in marine and inland waters. Specifically, we focus on a growing suite of techniques that link the analysis of bacterial identity with growth, morphology, and various physiological activities at the level of single cells. An overview is given of the potential and limitations of methodological approaches, and factors that might control the population sizes of different microbes in pelagic habitats are discussed.

FIG. 1.

Schematic example of phenotypic diversification of aquatic bacteria. The relationship between the different genotypes and their specific ecophysiological features, life strategies, and behavior is often poorly understood.

FIG. 2.

Conceptual model for an operational definition of microbial populations. In the context of ecological investigations three bacterial taxa, A, B, and C, can be meaningfully defined as different populations if they also differ in an ecologically relevant feature (parameter 1). However, a splitting of population C may be required if it is studied in the context of a second environmental variable (parameter 2).

FIG. 3.

FISH, a versatile tool for the study of microbial populations in aquatic systems. The FISH approach is embedded in a suite of techniques that are required for the acquisition and processing of rRNA sequence information or that allow simultaneous investigation of microbial geno- and phenotypes at the single-cell level. S₁ to S₄, samples.

FIG. 4.

Comparison of hybridized bacteria from North Sea waters (A) after FISH with fluorescently monolabeled probes and (B) after CARD-FISH. Photographic exposure times were (A) 10 s and (B) 1 s. (Modified from reference .)

FIG. 5.

Contribution of filamentous bacteria from the LD2 clade to total bacterial abundances (line and symbols) and biovolume (bars) in the spring plankton of a lake. (Modified from reference .)

FIG. 6.

(A) Glucose uptake into single cells under anoxic conditions as studied by FISH and microautoradiography. Green objects surrounded by black deposits are Roseobacter sp. cells from coastal North Sea waters that have incorporated radiolabeled substrate. (B) Immunocytochemical detection of DNA de novo synthesis in freshwater bacteria after incubation with bromodeoxyuridine. Green objects: cells affiliated with actinobacteria; yellow-orange objects: bromodeoxyuridine-positive actinobacteria; red objects: other bromodeoxyuridine-positive bacteria. Bar, 10 μm.

FIG. 7.

Seasonal population dynamics of marine Euryarchaeota and of bacteria from the Roseobacter lineage in the German Bight of the North Sea. Bars: phytoplankton biomass. (Combined from references and .)

FIG. 8.

Effect of size-selective protistan grazing on bacterioplankton biomass size distribution. Several microbial populations with different mean cell sizes are highlighted. (a) Low or no grazing: unimodal cell size distribution. Most biomass is distributed in populations close to the mean size, whereas very small or large populations are rare. (b) Heavy grazing: populations within the edible cell size range are eliminated unless they can escape predation by a change in their mean cell sizes. Under these conditions the growth of very small or very large phenotypes is favored. (Reproduced with permission from Nature Reviews Microbiology [215] copyright Macmillan Magazines Ltd.)