A Few Words on Diversity
Our knowledge of aquatic microbial diversity is largely derived from the analysis of 16S rRNA gene sequences directly PCR amplified from environmental DNA (239
) and from culture collections predominantly established on rich solid media (107
). Both approaches have revealed complementary and often nonoverlapping facets of diversity (but see reference 228
). Nevertheless, our perception of the total diversity of aquatic microbes is most probably incomplete. A recent investigation by shotgun cloning of large genome fragments from Sargasso Sea picoplankton concentrates and high-throughput genome analysis has produced >100 novel bacterial 16S rRNA sequence types in a single sample (305
Evidence has accumulated that there is relatively little overlap between the phylogenetic groups that are present in marine and freshwater environments (89, 180, 241), e.g., specific groups of archaea appear to be entirely limited to the marine water column (59, 76, 173). Lineages of 16 rRNA gene sequence types that occur in both habitat types include the SAR11 clade of Alphaproteobacteria (14, 85, 329), and the ammonia-oxidizing Betaproteobacteria (123, 297). Even within these clades, distinct clusters of marine and freshwater sequence types can be distinguished (329). Some clades of actinobacteria typically found in freshwater habitats also contain sequences from estuaries and marine waters (48, 309), whereas other clades within this phylum are exclusively of either marine or freshwater origin (91, 240, 309, 328). Members of the very diverse Cytophaga/Flexibacter/Flavobacterium group are common in some coastal and offshore marine habitats (45, 63, 144, 280), but they also occur in rivers and lakes (28, 143, 218, 223). Bacteria from this group appear to have radiated across a range of aquatic habitats, including biofilms and sediments (34, 158).
The phylogenetic ties between freshwater and soil microbes are still unclear. Sequence types from both environments have, e.g., been found within the freshwater acIV lineage of the actinobacteria (309). There are furthermore indications that microbial assemblages in some lakes may be similar to those in the influx from the catchment (156).
In the context of this review we distinguish between the multitude of microbial phylogenetic lineages that may occur in various aquatic systems and the few groups of microbes that have been shown to form substantial populations in such environments. Clearly, archival listings of microbial diversity from different habitats are a crucial first step to investigate the role and fate of aquatic microbes, since they provide the essential fundament for subsequent studies about the ecology of particular populations. However, it is equally important to progress from a purely qualitative appreciation of microbial diversity to the quantification of the abundances, biomasses, and activities of different phylogenetic groups. For example, it is presently still unclear if members of the Verrucomicrobia are an important component of freshwater assemblages. Such bacteria are frequently detected in lakes by PCR-based methods (157, 330, 331). From all we know, their densities might be one in a million but potentially also >10% of all cells. The following sections thus specifically discuss investigations that have established the cell concentrations, spatial distributions, temporal successions, or physiological features of specific microbial taxa in the plankton of marine and freshwater systems.
Bacterial Populations in the Marine Water Column
Some groups of marine bacteria had been known for years from their 16S rRNA gene sequences before their abundances in the water column were determined. This is the case for bacteria related to the marine SAR11 (188
), SAR86 (210
), SAR116 (71
), SAR202 (189
), and SAR406 (71
) clades, whereas for the various lineages of marine actinobacteria (240
) such evidence is still lacking. Members of the SAR11 clade are believed to be among the most common prokaryotes in the marine plankton. It has been reported that these bacteria may seasonally represent >50% of total bacterial abundances in surface waters of the northwestern Sargasso Sea and 25% of subeuphotic microbial assemblages (188
). Bacteria related to Roseobacter
sp. (also referred to as the SAR83 cluster, (241
) are another common component of coastal and offshore microbial assemblages, and they may constitute up to 25% of the marine picoplankton (63
). The seasonal abundance of Roseobacter
spp. in coastal North Sea picoplankton closely followed the development of phytoplankton biomass (Fig. 7
). The geographic distribution of one particular subcluster from this lineage appears to be limited to temperate and polar oceans (266
). In transects across the German Bight Gammaproteobacteria
related to the SAR86 lineage on average formed 7% of total cell numbers (210
), and 3 to 6% of all bacterial 16S rRNA genes in Monterey Bay surface waters were affiliated with this group during an upwelling event (295
). Genes encoding proteorhodopsin were first described in members of the SAR86 clade (19
), but recent findings indicate that such light-driven proton pumps might be a widespread feature of marine bacterioplankton (305
In addition to the well-established clades of marine bacteria, new groups have been described that may reach high densities in the water column. The NOR5 lineage of the OM60 clade of Gammaproteobacteria (39) seasonally represented between 5 and 10% of coastal picoplankton in the North Sea (63) and 2-3% in the western Mediterranean Sea (L. Alonso and J. Pernthaler, unpublished data). Uncultured members of the novel DE2 cluster (Cytophaga/Flexibacter/Flavobacterium group) accounted for 10% of total cells in samples from the Delaware Estuary and from the Chukchi Sea (Arctic Ocean) (144). In brackish waters of the Baltic Sea and in samples from the Skagerrak-Kattegat front, substantial populations of species related to Alphaproteobacteria and to the Cytophaga/Flexibacter/Flavobacterium group were detected using radioactively labeled whole-genome probes (226, 228). Interestingly, these bacteria also readily formed colonies on solid media, which clearly contrasts with findings from other marine sites (62).
The composition of microbial communities in more extreme habitats might sometimes be very simple. Hydrothermal circulation activities in deep sea environments produce buoyant plumes with substantially elevated levels of reduced chemicals. The bacterial assemblages within such a plume inside the caldera of the Suiyo Seamount volcano consisted almost entirely of two distinct phylogenetic populations that were related to sulfur-oxidizing symbionts of hydrothermal vent fauna (291). The caldera might thus represent a giant natural continuous-cultivation system for these two groups.
Sometimes, it may be necessary to define microbial populations at the level of single strains, e.g., for the study of pathogenic Vibrio spp. in marine waters. In coastal environments Vibrio cholerae can be found both attached on particles and free-living in the water column (44), and pronounced seasonal and horizontal differences in population sizes have been reported (83, 117). In microcosms spiked with V. cholerae, rapid growth of these bacteria was observed after addition of organic carbon (190). It is thus conceivable that anthropogenic eutrophication might indirectly favor the growth and dispersal of pathogenic Vibrio strains.
The two major pelagic lineages of Crenarchaeota
are among the most well studied phylogenetic group of uncultured microbes in marine picoplankton. Both oligo- and polynucleotide probes have been developed for the direct visualization of such microbes in water samples (57
). Recently, a protocol for CARD-FISH staining of Archaea
in samples from the deep sea has been described (296
). Originally it was believed that creanarchaeota only form large populations in the meso- and bathypelagic layers below the euphotic zone (59
). In a seasonal study in the North Pacific subtropical gyre, the mean annual abundances of Crenarchaeota
below 200 m water depth ranged between 20 and 40% of total picoplankton cells, which corresponded to 3 x 103
to 1 x 105
). Comparable abundances of this archaeal group were also reported from the deeper waters of the Antarctic circumpolar deep water (40
). However, the same study also detected large crenarchaeal populations by FISH in the surface waters of the Southern Ocean during the winter months. Such contrasting vertical distribution patterns are currently difficult to interpret.
The metabolic capacities of planktonic crenarchaea are unclear, but there are indications that members of this lineage might be auto- or mixotrophic (120, 321). The planktonic marine Euryarchaeota on the other hand appear to be a common element of coastal assemblages and surface waters. Members of this lineage seasonally formed >30% of all cells in the surface picoplankton of the North Sea (214) (Fig. 7). Seasonal blooms of Euryarchaeota were also observed during a long-term study in surface waters of the upper Santa Barbara Channel (191).
Numerically Important Bacteria in Freshwater
Seasonal dynamics of different freshwater bacterioplankton populations have first been reported from an ultraoligotrophic mountain lake (218
). So far, bacteria from two of the four typical freshwater lineages of Betaproteobacteria
as defined by Glöckner et al. (91
) have been detected in high abundance in the environment. Bacteria affiliated with the beta I clade (also termed the "Rhodoferax
sp. BAL47 lineage") (328
) formed populations of >10% in the summer plankton of a eutrophic reservoir (278
). A second lineage of Betaproteobacteria
related to Polynucleobacter necessarius
(beta II) seasonally constituted up to 50% of all pelagic microbes in the aerobic waters of a meromictic humic lake (35
). Filamentous bacteria from the LD2 subclade (328
) that is closely related to Haliscomenobacter hydrossis
) transiently formed >40% of total bacterial biomass in a mesotrophic lake (223
). Actinobacteria from the uncultured acI clade (91
) are another ubiquitous group of freshwater prokaryotes (91
) that seasonally occur in high densities in habitats of very different limnological characteristics, e.g., humic (35
) or high mountain lakes (91
Bacterial Populations Attached to Organic Particles
Microbial assemblages on suspended organic aggregates differ from those of the water column (56
). So far the particle-attached communities in marine habitats have only been investigated qualitatively by fingerprinting and comparative sequence analysis (48
). More information is available about limnic and riverine aggregates. Microbial populations on aggregates in fresh waters change with the ageing of such particles (101
) or during their transport from rivers into estuaries (265
). Three populations related to the genera Duganella
, and Acidovorax
formed almost half of the Betaproteobacteria
on organic aggregates obtained from Lake Constance at a depth of 50 m (261
). These bacteria effectively colonized artificially produced microaggregates within 24 h. Interestingly, members of the three genera were rarely detected in the planktonic microbial assemblage, and they were not affiliated with the presently defined clades of typical freshwater Betaproteobacteria
). Instead, these bacteria are known from highly eutrophic environments such as activated sludge (249
In contrast to the lake snow assemblages, riverine organic particles have been described to mainly harbor Betaproteobacteria related to the drinking water biofilm bacterium Aquabacterium commune. These bacteria formed up to 30% of all cells on lotic organic aggregates in the river Elbe (135). The composition of the microbial assemblages on such aggregates showed pronounced seasonal changes, and bacteria related to the Planctomycetales were absent in winter.