Clara Ruiz-González

Terrestrial origin of bacterial communities in complex boreal freshwater networks

Bacteria inhabiting boreal freshwaters are part of metacommunities where local assemblages are often linked by the flow of water in the landscape, yet the resulting spatial structure and the boundaries of the network metacommunity have never been explored. Here, we reconstruct the spatial structure of the bacterial metacommunity in a complex boreal aquatic network by determining the taxonomic composition of bacterial communities along the entire terrestrial/aquatic continuum, including soil and soilwaters, headwater streams, large rivers and lakes. We show that the network metacommunity has a directional spatial structure driven by a common terrestrial origin of aquatic communities, which are numerically dominated by taxa recruited from soils. Local community assembly is driven by variations along the hydrological continuum in the balance between mass effects and species sorting of terrestrial taxa, and seems further influenced by priority effects related to the spatial sequence of entry of soil bacteria into the network.

Away from darkness: a review on the effects of solar radiation on heterotrophic bacterioplankton activity

Heterotrophic bacterioplankton are main consumers of dissolved organic matter (OM) in aquatic ecosystems, including the sunlit upper layers of the ocean and freshwater bodies. Their well-known sensitivity to ultraviolet radiation (UVR), together with some recently discovered mechanisms bacteria have evolved to benefit from photosynthetically available radiation (PAR), suggest that natural sunlight plays a relevant, yet difficult to predict role in modulating bacterial biogeochemical functions in aquatic ecosystems. Three decades of experimental work assessing the effects of sunlight on natural bacterial heterotrophic activity reveal responses ranging from high stimulation to total inhibition. In this review, we compile the existing studies on the topic and discuss the potential causes underlying these contrasting results, with special emphasis on the largely overlooked influences of the community composition and the previous light exposure conditions, as well as the different temporal and spatial scales at which exposure to solar radiation fluctuates. These intricate sunlight-bacteria interactions have implications for our understanding of carbon fluxes in aquatic systems, yet further research is necessary before we can accurately evaluate or predict the consequences of increasing surface UVR levels associated with global change.

Linking microbial community structure and microbial processes: an empirical and conceptual overview

A major goal of microbial ecology is to identify links between microbial community structure and microbial processes. Although this objective seems straightforward, there are conceptual and methodological challenges to designing studies that explicitly evaluate this link. Here, we analyzed literature documenting structure and process responses to manipulations to determine the frequency of structure-process links and whether experimental approaches and techniques influence link detection. We examined nine journals (published 2009-13) and retained 148 experimental studies measuring microbial community structure and processes. Many qualifying papers (112 of 148) documented structure and process responses, but few (38 of 112 papers) reported statistically testing for a link. Of these tested links, 75% were significant and typically used Spearman or Pearsons correlation analysis (68%). No particular approach for characterizing structure or processes was more likely to produce significant links. Process responses were detected earlier on average than responses in structure or both structure and process. Together, our findings suggest that few publications report statistically testing structure-process links. However, when links are tested for they often occur but share few commonalities in the processes or structures that were linked and the techniques used for measuring them.

Interactions between hydrology and water chemistry shape bacterioplankton biogeography across boreal freshwater networks

Disentangling the mechanisms shaping bacterioplankton communities across freshwater ecosystems requires considering a hydrologic dimension that can influence both dispersal and local sorting, but how the environment and hydrology interact to shape the biogeography of freshwater bacterioplankton over large spatial scales remains unexplored. Using Illumina sequencing of the 16S ribosomal RNA gene, we investigate the large-scale spatial patterns of bacterioplankton across 386 freshwater systems from seven distinct regions in boreal Québec. We show that both hydrology and local water chemistry (mostly pH) interact to shape a sequential structuring of communities from highly diverse assemblages in headwater streams toward larger rivers and lakes dominated by fewer taxa. Increases in water residence time along the hydrologic continuum were accompanied by major losses of bacterial richness and by an increased differentiation of communities driven by local conditions (pH and other related variables). This suggests that hydrology and network position modulate the relative role of environmental sorting and mass effects on community assembly by determining both the time frame for bacterial growth and the composition of the immigrant pool. The apparent low dispersal limitation (that is, the lack of influence of geographic distance on the spatial patterns observed at the taxonomic resolution used) suggests that these boreal bacterioplankton communities derive from a shared bacterial pool that enters the networks through the smallest streams, largely dominated by mass effects, and that is increasingly subjected to local sorting of species during transit along the hydrologic continuum.

Effects of large river dam regulation on bacterioplankton community structure

Large rivers are commonly regulated by damming, yet the effects of such disruption on prokaryotic communities have seldom been studied. We describe the effects of the three large reservoirs of the Ebro River (NE Iberian Peninsula) on bacterioplankton assemblages by comparing several sites located before and after the impoundments on three occasions. We monitored the abundances of several bacterial phylotypes identified by rRNA gene probing, and those of two functional groups (picocyanobacteria and aerobic anoxygenic phototrophic bacteria-AAPs). Much greater numbers of particles colonized by bacteria were found in upstream waters than downstream sites. Picocyanobacteria were found in negligible numbers at most sites, whereas AAPs constituted up to 14% of total prokaryotes, but there was no clear effect of reservoirs on the spatial dynamics of these two groups. Instead, damming caused a pronounced decline in Betaproteobacteria, Gammaproteobacteria and Bacteroidetes from upstream to downstream sites, whereas Alphaproteobacteria and Actinobacteria significantly increased after the reservoirs. Redundancy analysis revealed that conductivity, temperature and dissolved inorganic nitrogen were the environmental predictors that best explained the observed variability in bacterial community composition. Our data show that impoundments exerted significant impacts on bacterial riverine assemblages and call attention to the unforeseen ecological consequences of river regulation.

Sunlight modulates the relative importance of heterotrophic bacteria and picophytoplankton in DMSP-sulphur uptake

There is a large body of evidence supporting a major role of heterotrophic bacteria in dimethylsulphoniopropionate (DMSP) utilisation as a source of reduced sulphur. However, a role for phototrophic microorganisms has been only recently described and little is known about their contribution to DMSP consumption and the potential modulating effects of sunlight. In an attempt to ascertain the relative quantitative roles of heterotrophic bacteria and picophytoplankton in the osmoheterotrophic uptake of DMSP-sulphur upon exposure to natural sunlight conditions, we incubated northwestern Mediterranean waters under various optical filters and used an array of bulk and single-cell activity methods to trace the fate of added 35S-DMSP. Flow cytometry cell sorting confirmed dark 35S uptake by Prochlorococcus, Synechococcus and heterotrophic bacteria, the latter being the most efficient in terms of uptake on a cell volume basis. Under exposure to full sunlight, however, the relative contribution of Synechococcus was significantly enhanced, mainly because of the inhibition of heterotrophic bacteria. Microautoradiography showed a strong increase in the proportion of Synechococcus cells actively taking up 35S-DMSP, which, after full sunlight exposure, made up to 15% of total active Bacteria. Parallel incubations with 3H-leucine generally showed no clear responses to light. Finally, size-fractionated assimilation experiments showed greater relative cyanobacterial assimilation during the day than at night compared with that of heterotrophic bacteria. Our results show for the first time a major influence of sunlight in regulating the competition among autotrophic and heterotrophic picoplankton for DMSP uptake at both the daily and seasonal time scales.

Phosphorus use by planktonic communities in a large regulated Mediterranean river.

The regulation of large rivers to meet human requirements (e.g. hydroelectricity production, flood prevention, recreation activities) alters the longitudinal distribution of plankton communities and may affect their capacity to use nutrients and organic matter. Here we analyzed phosphorus (P) availability and use by phytoplankton and bacterioplankton in 6 upstream and 5 downstream sites from a reservoir system in the Ebro River (N Spain). Alkaline phosphatase activity (APA) was related to nutrient availability and biomass of both phytoplankton and bacterioplankton. During dry periods phytoplankton and bacterioplankton APA was inversely correlated to P availability in the water, but these patterns became less clear during wet periods. The phosphorus-APA patterns were more consistent in the upstream sites and especially during dry periods. Although phytoplankton APA was 6-40 times greater than that of bacterioplankton, APA per unit of biomass suggested that bacterioplankton was more efficient at utilizing dissolved organic phosphorus (DOP) in the upstream section during dry periods. Imbalanced N:P ratios in the particulate (N:P ranging 133-170) and dissolved (N:P ranging 301-819) water fractions confirmed the strong P limitation in these upstream communities. The phosphorus-APA patterns were weaker in the downstream section and during wet periods. The reservoirs caused a change in the downstream dynamics, where bacterioplankton biomass was positively correlated to APA but APA per unit of biomass decreased. Our findings reveal that river regulation drives changes in plankton use of organic phosphorus, especially during extreme dry periods.

Transport and transformation of soil-derived CO2, CH4 and DOC sustain CO2 supersaturation in small boreal streams

Streams are typically supersaturated in carbon dioxide (CO2) and methane (CH4), and are recognized as important components of regional carbon (C) emissions in northern landscapes. Whereas there is consensus that in most of the systems the CO2 emitted by streams represents C fixed in the terrestrial ecosystem, the pathways delivering this C to streams are still not well understood. We assessed the contribution of direct soil CO2 injection versus the oxidation of soil-derived dissolved organic C (DOC) and CH4 in supporting CO2 supersaturation in boreal streams in Québec. We measured the concentrations of CO2, CH4 and DOC in 43 streams and adjacent soil waters during summer base-flow period. A mass balance approach revealed that all three pathways are significant, and that the mineralization of soil-derived DOC and CH4 accounted for most of the estimated stream CO2 emissions (average 75% and 10%, respectively), and that these estimated contributions did not change significantly between the studied low order (≤3) streams. Whereas some of these transformations take place in the channel proper, our results suggest that they mainly occur in the hyporheic zones of the streams. Our results further show that stream CH4 emissions can be fully explained by soil CH4 inputs. This study confirms that these boreal streams, and in particular their hyporheic zones, are extremely active processors of soil derived DOC and CH4, not just vents for soil produced CO2.

Single-cell activity of freshwater aerobic anoxygenic phototrophic bacteria and their contribution to biomass production

Aerobic anoxygenic phototrophic (AAP) bacteria are photoheterotrophs that despite their low abundances have been hypothesized to play an ecologically and biogeochemically important role in aquatic systems. Characterizing this role requires a better understanding of the in situ dynamics and activity of AAP bacteria. Here we provide the first assessment of the single-cell activity of freshwater AAP bacteria and their contribution to total bacterial production across lakes spanning a wide trophic gradient, and explore the role of light in regulating AAP activity. The proportion of cells that were active in leucine incorporation and the level of activity per cell were consistently higher for AAP than for bulk bacteria across lakes. As a result, AAP bacteria contributed disproportionately more to total bacterial production than to total bacterial abundance. Interestingly, although environmentally driven patterns in activity did not seem to differ largely between AAP and bulk bacteria, their response to light did, and exposure to light resulted in increases in the proportion of active AAP bacteria with no clear effect on their cell-specific activity. This suggests that light may play a role in the activation of AAP bacteria, enabling these photoheterotrophs to contribute more to the carbon cycle than suggested by their abundance.

Sunlight Effects on the Osmotrophic Uptake of DMSP-Sulfur and Leucine by Polar Phytoplankton

Even though the uptake and assimilation of organic compounds by phytoplankton has been long recognized, very little is still known about its potential ecological role in natural marine communities and whether it varies depending on the light regimes the algae experience. We combined measurements of size-fractionated assimilation of trace additions of 3H-leucine and 35S-dimethylsulfoniopropionate (DMSP) with microautoradiography to assess the extent and relevance of osmoheterotrophy in summer phytoplankton assemblages from Arctic and Antarctic waters, and the role of solar radiation on it was further investigated by exposing samples to different radiation spectra. Significant assimilation of both substrates occurred in the size fraction containing most phytoplankton (>5 µm), sunlight exposure generally increasing 35S-DMSP-sulfur assimilation and decreasing 3H-leucine assimilation. Microautoradiography revealed that the capacity to take up both organic substrates seemed widespread among different polar algal phyla, particularly in pennate and centric diatoms, and photosynthetic dinoflagellates. Image analysis of the microautoradiograms showed for the first time interspecific variability in the uptakes of 35S-DMSP and 3H-leucine by phytoplankton depending on the solar spectrum. Overall, these results suggest that the role of polar phytoplankton in the utilization of labile dissolved organic matter may be significant under certain conditions and further confirm the relevance of solar radiation in regulating heterotrophy in the pelagic ocean.