Within- and between-lake variability in the composition of bacterioplankton communities: investigations using multiple spatial scales

This study examined the similarity of epilimnetic bacterial community composition (BCC) across several within- and among-lake spatial scales, and the environmental factors giving rise to similar bacterial communities in different lakes were also explored. Samples were collected from 13 northern and southern Wisconsin lakes representing gradients in lake size, productivity, dissolved organic carbon and humic acid contents, and pH. Hypotheses regarding patchy distribution of bacterial communities in lakes were tested by comparing samples collected from nearby (tens of meters) and distant (hundreds of meters) sampling sites in the same lake. BCC was characterized by using a molecular fingerprinting technique, automated ribosomal intergenic spacer analysis (ARISA). Overall, samples collected at the 10-m, 100-m, and between-lake scales differed by 13, 17, and 75%, respectively. Variation at these last two scales was significant. The development of within-lake variation in BCC appeared to depend on the isolation of water by lake shoreline features such as bays or narrow constrictions. ARISA profiles from northern lakes had fewer peaks and were less similar to each other than were those of the southern lakes, suggesting that regional features do not necessarily lead to the development of similar bacterial communities. Lakes at similar positions on productivity and dissolved organic carbon concentration gradients had similar bacterial communities, and bacterial diversity was positively correlated with lake productivity and water temperature. Factorial studies taking into account these gradients, as well as regional spatial scales, should provide much insight into the nature of aquatic bacterial biogeography.     

Geographic and Environmental Sources of Variation in Lake Bacterial Community Composition

This study used a genetic fingerprinting technique (automated ribosomal intergenic spacer analysis [ARISA]) to characterize microbial communities from a culture-independent perspective and to identify those environmental factors that influence the diversity of bacterial assemblages in Wisconsin lakes. The relationships between bacterial community composition and 11 environmental variables for a suite of 30 lakes from northern and southern Wisconsin were explored by canonical correspondence analysis (CCA). In addition, the study assessed the influences of ARISA fragment detection threshold (sensitivity) and the quantitative, semiquantitative, and binary (presence-absence) use of ARISA data. It was determined that the sensitivity of ARISA was influential only when presence-absence-transformed data were used. The outcomes of analyses depended somewhat on the data transformation applied to ARISA data, but there were some features common to all of the CCA models. These commonalities indicated that differences in bacterial communities were best explained by regional (i.e., northern versus southern Wisconsin lakes) and landscape level (i.e., seepage lakes versus drainage lakes) factors. ARISA profiles from May samples were consistently different from those collected in other months. In addition, communities varied along gradients of pH and water clarity (Secchi depth) both within and among regions. The results demonstrate that environmental, temporal, regional, and landscape level features interact to determine the makeup of bacterial assemblages in northern temperate lakes.     

Geographic and environmental sources of variation in lake bacterial community composition

This study used a genetic fingerprinting technique (automated ribosomal intergenic spacer analysis [ARISA]) to characterize microbial communities from a culture-independent perspective and to identify those environmental factors that influence the diversity of bacterial assemblages in Wisconsin lakes. The relationships between bacterial community composition and 11 environmental variables for a suite of 30 lakes from northern and southern Wisconsin were explored by canonical correspondence analysis (CCA). In addition, the study assessed the influences of ARISA fragment detection threshold (sensitivity) and the quantitative, semiquantitative, and binary (presence-absence) use of ARISA data. It was determined that the sensitivity of ARISA was influential only when presence-absence-transformed data were used. The outcomes of analyses depended somewhat on the data transformation applied to ARISA data, but there were some features common to all of the CCA models. These commonalities indicated that differences in bacterial communities were best explained by regional (i.e., northern versus southern Wisconsin lakes) and landscape level (i.e., seepage lakes versus drainage lakes) factors. ARISA profiles from May samples were consistently different from those collected in other months. In addition, communities varied along gradients of pH and water clarity (Secchi depth) both within and among regions. The results demonstrate that environmental, temporal, regional, and landscape level features interact to determine the makeup of bacterial assemblages in northern temperate lakes.     

Resource Availability and Spatial Heterogeneity Control Bacterial Community Response to Nutrient Enrichment in Lakes

The diversity and composition of ecological communities often co-vary with ecosystem productivity. However, the relative importance of productivity, or resource abundance, versus the spatial distribution of resources in shaping those ecological patterns is not well understood, particularly for the bacterial communities that underlie most important ecosystem functions. Increasing ecosystem productivity in lakes has been shown to influence the composition and ecology of bacterial communities, but existing work has only evaluated the effect of increasing resource supply and not heterogeneity in how those resources are distributed. We quantified how bacterial communities varied with the trophic status of lakes and whether community responses differed in surface and deep habitats in response to heterogeneity in nutrient resources. Using ARISA fingerprinting, we found that bacterial communities were more abundant, richer, and more distinct among habitats as lake trophic state and vertical heterogeneity in nutrients increased, and that spatial resource variation produced habitat specific responses of bacteria in response to increased productivity. Furthermore, changes in communities in high nutrient lakes were not produced by turnover in community composition but from additional taxa augmenting core bacterial communities found in lower productivity lakes. These data suggests that bacterial community responses to nutrient enrichment in lakes vary spatially and are likely influenced disproportionately by rare taxa.     

Temporal Patterns in Bacterial Communities in Three Temperate Lakes of Different Trophic Status

Despite considerable attention in recent years, the composition and dynamics of lake bacterial communities over annual time scales are poorly understood. This study used automated ribosomal intergenic spacer analysis (ARISA) to explore the patterns of change in lake bacterial communities in three temperate lakes over 2 consecutive years. The study lakes included a humic lake, an oligotrophic lake, and a eutrophic lake, and the epilimnetic bacterial communities were sampled every 2 weeks. The patterns of change in bacterial communities indicated that seasonal forces were important in structuring the behavior of the bacterial communities in each lake. All three lakes had relatively stable community composition in spring and fall, but summer changes were dramatic. Summertime variability was often characterized by recurrent drops in bacterial diversity. Specific ARISA fragments derived from these lakes were not constant among lakes or from year to year, and those fragments that did recur in lakes in different years did not exhibit the same seasonal pattern of recurrence. Nonetheless, seasonal patterns observed in 2000 were fairly successful predictors of the rate of change in bacterial communities and in the degree of autocorrelation of bacterial communities in 2001. Thus, seasonal forces may be important structuring elements of these systems as a whole even if they are uncoupled from the dynamics of the individual system components.     

Experimental manipulations of microbial food web interactions in a humic lake: shifting biological drivers of bacterial community structure

A previous multiyear study observed correlations between bacterioplankton community composition (BCC) and abundance and the dynamics of phytoplankton populations and bacterivorous grazers in a humic lake. These observations generated hypotheses about the importance of trophic interactions (both top-down and bottom-up) for structuring bacterial communities in this lake, which were tested using two multifactorial food web manipulation experiments that separately manipulated the intensity of grazing and the composition of the phytoplankton community. Our results, combined with field observations, suggest that a hierarchy of drivers structures bacterial communities in this lake. While other studies have noted links between aggregate measures of phytoplankton and bacterioplankton communities, we demonstrate here correlations between succession of phytoplankton assemblages and BCC as assessed by automated ribosomal intergenic spacer analysis (ARISA). We used a novel approach linking community ARISA data to phylogenetic assignments from sequence analysis of 16S rRNA gene clone libraries to examine the responses of specific bacterial phylotypes to the experimental manipulations. The synchronous dynamics of these populations suggests that primary producers may mediate BCC and diversity through labile organic matter production, which evolves in quality and quantity during phytoplankton succession. Superimposed on this resource-mediated control of BCC are brief periods of intense bacterivory that impact bacterial abundance and composition.     

Climate and landscape influence on indicators of lake carbon cycling through spatial patterns in dissolved organic carbon

Freshwater ecosystems are strongly influenced by both climate and the surrounding landscape, yet the specific pathways connecting climatic and landscape drivers to the functioning of lake ecosystems are poorly understood. Here, we hypothesize that the links that exist between spatial patterns in climate and landscape properties and the spatial variation in lake carbon (C) cycling at regional scales are at least partly mediated by the movement of terrestrial dissolved organic carbon (DOC) in the aquatic component of the landscape. We assembled a set of indicators of lake C cycling (bacterial respiration and production, chlorophyll a, production to respiration ratio, and partial pressure of CO₂), DOC concentration and composition, and landscape and climate characteristics for 239 temperate and boreal lakes spanning large environmental and geographic gradients across seven regions. There were various degrees of spatial structure in climate and landscape features that were coherent with the regionally structured patterns observed in lake DOC and indicators of C cycling. These different regions aligned well, albeit nonlinearly along a mean annual temperature gradient; whereas there was a considerable statistical effect of climate and landscape properties on lake C cycling, the direct effect was small and the overall effect was almost entirely overlapping with that of DOC concentration and composition. Our results suggest that key climatic and landscape signals are conveyed to lakes in part via the movement of terrestrial DOC to lakes and that DOC acts both as a driver of lake C cycling and as a proxy for other external signals.     

Dissolved Organic Carbon as Major Environmental Factor Affecting Bacterioplankton Communities in Mountain Lakes of Eastern Japan

Relationships between environmental factors and bacterial communities were investigated in 41 freshwater lakes located in mountainous regions of eastern Japan. Bacterioplankton community composition (BCC) was determined by polymerase chain reaction-denaturing gradient gel electrophoresis of the 16S rRNA gene and then evaluated on the basis of physicochemical and biological variables of the lakes. Canonical correspondence analysis revealed that BCC of oligotrophic lakes was significantly influenced by dissolved organic carbon (DOC) content, but its effect was not apparent in the analysis covering all lakes including mesotrophic and eutrophic ones. The generalized linear model showed the negative association of DOC on the taxon richness of bacterioplankton communities. DOC was positively correlated with the catchment area per lake volume, suggesting that a large fraction of DOC supplied to the lake was derived from terrestrial sources. These results suggest that allochthonous DOC has a significant effect on bacterioplankton communities especially in oligotrophic lakes. The genus Polynucleobacter was detected most frequently. The occurrence of Polynucleobacter species was positively associated with DOC and negatively associated with total phosphorus (TP) levels. In addition, TP had a stronger effect than DOC, suggesting that oligotrophy is the most important factor on the occurrence of this genus.     

The influence of habitat heterogeneity on freshwater bacterial community composition and dynamics

Multiple forces structure natural microbial communities, but the relative roles and interactions of these drivers are poorly understood. Gradients of physical and chemical parameters can be especially influential. In traditional ecological theory, variability in environmental conditions across space and time represents habitat heterogeneity, which may shape communities. Here we used aquatic microbial communities as a model to investigate the relationship between habitat heterogeneity and community composition and dynamics. We defined spatial habitat heterogeneity as vertical temperature and dissolved oxygen (DO) gradients in the water column, and temporal habitat heterogeneity as variation throughout the open-water season in these environmental parameters. Seasonal lake mixing events contribute to temporal habitat heterogeneity by destroying and re-creating these gradients. Because of this, we selected three lakes along a range of annual mixing frequency (polymictic, dimictic, meromictic) for our study. We found that bacterial community composition (BCC) was distinct between the epilimnion and hypolimnion within stratified lakes, and also more variable within the epilimnia through time. We found stark differences in patterns of epilimnion and hypolimnion dynamics over time and across lakes, suggesting that specific drivers have distinct relative importance for each community.     

Drivers of long‐term invertebrate community stability in changing Swedish lakes

Research on ecosystem stability has had a strong focus on local systems. However, environmental change often occurs slowly at broad spatial scales, which requires regional‐level assessments of long‐term stability. In this study, we assess the stability of macroinvertebrate communities across 105 lakes in the Swedish “lakescape.” Using a hierarchical mixed‐model approach, we first evaluate the environmental pressures affecting invertebrate communities in two ecoregions (north, south) using a 23 year time series (1995–2017) and then examine how a set of environmental and physical variables affect the stability of these communities. Results show that lake latitude, size, total phosphorus and alkalinity affect community composition in northern and southern lakes. We find that lake stability is affected by species richness and lake size in both ecoregions and alkalinity and total phosphorus in northern lakes. There is large heterogeneity in the patterns of community stability of individual lakes, but relationships between that stability and environmental drivers begin to emerge when the lakescape, composed of many discrete lakes, is the focal unit of study. The results of this study highlight that broad‐scale comparisons in combination with long time series are essential to understand the effects of environmental change on the stability of lake communities in space and time.     

Microcommunities and microgradients: Linking nutrient regeneration,microbial mutualism,and high sustained aquatic primary production

Nutrient regeneration is essential to sustained primary production in the aquatic environment because of coupled physical and metabolic gradients. The commonly evaluated ecosystem perspective of nutrient regeneration, as is illustrated among planktonic paradigms of lake ecosystems, functions only at macrotemporal and spatial scales. Most inland waters are small and shallow. Consequently, most organic matter of these waters is derived from photosynthesis of emergent, floating-leaved, and submersed higher plants and microflora associated with living substrata and detritus, including sediments, as well as terrestrial sources. The dominant primary productivity of inland aquatic ecosystems is not planktonic, but rather is associated with surfaces. The high sustained rates of primary production among sessile communities are possible because of the intensive internal recycling of nutrients, including carbon. Steep gradients exist within these attached microbial communities that (a) require rapid, intensive recycling of carbon, phosphorus, nitrogen, and other nutrients between producers, particulate and dissolved detritus, and bacteria and protists: (b) augment internal community recycling and losses with small external inputs of carbon and nutrients from the overlying water or from the supporting substrata; and (c) encourage maximal conservation of nutrients. Examples of microenvironmental recycling of carbon, phosphorus, and oxygen among epiphytic, epipelic, and epilithic communities are explained. Recalcitrant dissolved organic compounds from decomposition can serve both as carbon and energy substrates as well as be selectively inhibitory to microbial metabolism and nutrient recycling. Rapid recycling of nutrient and organic carbon within micro-environments operates at all levels, planktonic as well as attached, and is mandatory for high sustained productivity.     

Spatial scales of bacterial community diversity at cold seeps (Eastern Mediterranean Sea)

Cold seeps are highly productive, fragmented marine ecosystems that form at the seafloor around hydrocarbon emission pathways. The products of microbial utilization of methane and other hydrocarbons fuel rich chemosynthetic communities at these sites, with much higher respiration rates compared with the surrounding deep-sea floor. Yet little is known as to the richness, composition and spatial scaling of bacterial communities of cold seeps compared with non-seep communities. Here we assessed the bacterial diversity across nine different cold seeps in the Eastern Mediterranean deep-sea and surrounding seafloor areas. Community similarity analyses were carried out based on automated ribosomal intergenic spacer analysis (ARISA) fingerprinting and high-throughput 454 tag sequencing and were combined with in situ and ex situ geochemical analyses across spatial scales of a few tens of meters to hundreds of kilometers. Seep communities were dominated by Deltaproteobacteria, Epsilonproteobacteria and Gammaproteobacteria and shared, on average, 36% of bacterial types (ARISA OTUs (operational taxonomic units)) with communities from nearby non-seep deep-sea sediments. Bacterial communities of seeps were significantly different from those of non-seep sediments. Within cold seep regions on spatial scales of only tens to hundreds of meters, the bacterial communities differed considerably, sharing <50% of types at the ARISA OTU level. Their variations reflected differences in porewater sulfide concentrations from anaerobic degradation of hydrocarbons. This study shows that cold seep ecosystems contribute substantially to the microbial diversity of the deep-sea.     

Annual Patterns in Bacterioplankton Community Variability in a Humic Lake

Bacterioplankton community composition (BCC) was monitored in a shallow humic lake in northern Wisconsin, USA, over 3 years using automated ribosomal intergenic spacer analysis (ARISA). Comparison of ARISA profiles of bacterial communities over time indicated that BCC was highly variable on a seasonal and annual scale. Nonmetric multidimensional scaling (MDS) analysis indicated little similarity in BCC from year to year. Nevertheless, annual patterns in bacterioplankton community diversity were observed. Trends in bacterioplankton community diversity were correlated to annual patterns in community succession observed for phytoplankton and zooplankton populations, consistent with the notion that food web interactions affect bacterioplankton community structure in this humic lake. Bacterioplankton communities experience a dramatic drop in richness and abundance each year in early summer, concurrent with an increase in the abundance of both mixotrophic and heterotrophic flagellates. A second drop in richness, but not abundance, is observed each year in late summer, coinciding with an intense bloom of the nonphagotrophic dinoflagellate Peridinium limbatum. A relationship between bacterial community composition, size, and abundance and the population dynamics of Daphnia was also observed. The noted synchrony between these major population and species shifts suggests that linkages across trophic levels play a role in determining the annual time course of events for the microbial and metazoan components of the plankton.     

Characterization of Thrombolitic Bioherm Cyanobacterial Assemblages in a Meromictic Marl Lake (Fayetteville Green Lake,New York)

The Fayetteville Green Lake is a small (0.258 km²) meromictic marl lake that is host to a thrombolitic bioherm inhabited by coccoid and filamentous cyanobacteria. To date there has been only limited study of bioherm cyanobacterial community ecology, and none focusing on their molecular diversity. Samples of the bioherm were collected along vertical and spatial transects on a portion of the thrombolite in early fall 2010. Cyanobacterial assemblage spatial variability and operational taxonomic unit composition was analyzed by automated rRNA intergenic spacer analysis (ARISA). A total of 123 cyanobacterial ARISA operational taxonomic units were observed across all fingerprints. Cyanobacterial assemblages were variable across depth and spatial gradients, and may be structured by gradients in light availability and habitat stability. Cyanobacterial community fingerprints were more taxonomic unit rich, diverse, and had greater fingerprint similarity in deeper samples than those at the surface. Several operational taxonomic units were common to all samples taken, while the majority of assemblage components were heterogeneous between transects and depths. Hence, our results suggest that cyanobacterial communities on the thrombolite in Green Lake represent a mixture of taxa that are selected for by prevailing physicochemical conditions, while other taxa are selected for on spatial scales of meters and may represent more specialized cyanobacteria on the thrombolite. Moreover, our data suggest that the depth-dependent structure of bioherm cyanobacterial assemblages may be a consequence of habitat conditions, which may include light intensity and quality, temperature variation and habitat stability.     

Influence of dissolved organic matter source on lake bacterioplankton structure and function--implications for seasonal dynamics of community composition

It has been suggested that autochthonous (internally produced) organic carbon and allochthonous (externally produced) organic carbon are utilized by phylogenetically different bacterioplankton. We examined the relationship between the source of organic matter and the structure and function of lake bacterial communities. Differences and seasonal changes in bacterial community composition in two lakes differing in their source of organic matter were followed in relation to environmental variables. We also performed batch culture experiments with amendments of various organic substrates, namely fulvic acids, leachates from algae, and birch and maple leaves. Differences in bacterial community composition between the lakes, analysed by terminal restriction fragment length polymorphism, correlated with variables related to the relative loading of autochthonous and allochthonous carbon (water colour, dissolved organic carbon, nutrients, and pH). Seasonal changes correlated with temperature, chlorophyll and dissolved organic carbon in both lakes. The substrate amendments led to differences in both structure and function, i.e. production, respiration and growth yield, of the bacterial community. In conclusion, our results suggest that the source of organic matter influences community composition both within and among lakes and that there may be a coupling between the structure and function of the bacterial community.     

Scale-dependent effects of natural environmental gradients,industrial emissions and dispersal processes on zooplankton metacommunity structure: Implications for the bioassessment of boreal lakes

Environmental controls were traditionally considered as sole determinants of community assembly for freshwater bioassessment studies, whereas potential importance of dispersal processes and spatial scale have received limited attention. We conducted a bioassessment of lakes across northeast Alberta, Canada using crustacean zooplankton to develop a framework for evaluating if and how atmospheric emissions from the nearby Athabasca Oil Sands Region could impact their community assemblages. We quantified the effects of environmental gradients and spatially contingent dispersal processes for determining zooplankton community composition of 97 lakes at two spatial scales (regional and sub-regional) using constrained ordination, spatial modeling and variance partitioning techniques. Our findings indicated that effects of both environmental gradients and dispersal processes on species composition were scale-dependent. Zooplankton community composition was significantly correlated to environmental parameters that are directly and indirectly sensitive to industrial deposition including nitrate, sulphate, dissolved organic carbon, base cation, chloride, trace metal concentrations and predation regime, indicating their potential to track future environmental impacts. The relative importance of these environmental predictors varied with spatial scale, yet unraveling the effects of natural environmental heterogeneity vs. industrial deposition on this scale-dependency was not possible due to lack of regional baseline information. Dispersal processes were not important in shaping zooplankton communities at the sub-regional scale, but had limited, yet significant influence on species composition at the regional scale, emphasizing the need for cautious interpretation of broad-scale community patterns. Beyond establishing crucial regional baselines, our study highlights the necessity for explicit incorporation of dispersal effects and spatial scale in bioassessment of lakes across landscapes.     

Climate drivers of diatom distribution in shallow subarctic lakes

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Light and nutrient control phytoplankton biomass responses to global change in northern lakes

Global change affects terrestrial loadings of colored dissolved organic carbon (DOC) and nutrients to northern lakes. Still, little is known about how phytoplankton respond to changes in light and nutrient availability across gradients in lake DOC. In this study, we used results from whole‐lake studies in northern Sweden to show that annual mean phytoplankton biomass expressed unimodal curved relationships across lake DOC gradients, peaking at threshold DOC levels of around 11 mg/L. Whole‐lake single nutrient enrichment in selected lakes caused elevated biomass, with most pronounced effect at the threshold DOC level. These patterns give support to the suggested dual control by DOC on phytoplankton via nutrient (positively) and light (negatively) availability and imply that the lakes' location along the DOC axis is critical in determining to what extent phytoplankton respond to changes in DOC and/or nutrient loadings. By using data from the large Swedish Lake Monitoring Survey, we further estimated that 80% of northern Swedish lakes are below the DOC threshold, potentially experiencing increased phytoplankton biomass with browning alone, and/or combined with nutrient enrichment. The results support the previous model results on effects of browning and eutrophication on lake phytoplankton, and provide important understanding of how northern lakes may respond to future global changes.     

Links between Terrestrial Primary Production and Bacterial Production and Respiration in Lakes in a Climate Gradient in Subarctic Sweden

We compared terrestrial net primary production (NPP) and terrestrial export of dissolved organic carbon (DOC) with lake water heterotrophic bacterial activity in 12 headwater lake catchments along an altitude gradient in subarctic Sweden. Modelled NPP declined strongly with altitude and annual air temperature decreases along the altitude gradient (6°C between the warmest and the coldest catchment). Estimated terrestrial DOC export to the lakes was closely correlated to NPP. Heterotrophic bacterial production (BP) and respiration (BR) were mainly based on terrestrial organic carbon and strongly correlated with the terrestrial DOC export. Excess respiration over PP of the pelagic system was similar to net emission of CO₂ in the lakes. BR and CO₂ emission made up considerably higher shares of the terrestrial DOC input in warm lakes than in cold lakes, implying that respiration and the degree of net heterotrophy in the lakes were dependant not only on terrestrial export of DOC, but also on characteristics in the lakes which changed along the gradient and affected the bacterial metabolization of allochthonous DOC. The study showed close links between terrestrial primary production, terrestrial DOC export and bacterial activity in lakes and how these relationships were dependant on air temperature. Increases in air temperature in high latitude unproductive systems might have considerable consequences for lake water productivity and release of CO₂ to the atmosphere, which are ultimately determined by terrestrial primary production.     

Environmental rather than spatial factors structure bacterioplankton communities in shallow lakes along a > 6000 km latitudinal gradient in South America

Metacommunity studies on lake bacterioplankton indicate the importance of environmental factors in structuring communities. Yet most of these studies cover relatively small spatial scales. We assessed the relative importance of environmental and spatial factors in shaping bacterioplankton communities across a > 6000 km latitudinal range, studying 48 shallow lowland lakes in the tropical, tropicali (isothermal subzone of the tropics) and tundra climate regions of South America using denaturing gradient gel electrophoresis. Bacterioplankton community composition (BCC) differed significantly across regions. Although a large fraction of the variation in BCC remained unexplained, the results supported a consistent significant contribution of local environmental variables and to a lesser extent spatial variables, irrespective of spatial scale. Upon correction for space, mainly biotic environmental factors significantly explained the variation in BCC. The abundance of pelagic cladocerans remained particularly significant, suggesting grazer effects on bacterioplankton communities in the studied lakes. These results confirm that bacterioplankton communities are predominantly structured by environmental factors, even over a large‐scale latitudinal gradient (6026 km), and stress the importance of including biotic variables in studies that aim to understand patterns in BCC.