Persistent nitrogen limitation of stream biofilm communities along climate gradients in the Arctic

Climate change is rapidly reshaping Arctic landscapes through shifts in vegetation cover and productivity, soil resource mobilization, and hydrological regimes. The implications of these changes for stream ecosystems and food webs is unclear and will depend largely on microbial biofilm responses to concurrent shifts in temperature, light, and resource supply from land. To study those responses, we used nutrient diffusing substrates to manipulate resource supply to biofilm communities along regional gradients in stream temperature, riparian shading, and dissolved organic carbon (DOC) loading in Arctic Sweden. We found strong nitrogen (N) limitation across this gradient for gross primary production, community respiration and chlorophyll‐a accumulation. For unamended biofilms, activity and biomass accrual were not closely related to any single physical or chemical driver across this region. However, the magnitude of biofilm response to N addition was: in tundra streams, biofilm response was constrained by thermal regimes, whereas variation in light availability regulated this response in birch and coniferous forest streams. Furthermore, heterotrophic responses to experimental N addition increased across the region with greater stream water concentrations of DOC relative to inorganic N. Thus, future shifts in resource supply to these ecosystems are likely to interact with other concurrent environmental changes to regulate stream productivity. Indeed, our results suggest that in the absence of increased nutrient inputs, Arctic streams will be less sensitive to future changes in other habitat variables such as temperature and DOC loading.     

Kinetic modeling of phototrophic biofilms: the PHOBIA model

A kinetic model for mixed phototrophic biofilms is introduced, which focuses on the interactions between photoautotrophic, heterotrophic, and chemoautotrophic (nitrifying) functional microbial groups. Biofilm-specific phenomena are taken into account, such as extracellular polymeric substances (EPS) production by phototrophs as well as gradients of substrates and light in the biofilm. Acid-base equilibria, in particular carbon speciation, are explicitly accounted for, allowing for the determination of pH profiles across the biofilm. Further to previous models reported in literature, the PHOBIA model combines a number of kinetic mechanisms specific to phototrophic microbial communities, such as internal polyglucose storage under dynamic light conditions, phototrophic growth in the darkness using internally stored reserves, photoadaptation and photoinhibition, preference for ammonia over nitrate as N-source and the ability to utilize bicarbonate as a carbon source in the absence of CO(2). The sensitivity of the PHOBIA model to a number of key parameters is analyzed. An example on the potential use of phototrophic biofilms in wastewater polishing is discussed, where their performance is compared with conventional algal ponds. The PHOBIA model is presented in a manner that is compatible with other reference models in the area of water treatment. Its current version forms a theoretical base which is readily extendable once further experimental observations become available.     

Availability of glucose and light modulates the structure and function of a microbial biofilm

We have studied the differences in the organic matter processing and biofilm composition and structure between autoheterotrophic and heterotrophic biofilm communities. Microbial communities grown on artificial biofilms were monitored, following incubation under light and dark conditions and with or without the addition of glucose as a labile organic compound. Glucose addition greatly affected the microbial biofilm composition as shown by differences in 16S rRNA gene fingerprints. A significant increase in β-glucosidase and peptidase enzyme activities were also observed in glucose-amended biofilms incubated in the dark, suggesting an active bacterial community. Light enhanced the algal and bacterial growth, as well as higher extracellular enzyme activity, thereby indicating a tight algal–bacterial coupling in biofilms incubated under illumination. In these biofilms, organic compounds excreted by photosynthetic microorganisms were readily available for bacterial heterotrophs. This algal–bacterial relationship weakened in glucose-amended biofilms grown in the light, probably because heterotrophic bacteria preferentially use external labile compounds. These results suggest that the availability of labile organic matter in the flowing water and the presence of light may alter the biofilm composition and function, therefore affecting the processing capacity of organic matter in the stream ecosystem.     

Shifts in microbial community structure and function in light‐ and dark‐grown biofilms driven by warming

Biofilms are dynamic players in biogeochemical cycling in running waters and are subjected to environmental stressors like those provoked by climate change. We investigated whether a 2°C increase in flowing water would affect prokaryotic community composition and heterotrophic metabolic activities of biofilms grown under light or dark conditions. Neither light nor temperature treatments were relevant for selecting a specific bacterial community at initial phases (7‐day‐old biofilms), but both variables affected the composition and function of mature biofilms (28‐day‐old). In dark‐grown biofilms, changes in the prokaryotic community composition due to warming were mainly related to rotifer grazing, but no significant changes were observed in functional fingerprints. In light‐grown biofilms, warming also affected protozoan densities, but its effect on prokaryotic density and composition was less evident. In contrast, heterotrophic metabolic activities in light‐grown biofilms under warming showed a decrease in the functional diversity towards a specialized use of several carbohydrates. Results suggest that prokaryotes are functionally redundant in dark biofilms but functionally plastic in light biofilms. The more complex and self‐serving light‐grown biofilm determines a more buffered response to temperature than dark‐grown biofilms. Despite the moderate increase in temperature of only 2°C, warming conditions drive significant changes in freshwater biofilms, which responded by finely tuning a complex network of interactions among microbial populations within the biofilm matrix.     

Light availability affects stream biofilm bacterial community composition and function,but not diversity

Changes in riparian vegetation or water turbidity and browning in streams alter the local light regime with potential implications for stream biofilms and ecosystem functioning. We experimented with biofilms in microcosms grown under a gradient of light intensities (range: 5–152 μmole photons s^?1 m^?2) and combined 454‐pyrosequencing and enzymatic activity assays to evaluate the effects of light on biofilm structure and function. We observed a shift in bacterial community composition along the light gradient, whereas there was no apparent change in alpha diversity. Multifunctionality, based on extracellular enzymes, was highest under high light conditions and decoupled from bacterial diversity. Phenol oxidase activity, involved in the degradation of polyphenolic compounds, was twice as high on average under the lowest compared with the highest light condition. This suggests a shift in reliance of microbial heterotrophs on biofilm phototroph‐derived organic matter under high light availability to more complex organic matter under low light. Furthermore, extracellular enzyme activities correlated with nutrient cycling and community respiration, supporting the link between biofilm structure–function and biogeochemical fluxes in streams. Our findings demonstrate that changes in light availability are likely to have significant impacts on biofilm structure and function, potentially affecting stream ecosystem processes.     

Nutritional relationships among microorganisms in an epilithic biofilm community

Previous studies of an epilithic algal-bacterial community in a pristine mountain stream suggested that heterotrophic bacteria were responding to the metabolic activities of the phototrophic population. Subsequent studies were performed to follow the flow of labeled carbon, from its initial inorganic form, through the trophic levels of the mat community. A majority of primary production metabolites were excreted by the algal population during active growth; this shifted to an incorporation into cellular material as phototrophic activity declined. Results suggest that there was a direct flux of soluble algal products to the bacterial population, with little heterotrophic utilization of dissolved organics from the overlying stream water. Both phototrophic productivity and bacterial utilization of algal products peaked at approximately the same time of year. Activity of the diatom-dominated algal population declined as silica concentrations in the stream water dropped, leading to a situation in which the sessile bacteria were substrate limited. These events resulted in an almost complete disappearance of the community in early September.     

In situ light and phosphorus manipulations reveal potential role of biofilm algae in enhancing enzyme‐mediated decomposition of organic matter in streams

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Nitrogen limitation of heterotrophic biofilms in boreal streams

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Phototrophic biofilms and their potential applications

Phototrophic biofilms occur on surfaces exposed to light in a range of terrestrial and aquatic environments. Oxygenic phototrophs like diatoms, green algae, and cyanobacteria are the major primary producers that generate energy and reduce carbon dioxide, providing the system with organic substrates and oxygen. Photosynthesis fuels processes and conversions in the total biofilm community, including the metabolism of heterotrophic organisms. A matrix of polymeric substances secreted by phototrophs and heterotrophs enhances the attachment of the biofilm community. This review discusses the actual and potential applications of phototrophic biofilms in wastewater treatment, bioremediation, fish-feed production, biohydrogen production, and soil improvement.     

Influence of dissolved organic matter and inorganic nutrients on the biofilm bacterial community on artificial substrates in a northeastern Ohio, USA, stream

Stream bacteria may be influenced by the composition and availability of dissolved organic matter (DOM) and inorganic nutrients, but knowledge about how individual phylogenetic groups in biofilm are affected is still limited. In this study, the influence of DOM and inorganic nutrients on stream biofilm bacteria was examined. Biofilms were developed on artificial substrates (unglazed ceramic tiles) for 21 days in a northeastern Ohio (USA) stream for five consecutive seasons. Then, the developed biofilm assemblages were exposed, in the laboratory, to DOM (glucose, leaf leachate, and algal exudates) and inorganic nutrients (nitrate, phosphate, and nitrate and phosphate in combination) amendments for 6 days. Bacterial numbers in the biofilms were generally higher in response to the DOM treatments than to the inorganic nutrient treatments. There were also apparent seasonal variations in the response patterns of the individual bacterial taxa to the nutrient treatments; an indication that limiting resources to bacteria in stream biofilms may change over time. Overall, in contrast to the other treatments, bacterial abundance was generally highest in response to the low-molecular-weight DOM (i.e., glucose) treatment. These results further suggest that there are interactions among the different bacterial groups in biofilms that are impacted by the associated nutrient dynamics among seasons in stream ecosystems.     

Seasonal determinations of extracellular hydrolytic activities in heterotrophic and mixed heterotrophic/autotrophic biofilms from two contrasting rivers

The temporal changes in extracellular enzyme activities in freshwater microbial biofilms were examined in two contrasting river sites in North Wales over a 12 month period. Sites were a first order, unshaded oligotrophic upland stream (Nant Waen) and a fourth order, mildly eutrophic river with riparian tree cover (River Clywedog). When algal populations were low, biofilms of the more eutrophic site supported greater enzyme activities and higher population densities than the oligotrophic site. Composition, concentration and origin of substrates available to the respective biofilm communities influenced extracellular processing patterns. Reduction in algal populations depressed total and extracellular activities in biofilms from the first order site, suggesting that biofilm communities here were maintained by in situ primary production. Biofilms from Nant Waen were often found to contain higher extracellular activities per cell than the more eutrophic River Clywedog biofilms, which might represent the enhanced ability of an oligotrophic biofilm to accumulate extracellular enzymes. In contrast, light and darkgrown River Clywedog biofilms were not enzymatically distinct, inferring a less important role for biofilm phototrophs. Some evidence was found for increased reliance on allochthonous substrates in the River Clywedog for biofilm maintenance.     

Do leaf-litter decomposers control biofilm primary production and benthic algal community structure in forest streams? Insights from an outdoor mesocosm experiment

• 1. Forested headwater streams are generally considered to be light-limited ecosystems where primary production is reduced, and the main source of energy and nutrients is composed of allochthonous detritus. We hypothesised that in these ecosystems, the development of primary producers might also be limited by (1) competition for nutrients with leaf-litter decomposers (e.g. bacteria and fungi), and (2) leaf-litter leachates or allelopathic compounds produced by aquatic fungi.
• 2. To test these hypotheses, a 48-day mesocosm experiment was performed in 12 artificial streams containing stream water inoculated with epilithic biofilm suspensions collected from a forested headwater stream. Three different treatments were applied: control without leaf litter (C), microbially conditioned leaf litter added at the beginning of the experiment and left to decompose throughout the experiment (L), or leaf litter renewed three times during the experiment (RL).
• 3. We predicted that (1) the presence of litter, through microbial nutrient immobilisation and allelopathy, would reduce primary production and that (2) this effect would be amplified by litter renewal. We also predicted that nutrient competition would mean that (3) leaf-litter decomposers will alter primary producer community composition and physiology. These predictions were tested by analysing biofilm development, physiology, stoichiometry, and benthic algal community structure. To distinguish between the effects of nutrient immobilisation and allelopathy, the biofilm responses to leaf-litter leachates collected after different microbial conditioning durations were also measured in a parallel laboratory experiment.
• 4. Contrary to our expectations, by day 28, primary producer growth was higher in the mesocosms containing leaf litter (L and RL) despite the rapid decrease in dissolved nutrients when leaf litter was present. After 48 days, the lowest phototrophic biofilm development was observed when leaf litter was renewed (RL), whereas phototrophic biofilm development was similar in the C and L treatments. Biofilm stoichiometry indicated that this effect was most probably related to greater nitrogen limitation in the RL treatment. The presence of leaf litter also affected primary producers' photophysiology, which could be attributed to changes in taxonomic composition and to physiological adjustments of primary producers.
• 5. Laboratory measurements showed that despite a strong inhibition of primary producer growth by unconditioned leaf-litter leachates, microbially conditioned leaf litter had either low or no effects on the development of primary producers.
• 6. These results reveal that leaf-litter decomposers can have both positive and negative effects on primary producers underlining the need to consider microbial interactions when investigating the functioning of forested headwater streams.

     

Urban infrastructure influences dissolved organic matter quality and bacterial metabolism in an urban stream network

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Light availability regulates the response of algae and heterotrophic bacteria to elevated nutrient levels and warming in a northern boreal peatland

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Nutrient limitation of epilithic and epixylic biofilms in ten North American streams

1. Nutrient diffusing substrata were used to determine the effect of added inorganic nitrogen (N) and phosphorus (P) on the development of epilithic and epixylic biofilms in 10 North American streams. Four treatments of diffusing substrata were used: Control (agar only), N addition (0.5 m NaNO₃), P addition (0.5 m KH₂PO₄), and N + P combined (0.5 m NaNO₃ + 0.5 m KH₂PO₄). Agar surfaces were covered with glass fibre filters (for epilithon) or discs of untreated white oak wood veneer (for epixylon). 2. We found that if algae showed significant response to nutrient addition, N limitation (either N alone or N with P) was the most frequent response both on GF/F filters and on wood. Despite the low dissolved nutrient concentrations in our study streams, more than a third of the streams did not show any response to N or P addition. In fact, P was never the sole limiting nutrient for algal biofilms in this study. 3. Nutrient addition influenced algal colonisation of inorganic versus organic substrata in different ways. The presence of other biofilm constituents (e.g. fungi or bacteria) may influence whether algal biomass on wood increased in response to nutrient addition. Algae on organic and inorganic substrata responded similarly to nutrient addition in only one stream. 4. Fungal biomass on wood was nutrient limited in six of 10 study streams. N limitation of fungal biomass (with or without secondary P limitation) was most frequent, but P limitation did occur in two streams. 5. Our results show that biomass responses to nutrient addition by the heterotrophic and autotrophic components of the epixylic biofilm were different, though both experienced the same stream nutrient conditions. For algae and fungi growing on wood, limiting nutrients were rarely similar. Only three of nine streams showed the same biomass response to nutrient addition, including two that showed no significant change in biomass despite added nutrients.     

Biofilm formation at warming temperature: acceleration of microbial colonization and microbial interactive effects

River biofilms that grow on wet benthic surface are mainly composed of bacteria, algae, cyanobacteria and protozoa embedded in a polysaccharide matrix. The effects of increased river water temperature on biofilm formation were investigated. A laboratory experiment was designed employing two temperatures (11.1-13.2°C, night-day; 14.7-16.0°C, night-day) and two nutrient levels (0.054 mg P l(-1), 0.75 mg N l(-1); 0.54 mg P l(-1), 7.5 mg N l(-1)). Biofilm formation at the higher temperature was faster, while the biomass of the mature biofilm was mainly determined by nutrient availability. The specific response of the three microbial groups that colonized the substrata (algae, bacteria and ciliates) was modulated by interactions between them. The greater bacterial growth rate and earlier bacterial colonization at the higher temperature and higher nutrient status was not translated into the accrual of higher bacterial biomass. This may result from ciliates grazing on the bacteria, as shown by an earlier increase in peritrichia at higher temperatures, and especially at high nutrient conditions. Temperature and ciliate grazing might determine the growth of a distinctive bacterial community under warming conditions. Warmer conditions also produced a thicker biofilm, while functional responses were much less evident (increases in the heterotrophic utilization of polysaccharides and peptides, but no increase in primary production and respiration). Increasing the temperature of river water might lead to faster biofilm recolonization after disturbances, with a distinct biofilm community structure that might affect the trophic web. Warming effects would be expected to be more relevant under eutrophic conditions.     

The role of micro-organisms in the ecological connectivity of running waters

1. Riparian zones hold a central place in the hydrological cycle, owing to the prevalence of surface and groundwater interactions. In riparian transition zones, the quality of exfiltrating water is heavily influenced by microbial activities within the bed sediments. This paper reviews the role of micro-organisms in biogeochemical cycling in the riparian-hyporheic ecotone. 2. The production of organic substances, such as cellulose and lignin, by riparian vegetation is an important factor influencing the pathways of microbial processing in the riparian zone. For example, anaerobic sediment patches, created by entrainment of allochthonous organic matter, are focal sites of microbial denitrification. 3. The biophysical structure of the riparian zone largely influences in-stream microbial transformations through the retention of organic matter. Particulate and dissolved organic matter (POM and DOM) is retained effectively in the hyporheic zone, which drives biofilm development and associated microbial activity. 4. The structure of the riparian zone, the mechanisms of POM retention, the hydrological linkages to the stream and the intensity of key biogeochemical processes vary greatly along the river continuum and in relation to the geomorphic setting. However, the present state of knowledge of organic matter metabolism in the hyporheic zone suggests that lateral ecological connectivity is a basic attribute of lotic ecosystems. 5. Due to their efficiency in transforming POM into heterotrophic microbial biomass, attached biofilms form an abundant food resource for an array of predators and grazers in the interstitial environments of rivers and streams. The interstitial microbial loop, and the intensity of microbial production within the bed sediments, may be a primary driver of the celebrated high productivity and biodiversity of the riparian zone. 6. New molecular methods based on the analysis of the low molecular weight RNA (LMW RNA) allow unprecedented insights into the community structure of natural bacterial assemblages and also allow identification and study of specific strains hitherto largely unknown. 7. Research is needed on the development and evaluation of sampling methods for interstitial micro-organisms, on the characterization of biofilm structure, on the analysis of the biodegradable matter in the riparian-hyporheic ecotone, on the regulation mechanisms exerted on microbiota by interstitial predators and grazers, and on measures of microbial respiration and other key activities that influence biogeochemical cycles in running waters. 8. Past experiences from large-scale alterations of riparian zones by humans, such as the River Rhine in central Europe, undeniably demonstrate the detrimental consequences of disconnecting rivers from their riparian zones. A river management approach that uses the natural services of micro-organisms within intact riparian zones could substantially reduce the costs of clean, sustainable water supplies for humans.     

The quality of organic matter mediates the response of heterotrophic biofilms to phosphorus enrichment of the water column and substratum

1. Heterotrophic biofilms are important drivers of community respiration, nutrient cycling and decomposition of organic matter in stream ecosystems. Both organic matter quality and nutrient levels have been shown to affect biofilm biomass and activity individually, but both factors have rarely been manipulated simultaneously. 2. To experimentally manipulate the organic matter quality and phosphorus (P) levels of both the substratum and water column, we first used cellulose cloth as a low‐quality organic material and enhanced its quality and P‐content by amending the underlying agar with maltose and P, respectively (Experiment I). To manipulate water column P, artificial substrata were incubated in low‐ and high‐P sites of a whole‐stream P‐enrichment in lowland Costa Rica. 3. Results from Experiment I suggest that heterotrophic biofilm respiration on cellulose cloth is co‐limited by carbon (C) and P. Biofilm respiration responded in an additive manner to combined effects of maltose and P‐enrichment of water column and synergistically to maltose and high‐P in substrata. 4. As decomposing organic matter that supports heterotrophic biofilms varies naturally in its labile C content along with other physical and chemical properties, we conducted a second experiment (Experiment II) in which we amended leaf discs from two species (Trema integerrima, a labile C source and Zygia longifolia, a recalcitrant C source) with maltose. We incubated the substrata in low‐ and high‐P sites of the P‐enrichment stream. 5. Results from Experiment II indicate that biofilm respiration on a labile C source (Trema) was not C‐limited, while biofilm respiration on a recalcitrant C source (Zygia) was C‐limited. Phosphorus stimulated the biofilm respiration and breakdown rate on Trema, but not on Zygia, supporting the hypothesis that the stimulatory effect of P‐enrichment is dependent on the availability of labile C in decomposing leaves. 6. Our results suggest that the interactive effects of organic matter quality and nutrient loading of streams can significantly increase microbial biofilm activity, potentially altering the trophic base of stream food webs. Researchers should consider both the organic matter quality and the enrichment of both water column and substrata to better predict the effects of anthropogenic nutrient loading to stream the ecosystems.