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Microbes play a critical role in plant litter decomposition and influence the fate of carbon in rivers and riparian zones. When decomposing low-nutrient plant litter, microbes acquire nitrogen (N) and phosphorus (P) from the environment (i.e., nutrient immobilization), and this process is potentially sensitive to nutrient loading and changing climate. Nonetheless, environmental controls on immobilization are poorly understood because rates are also influenced by plant litter chemistry, which is coupled to the same environmental factors. Here we used a standardized, low-nutrient organic matter substrate (cotton strips) to quantify nutrient immobilization at 100 paired stream and riparian sites representing 11 biomes worldwide. Immobilization rates varied by three orders of magnitude, were greater in rivers than riparian zones, and were strongly correlated to decomposition rates. In rivers, P immobilization rates were controlled by surface water phosphate concentrations, but N immobilization rates were not related to inorganic N. The N:P of immobilized nutrients was tightly constrained to a molar ratio of 10:1 despite wide variation in surface water N:P. Immobilization rates were temperature-dependent in riparian zones but not related to temperature in rivers. However, in rivers nutrient supply ultimately controlled whether microbes could achieve the maximum expected decomposition rate at a given temperature. Collectively, we demonstrated that exogenous nutrient supply and immobilization are critical control points for decomposition of organic matter. Key Points • Nitrogen (N) and phosphorus (P) immobilization was measured on organic matter (cotton) in 100 rivers and riparian zones representing 11 biomes • Elevated temperature in riparian zones and phosphate in rivers increased immobilization, and consequently accelerated decomposition • N and P immobilization was strongly linked by microbial stoichiometry despite widely varied surface-water nutrient ratios Plain Language Summary Bacteria and fungi contribute to the breakdown of leaf litter in rivers and floodplains. To break down leaf litter, these microbes need the nutrients nitrogen and phosphorus (P), and microbes can get nutrients either from the leaf litter itself or from the environment. Most leaf litter has low nutrient content and microbes must rely on the environment to supply nutrients. We studied microbial nutrient uptake from the environment during litter breakdown to determine whether it varies predictably across the globe and how it is influenced by changing climate and nutrient pollution. In 100 rivers and floodplains in 11 of Earth's major biomes we placed small strips of cotton as stand-ins for leaf litter. Nutrient uptake was consistently greater on cotton strips that were submerged in the river compared to cotton on the floodplain. For microbes in the river, nutrient uptake was faster in instances where there was more P in the water. For microbes in the floodplain, nutrient uptake was faster where temperatures were warmer. Faster nutrient uptake by microbes was linked with faster cotton breakdown in rivers and floodplains. Our study shows that climate change and nutrient pollution can alter the activity of microbes in rivers and floodplains.

Elevated atmospheric carbon dioxide (CO2) concentration, rising water temperatures, and intensification of hydrologic regimes are characteristics of global climate change that affect rates of leaf litter decomposition in lotic ecosystems. Predicted effects of elevated atmospheric CO2 concentration and elevated temperature negate each other. However, a recent meta-analysis found no effect of elevated atmospheric CO2 on decomposition, while temperature consistently stimulates rates of decomposition. The sensitivity of litter decomposition to shifts in temperature is less clear due to methodological differences between studies calculating the apparent activation energy of decomposition and the multitude of biotic and abiotic variables that enhance or mitigate the effect of temperature. Both floods and droughts are becoming more frequent features of hydrologic regimes, but spatial and temporal variation in hydrologic intensification adds further challenge for predicting how climate change will alter decomposition rates. Despite these complexities, it is clear that altered rates of litter decomposition have cascading influence on the global C budget and food web dynamics. Thus, improved understanding of the individual and interactive effects of elevated atmospheric CO2 concentration, warming, and shifting hydrology on decomposition rates remains a vital research need.

Anthropogenic increases in nitrogen (N) and phosphorus (P) concentrations can strongly influence the structure and function of ecosystems. Even though lotic ecosystems receive cumulative inputs of nutrients applied to and deposited on land, no comprehensive assessment has quantified nutrient-enrichment effects within streams and rivers. We conducted a meta-analysis of published studies that experimentally increased concentrations of N and/or P in streams and rivers to examine how enrichment alters ecosystem structure (state: primary producer and consumer biomass and abundance) and function (rate: primary production, leaf breakdown rates, metabolism) at multiple trophic levels (primary producer, microbial heterotroph, primary and secondary consumers, and integrated ecosystem). Our synthesis included 184 studies, 885 experiments, and 3497 biotic responses to nutrient enrichment. We documented widespread increases in organismal biomass and abundance (mean response = +48%) and rates of ecosystem processes (+54%) to enrichment across multiple trophic levels, with no large differences in responses among trophic levels or between autotrophic or heterotrophic food-web pathways. Responses to nutrient enrichment varied with the nutrient added (N, P, or both) depending on rate versus state variable and experiment type, and were greater in flume and whole-stream experiments than in experiments using nutrient-diffusing substrata. Generally, nutrient-enrichment effects also increased with water temperature and light, and decreased under elevated ambient concentrations of inorganic N and/or P. Overall, increased concentrations of N and/or P altered multiple food-web pathways and trophic levels in lotic ecosystems. Our results indicate that preservation or restoration of biodiversity and ecosystem functions of streams and rivers requires management of nutrient inputs and consideration of multiple trophic pathways.

The carbon use efficiency (CUE) of microbial communities partitions the flow of C from primary producers to the atmosphere, decomposer food webs, and soil C stores. CUE, usually defined as the ratio of growth to assimilation, is a critical parameter in ecosystem models, but is seldom measured directly in soils because of the methodological difficulty of measuring in situ rates of microbial growth and respiration. Alternatively, CUE can be estimated indirectly from the elemental stoichiometry of organic matter and microbial biomass, and the ratios of C to nutrient-acquiring ecoenzymatic activities. We used this approach to estimate and compare microbial CUE in >2000 soils from a broad range of ecosystems. Mean CUE based on C:N stoichiometry was 0.269 ± 0.110 (mean ± SD). A parallel calculation based on C:P stoichiometry yielded a mean CUE estimate of 0.252 ± 0.125. The mean values and frequency distributions were similar to those from aquatic ecosystems, also calculated from stoichiometric models, and to those calculated from direct measurements of bacterial and fungal growth and respiration. CUE was directly related to microbial biomass C with a scaling exponent of 0.304 (95% CI 0.237–0.371) and inversely related to microbial biomass P with a scaling exponent of −0.234 (95% CI −0.289 to −0.179). Relative to CUE, biomass specific turnover time increased with a scaling exponent of 0.509 (95% CI 0.467–0.551). CUE increased weakly with mean annual temperature. CUE declined with increasing soil pH reaching a minimum at pH 7.0, then increased again as soil pH approached 9.0, a pattern consistent with pH trends in the ratio of fungal : bacteria abundance and growth. Structural equation models that related geographic variables to CUE component variables showed the strongest connections for paths linking latitude and pH to β-glucosidase activity and soil C:N:P ratios. The integration of stoichiometric and metabolic models provides a quantitative description of the functional organization of soil microbial communities that can improve the representation of CUE in microbial process and ecosystem simulation models.

Microbial community metabolism relies on external digestion, mediated by extracellular enzymes that break down complex organic matter into molecules small enough for cells to assimilate. We analyzed the kinetics of 40 extracellular enzymes that mediate the degradation and assimilation of carbon, nitrogen and phosphorus by diverse aquatic and terrestrial microbial communities (1160 cases). Regression analyses were conducted by habitat (aquatic and terrestrial), enzyme class (hydrolases and oxidoreductases) and assay methodology (low affinity and high affinity substrates) to relate potential reaction rates to substrate availability. Across enzyme classes and habitats, the scaling relationships between apparent Vmax and apparent Km followed similar power laws with exponents of 0.44 to 0.67. These exponents, called elasticities, were not statistically distinct from a central value of 0.50, which occurs when the Km of an enzyme equals substrate concentration, a condition optimal for maintenance of steady state. We also conducted an ecosystem scale analysis of ten extracellular hydrolase activities in relation to soil and sediment organic carbon (2,000–5,000 cases/enzyme) that yielded elasticities near 1.0 (0.9 ± 0.2, n = 36). At the metabolomic scale, the elasticity of extracellular enzymatic reactions is the proportionality constant that connects the C:N:P stoichiometries of organic matter and ecoenzymatic activities. At the ecosystem scale, the elasticity of extracellular enzymatic reactions shows that organic matter ultimately limits effective enzyme binding sites. Our findings suggest that one mechanism by which microbial communities maintain homeostasis is regulating extracellular enzyme expression to optimize the short-term responsiveness of substrate acquisition. The analyses also show that, like elemental stoichiometry, the fundamental attributes of enzymatic reactions can be extrapolated from biochemical to community and ecosystem scales.

Riparian ecosystems support mosaics of terrestrial and aquatic plant species that enhance regional biodiversity and provide important ecosystem services to humans. Species composition and the distribution of functional traits – traits that define species in terms of their ecological roles – within riparian plant communities are rapidly changing in response to various global change drivers. Here, we present a conceptual framework illustrating how changes in dependent wildlife communities and ecosystem processes can be predicted by examining shifts in riparian plant functional trait diversity and redundancy (overlap). Three widespread examples of altered riparian plant composition are: shifts in the dominance of deciduous and coniferous species; increases in drought-tolerant species; and the increasing global distribution of plantation and crop species. Changes in the diversity and distribution of critical plant functional traits influence terrestrial and aquatic food webs, organic matter production and pro...

The net primary production of the biosphere is consumed largely by microorganisms, whose metabolism creates the trophic base for detrital foodwebs, drives element cycles, and mediates atmospheric composition. Biogeochemical constraints on microbial catabolism, relative to primary production, create reserves of detrital organic carbon in soils and sediments that exceed the carbon content of the atmosphere and biomass. The production of organic matter is an intracellular process that generates thousands of compounds from a small number of precursors drawn from intermediary metabolism. Osmotrophs generate growth substrates from the products of biosynthesis and diagenesis by enzyme-catalyzed reactions that occur largely outside cells. These enzymes, which we define as ecoenzymes, enter the environment by secretion and lysis. Enzyme expression is regulated by environmental signals, but once released from the cell, ecoenzymatic activity is determined by environmental interactions, represented as a kinetic cascade, that lead to multiphasic kinetics and large spatiotemporal variation. At the ecosystem level, these interactions can be viewed as an energy landscape that directs the availability and flow of resources. Ecoenzymatic activity and microbial metabolism are integrated on the basis of resource demand relative to environmental availability. Macroecological studies show that the most widely measured ecoenzymatic activities have a similar stoichiometry for all microbial communities. Ecoenzymatic stoichiometry connects the elemental stoichiometry of microbial biomass and detrital organic matter to microbial nutrient assimilation and growth. We present a model that combines the kinetics of enzyme activity and community growth under conditions of multiple resource limitation with elements of metabolic and ecological stoichiometry theory. This biogeochemical equilibrium model provides a framework for comparative studies of microbial community metabolism, the principal driver of biogeochemical cycles.

The kinetics and elemental composition of cellular units that mediate production and respiration are the basis for the metabolic and stoichiometric theories of ecological organization. This theoretical framework extends to the activities of microbial enzymes released into the environment (ecoenzymes) that mediate the release of assimilable substrate from detrital organic matter. In this paper, we analyze the stoichiometry of ecoenzymatic activities in the surface sediments of lotic ecosystems and compare those results to the stoichiometry observed in terrestrial soils. We relate these ecoenzymatic ratios to energy and nutrient availability in the environment as well as microbial elemental content and growth efficiency. The data, collected by US Environmental Protection Agency, include the potential activities of 11 enzymes for 2,200 samples collected across the US, along with analyses of sediment C, N and P content. On average, ecoenzymatic activities in stream sediments are 2–5 times greater per gC than those of terrestrial soils. Ecoenzymatic ratios of C, N and P acquisition activities support elemental analyses showing that microbial metabolism is more likely to be C-limited than N or P-limited compared to terrestrial soils. Ratios of hydrolytic to oxidative activities indicate that sediment organic matter is more labile than soil organic matter and N acquisition is less dependent on humic oxidation. The mean activity ratios of glycosidases and aminopeptidases reflect the environmental abundance of their respective substrates. For both freshwater sediments and terrestrial soils, the mean C:nutrient ratio of microbial biomass normalized to growth efficiency approximates the mean ecoenzymatic C:nutrient activity ratios normalized to environmental C:nutrient abundance. This relationship defines a condition for biogeochemical equilibrium consistent with stoichiometric and metabolic theory.

The flow of carbon and nutrients from plant production into detrital food webs is mediated by microbial enzymes released into the environment (ecoenzymes). Ecoenzymatic activities are linked to both microbial metabolism and environmental resource availability. In this paper, we extend the theoretical and empirical framework for ecoenzymatic stoichiometry from nutrient availability to carbon composition by relating ratios of β-1,4-glucosidase (BG), acid (alkaline) phosphatase (AP), β-N-acetylglucosaminidase (NAG), leucine aminopeptidase (LAP) and phenol oxidase (POX) activities in soils to measures of organic matter recalcitrance, using data from 28 ecosystems. BG and POX activities are uncorrelated even though both are required for lignocellulose degradation. However, the ratio of BG:POX activity is negatively correlated with the relative abundance of recalcitrant carbon. Unlike BG, POX activity is positively correlated with (NAG + LAP) and AP activities. We propose that the effect of organic matter recalcitrance on microbial C:N and C:P threshold element ratios (TER) can be represented by normalizing BG, AP and (NAG + LAP) activities to POX activity. The scaling relationships among these ratios indicate that the increasing recalcitrance of decomposing organic matter effectively reverses the growth rate hypothesis of stoichiometric theory by decreasing carbon and nutrient availability and slowing growth, which increases TERN:P. This effect is consistent with the narrow difference between the mean elemental C:N ratios of soil organic matter and microbial biomass and with the inhibitory effect of N enrichment on rates of decomposition and microbial metabolism for recalcitrant organic matter. From these findings, we propose a conceptual framework for bottom-up decomposition models that integrate the stoichiometry of ecoenzymatic activities into general theories of ecology.

Biota can be described in terms of elemental composition, expressed as an atomic ratio of carbon:nitrogen:phosphorus (refs 1-3). The elemental stoichiometry of microoorganisms is fundamental for understanding the production dynamics and biogeochemical cycles of ecosystems because microbial biomass is the trophic base of detrital food webs. Here we show that heterotrophic microbial communities of diverse composition from terrestrial soils and freshwater sediments share a common functional stoichiometry in relation to organic nutrient acquisition. The activities of four enzymes that catalyse the hydrolysis of assimilable products from the principal environmental sources of C, N and P show similar scaling relationships over several orders of magnitude, with a mean ratio for C:N:P activities near 1:1:1 in all habitats. We suggest that these ecoenzymatic ratios reflect the equilibria between the elemental composition of microbial biomass and detrital organic matter and the efficiencies of microbial nutrient assimilation and growth. Because ecoenzymatic activities intersect the stoichiometric and metabolic theories of ecology, they provide a functional measure of the threshold at which control of community metabolism shifts from nutrient to energy flow.

Restoration activity has exponentially increased across the Southwest since 1990. Over 37,000 records were compiled into the National River Restoration Science Synthesis (NRRSS) database to summarize restoration trends and assess project effectiveness. We analyzed data from 576 restoration projects in the Southwest (NRRSS-SW). More than 50% of projects were less than or equal to 3 km in length. The most common restoration project intent categories were riparian management, water quality management, in-stream habitat improvement, and flow modification. Common project activities were well matched to goals. Conservative estimates of total restoration costs exceeded $500 million. Most restoration dollars have been allocated to flow modification and water quality management. Monitoring was linked to 28% of projects across the Southwest, as opposed to just 10% nationwide. Mean costs were statistically similar whether or not projects were monitored. Results from 48 telephone interviews provided validation of NRRSS-SW database analyses but showed that project costs are often underreported within existing datasets. The majority of interviewees considered their projects to be successful, most often based upon observed improvements to biota or positive public reaction rather than evaluation of field data. The efficacy of restoration is difficult to ascertain given the dearth of information contained within most datasets. There is a great need for regional entities that not only track information on project implementation but also maintain and analyze monitoring data associated with restoration. Agencies that fund or regulate restoration should reward projects that emphasize monitoring and evaluation as much as project implementation.

The study of metabolic scaling in stream ecosystems is complicated by their openness to external resource inputs. For heterotrophic bacteria, which are a large component of stream metabolism, it may be possible to integrate the effects of resource availability and temperature on production using metabolic scaling theory and the kinetics of extracellular enzyme activity (EEA) associated with the degradation of major nutrient pools. With this goal, we analyzed previously published data on EEA and bacterial production for two rivers in northwestern Ohio, USA. The EEA data included estimates of apparent Vmax, a measure of catalytic capacity, and apparent Km, a measure of available substrate concentration, for six extracellular enzymes (alpha-glucosidase, beta-glucosidase, aminopeptidase, protease, phosphatase, and acetyl esterase). Sampling was done over an annual cycle with a temperature range of 4 31 degrees C, while EEA assays were conducted at 20 degrees C. The EEA kinetic measures were scaled to ambient stream temperature using an activation energy (Ea) of 0.5 eV (8.01 x 10(-20) J) and converted to estimates of the turnover rate (St) of their associated substrate pools. The St values associated with protein utilization, the largest substrate pool, had the strongest relationship to bacterial production (r2 = 0.49-0.52); those for carbohydrate utilization, the smallest substrate pool, had the weakest (r2= 0.09-0.15). Comparisons of apparent Ea over the annual cycle showed that the trophic basis of bacterial production switched from relatively high carbohydrate consumption in autumn and winter to relatively high protein consumption in spring and summer, corresponding to seasonal dynamics in plant litter inputs and algal production, respectively. Over the annual cycle, the summed substrate generation rate of the six enzymes was similar in magnitude and strongly correlated with bacterial production (r2 = 0.56). This approach combines effects of substrate pool size, catalytic capacity, and temperature on bacterial production and could be used to compare ecosystems along latitudinal gradients where resource, rather than temperature, effects on metabolic scaling are of greater magnitude.

The degradation of detrital organic matter and assimilation of carbon (C), nitrogen (N), and phosphorus (P) by heterotrophic microbial communities is mediated by enzymes released into the environment (ecoenzymes). For the attached microbial communities of soils and freshwater sediments, the activities of β-glucosidase, β-N-acetylglucosaminidase, leucine aminopeptidase, and phosphatase show consistent stoichiometric patterns. To determine whether similar constraints apply to planktonic communities, we assembled data from nine studies that include measurements of these enzyme activities along with microbial productivity. By normalizing enzyme activity to productivity, we directly compared the ecoenzymatic stoichiometry of aquatic biofilm and bacterioplankton communities. The relationships between β-glucosidase and α-glucosidase and β-glucosidase and β-N-acetylglucosaminidase were statistically indistinguishable for the two community types, while the relationships between β-glucosidase and phosphatase and β-glucosidase and leucine aminopeptidase significantly differed. For β-glucosidase vs. phosphatase, the differences in slope (biofilm 0.65, plankton 1.05) corresponded with differences in the mean elemental C:P ratio of microbial biomass (60 and 106, respectively). For β-glucosidase vs. leucine aminopeptidase, differences in slope (0.80 and 1.02) did not correspond to differences in the mean elemental C:N of biomass (8.6 and 6.6). β-N-Acetylglucosaminidase activity in biofilms was significantly greater than that of plankton, suggesting that aminosaccharides were a relatively more important N source for biofilms, perhaps because fungi are more abundant. The slopes of β-glucosidase vs. (β-N-acetylglucosaminidase + leucine aminopeptidase) regressions (biofilm 1.07, plankton 0.94) corresponded more closely to the estimated difference in mean biomass C:N. Despite major differences in physical structure and trophic organization, biofilm and plankton communities have similar ecoenzymatic stoichiometry in relation to productivity and biomass composition. These relationships can be integrated into the stoichiometric and metabolic theories of ecology and used to analyze community metabolism in relation to resource constraints.

Dynamics of nutrient exchange between floodplains and rivers have been altered by changes in flow management and proliferation of nonnative plants. We tested the hypothesis that the nonnative, actinorhizal tree, Russian olive (Elaeagnus angustifolia), alters dynamics of leaf litter decomposition compared to native cottonwood (Populus deltoides ssp. wislizeni) along the Rio Grande, a river with a modified flow regime, in central New Mexico (U.S.A.). Leaf litter was placed in the river channel and the surface and subsurface horizons of forest soil at seven riparian sites that differed in their hydrologic connection to the river. All sites had a cottonwood canopy with a Russian olive-dominated understory. Mass loss rates, nutrient content, fungal biomass, extracellular enzyme activities (EEA), and macroinvertebrate colonization were followed for three months in the river and one year in forests. Initial nitrogen (N) content of Russian olive litter (2.2%) was more than four times that of cottonwood (0.5%). Mass loss rates (k; in units of d(-1)) were greatest in the river (Russian olive, k = 0.0249; cottonwood, k = 0.0226), intermediate in subsurface soil (Russian olive, k = 0.0072; cottonwood, k = 0.0031), and slowest on the soil surface (Russian olive, k = 0.0034; cottonwood, k = 0.0012) in a ratio of about 10:2:1. Rates of mass loss in the river were indistinguishable between species and proportional to macroinvertebrate colonization. In the riparian forest, Russian olive decayed significantly faster than cottonwood in both soil horizons. Terrestrial decomposition rates were related positively to EEA, fungal biomass, and litter N, whereas differences among floodplain sites were related to hydrologic connectivity with the river. Because nutrient exchanges between riparian forests and the river have been constrained by flow management, Russian olive litter represents a significant annual input of N to riparian forests, which now retain a large portion of slowly decomposing cottonwood litter with a high potential for N immobilization. As a result, retention and mineralization of litter N within these forests is controlled by hydrologic connectivity to the river, which affects litter export and in situ decomposition.