Ecoenzymatic Stoichiometry and Ecological Theory Sinsabaugh, Robert L; Follstad Shah, Jennifer J
Annual review of ecology, evolution, and systematics,
01/2012, Volume:
43, Issue:
1
Journal Article
Peer reviewed
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.
Biota can be described in terms of elemental composition, expressed as an atomic ratio of carbon:nitrogen:phosphorus. 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.
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.
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.
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.
The microbiome concept has drawn attention to the complex signal and syntrophic networks that underlie microbial community organization. This self-organization may lead to patterns in the allometric ...scaling of microbial community metabolism that differ from those of macrobial communities. Using meta-analyses, we analyzed the power scaling relationships between community production, respiration, extracellular enzyme activity and biomass for bacteria and fungi across aquatic and terrestrial ecosystems. The scaling exponents for community production versus biomass for fungi and bacteria were 0.85 ± 0.06 (95 % CI) and 0.72 ± 0.07, respectively. The scaling exponent for fungal respiration versus production was 0.61 ± 0.06. Previous studies reported exponents of 0.41, 0.44 and 0.58 for bacterial respiration versus production. Carbon use efficiency increased with biomass for both fungi and bacteria with an exponent of 0.27 ± 0.06. The potential activities of four widely measured extracellular enzymes were directly related to community production with power scaling exponents of 1.0–1.2. The frequency distribution of biomass turnover times (median 112 h for bacteria and 1,128 h for fungi) overlapped substantially with those for environmental substrate turnover, presented in a prior analysis of extracellular enzyme kinetics. These metabolic relationships, which have scaling exponents of 0.5, are linked by the ratio of assimilation to carbon use efficiency. This connection ties ecological stoichiometry and metabolic theory to microbial community homeostasis. At the ecosystem scale, allometry of microbial communities has similarities to that of eusocial insects but differs from that of plant communities, perhaps as a result of proto-cooperative processes that contribute to microbial community organization.
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 processing, nutrient cycling, water quality, and water availability. Effective conservation efforts and riparian ecosystems management require matching of plant functional trait diversity and redundancy with tolerance to environmental changes in all biomes.
Streams and rivers are important conduits of terrestrially derived carbon (C) to atmospheric and marine reservoirs. Leaf litter breakdown rates are expected to increase as water temperatures rise in ...response to climate change. The magnitude of increase in breakdown rates is uncertain, given differences in litter quality and microbial and detritivore community responses to temperature, factors that can influence the apparent temperature sensitivity of breakdown and the relative proportion of C lost to the atmosphere vs. stored or transported downstream. Here, we synthesized 1025 records of litter breakdown in streams and rivers to quantify its temperature sensitivity, as measured by the activation energy (Ea, in eV). Temperature sensitivity of litter breakdown varied among twelve plant genera for which Ea could be calculated. Higher values of Ea were correlated with lower‐quality litter, but these correlations were influenced by a single, N‐fixing genus (Alnus). Ea values converged when genera were classified into three breakdown rate categories, potentially due to continual water availability in streams and rivers modulating the influence of leaf chemistry on breakdown. Across all data representing 85 plant genera, the Ea was 0.34 ± 0.04 eV, or approximately half the value (0.65 eV) predicted by metabolic theory. Our results indicate that average breakdown rates may increase by 5–21% with a 1–4 °C rise in water temperature, rather than a 10–45% increase expected, according to metabolic theory. Differential warming of tropical and temperate biomes could result in a similar proportional increase in breakdown rates, despite variation in Ea values for these regions (0.75 ± 0.13 eV and 0.27 ± 0.05 eV, respectively). The relative proportions of gaseous C loss and organic matter transport downstream should not change with rising temperature given that Ea values for breakdown mediated by microbes alone and microbes plus detritivores were similar at the global scale.
Warmer water enhances decomposition of organic matter in streams and rivers, but it is unclear if climate change will result in more carbon emitted to the atmosphere or transported to the ocean. We assembled over 1000 published data points on leaf litter breakdown in streams and rivers globally to assess how rates of breakdown will change with elevated temperature. Across 85 plant genera, we found that rates may increase only half as much as expected should water temperature rise by 1–4 °C. Among 12 plant genera for which temperature sensitivity could be calculated individually, higher sensitivity was correlated with lower quality litter. Similarity in the temperature sensitivity of breakdown mediated by microbes alone or microbes plus detritivores suggests the relative proportions of carbon converted to gas or transported as smaller particles will not change with elevated temperature.
Background
Chronic kidney disease is a serious health condition and is increasing globally. Effective self‐management could slow disease progression and improve health outcomes, although the ...contribution of health literacy and knowledge for self‐management is not well known.
Aim
To investigate the recent evidence of health literacy and the relationship between health literacy, knowledge and self‐management of chronic kidney disease.
Methods
Arksey and O'Malley's framework informed this scoping review. Eligible studies involving adults with any grade of chronic kidney disease, measuring all dimensions of health literacy (i.e., functional, communicative, and critical), disease‐specific knowledge and self‐management, published in English between January 2005 and March 2020, were included.
Results
The scoping review found 12 eligible studies, with 11 assessing all dimensions of health literacy. No study examined health literacy, knowledge and self‐management. When individuals had greater health literacy, this was associated with greater knowledge about the disease. Communicative health literacy was a significant predictor of medication, diet and fluid adherence, and overall self‐management behaviours.
Conclusion
This scoping review shows that disease‐specific knowledge is important for health literacy and that health literacy is essential for effective self‐management of chronic kidney disease. The implications of these relationships can inform strategies for the development of evidence‐based patient education to support increased self‐management. There is also a need for further research to explore these associations.
Purpose Multiple smaller studies have demonstrated an association between overall survival and lymph node (LN) count from neck dissection in patients with head and neck cancer. This is a large cohort ...study to examine these associations by using a national cancer database. Patients and Methods The National Cancer Database was used to identify patients who underwent upfront nodal dissection for mucosal head and neck squamous cell carcinoma between 2004 and 2013. Patients were stratified by LN count into those with < 18 nodes and those with ≥ 18 nodes on the basis of prior work. A multivariable Cox proportional hazards regression model was constructed to predict hazard of mortality. Stratified models predicted hazard of mortality both for patients who were both node negative and node positive. Results There were 45,113 patients with ≥ 18 LNs and 18,865 patients with < 18 LNs examined. The < 18 LN group, compared with the ≥ 18 LN group, had more favorable tumor characteristics, with a lower proportion of T3 and T4 lesions (27.9% v 39.8%), fewer patients with positive nodes (46.6% v 60.5%), and lower rates of extracapsular extension (9.3% v 15.1%). Risk-adjusted Cox models predicting hazard of mortality by LN count showed an 18% increased hazard of death for patients with < 18 nodes examined (hazard ratio HR 1.18; 95% CI, 1.13 to 1.22). When stratified by clinical nodal stage, there was an increased hazard of death in both groups (node negative: HR, 1.24; 95% CI, 1.17 to 1.32; node positive: HR, 1.12; 95% CI, 1.05 to 1.19). Conclusion The results of our study demonstrate a significant overall survival advantage in both patients who are clinically node negative and node positive when ≥ 18 LNs are examined after neck dissection, which suggests that LN count is a potential quality metric for neck dissection.
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