Microbial communities in terrestrial surface soils are not widely limited by carbon.

Microbial communities in soils are generally considered to be limited by carbon (C), which could be a crucial control for basic soil functions and responses of microbial heterotrophic metabolism to climate change. However, global soil microbial C limitation (MCL) has rarely been estimated and is poorly understood. Here, we predicted MCL, defined as limited availability of substrate C relative to nitrogen and/or phosphorus to meet microbial metabolic requirements, based on the thresholds of extracellular enzyme activity across 847 sites (2476 observations) representing global natural ecosystems. Results showed that only about 22% of global sites in terrestrial surface soils show relative C limitation in microbial community. This finding challenges the conventional hypothesis of ubiquitous C limitation for soil microbial metabolism. The limited geographic extent of C limitation in our study was mainly attributed to plant litter, rather than soil organic matter that has been processed by microbes, serving as the dominant C source for microbial acquisition. We also identified a significant latitudinal pattern of predicted MCL with larger C limitation at mid- to high latitudes, whereas this limitation was generally absent in the tropics. Moreover, MCL significantly constrained the rates of soil heterotrophic respiration, suggesting a potentially larger relative increase in respiration at mid- to high latitudes than low latitudes, if climate change increases primary productivity that alleviates MCL at higher latitudes. Our study provides the first global estimates of MCL, advancing our understanding of terrestrial C cycling and microbial metabolic feedback under global climate change.

Plant, microbial and ecosystem carbon use efficiencies interact to stabilize microbial growth as a fraction of gross primary production.

The carbon use efficiency of plants (CUEa ) and microorganisms (CUEh ) determines rates of biomass turnover and soil carbon sequestration. We evaluated the hypothesis that CUEa and CUEh counterbalance at a large scale, stabilizing microbial growth (µ) as a fraction of gross primary production (GPP). Collating data from published studies, we correlated annual CUEa , estimated from satellite imagery, with locally determined soil CUEh for 100 globally distributed sites. Ecosystem CUEe , the ratio of net ecosystem production (NEP) to GPP, was estimated for each site using published models. At the ecosystem scale, CUEa and CUEh were inversely related. At the global scale, the apparent temperature sensitivity of CUEh with respect to mean annual temperature (MAT) was similar for organic and mineral soils (0.029°C-1 ). CUEa and CUEe were inversely related to MAT, with apparent sensitivities of -0.009 and -0.032°C-1 , respectively. These trends constrain the ratio µ : GPP (= (CUEa  × CUEh )/(1 - CUEe )) with respect to MAT by counterbalancing the apparent temperature sensitivities of the component processes. At the ecosystem scale, the counterbalance is effected by modulating soil organic matter stocks. The results suggest that a µ : GPP value of c. 0.13 is a homeostatic steady state for ecosystem carbon fluxes at a large scale.

Nutrient limitation mediates soil microbial community structure and stability in forest restoration.

Soil microorganisms are often limited by nutrients, representing an important control of heterotrophic metabolic processes. However, how nutrient limitations relate to microbial community structure and stability remains unclear, which creates a knowledge gap to understanding microbial biogeography and community changes during forest restoration. Here, we combined an eco-enzymatic stoichiometry model and high-throughput DNA sequencing to assess the potential roles of nutrient limitation on microbial community structure, assembly, and stability along a forest restoration sequence in the Qinling Mountains, China. Results showed that nutrient limitations tended to decrease during the oak forest restoration. Carbon and phosphorus limitations enhanced community dissimilarity and significantly increased bacterial alpha diversity, but not fungal diversity. Stochastic assembly processes primarily structured both bacterial (average contribution of 74.73 % and 74.17 % in bulk and rhizosheath soils, respectively) and fungal (average contribution of 77.23 % and 72.04 % in bulk and rhizosheath soils, respectively) communities during forest restoration, with nutrient limitation also contributing to the importance of stochastic processes in the bacterial communities. The migration rate (m) for bacteria was 0.19 and 0.23, respectively in both bulk soil and rhizosheath soil, and was greater than that for the fungi (m was 1.19 and 1.41, respectively), indicating a stronger dispersal limitation for fungal communities. Finally, nutrient limitations significantly affected bacterial and fungal co-occurrence with more interconnections occurring among weakly nutrient-limited microbial taxa and nutrient limitations reducing community stability when nutrient availability changed during forest restoration. Our findings highlight the fundamental effects of nutrient limitations on microbial communities and their self-regulation under changing environmental resources.

Carbon use efficiency of microbial communities: stoichiometry, methodology and modelling.

Carbon use efficiency (CUE) is a fundamental parameter for ecological models based on the physiology of microorganisms. CUE determines energy and material flows to higher trophic levels, conversion of plant-produced carbon into microbial products and rates of ecosystem carbon storage. Thermodynamic calculations support a maximum CUE value of ~ 0.60 (CUE max). Kinetic and stoichiometric constraints on microbial growth suggest that CUE in multi-resource limited natural systems should approach ~ 0.3 (CUE max /2). However, the mean CUE values reported for aquatic and terrestrial ecosystems differ by twofold (~ 0.26 vs. ~ 0.55) because the methods used to estimate CUE in aquatic and terrestrial systems generally differ and soil estimates are less likely to capture the full maintenance costs of community metabolism given the difficulty of measurements in water-limited environments. Moreover, many simulation models lack adequate representation of energy spilling pathways and stoichiometric constraints on metabolism, which can also lead to overestimates of CUE. We recommend that broad-scale models use a CUE value of 0.30, unless there is evidence for lower values as a result of pervasive nutrient limitations. Ecosystem models operating at finer scales should consider resource composition, stoichiometric constraints and biomass composition, as well as environmental drivers, to predict the CUE of microbial communities.

Trade-offs in carbon-degrading enzyme activities limit long-term soil carbon sequestration with biochar addition.

Biochar amendment is one of the most promising agricultural approaches to tackle climate change by enhancing soil carbon (C) sequestration. Microbial-mediated decomposition processes are fundamental for the fate and persistence of sequestered C in soil, but the underlying mechanisms are uncertain. Here, we synthesise 923 observations regarding the effects of biochar addition (over periods ranging from several weeks to several years) on soil C-degrading enzyme activities from 130 articles across five continents worldwide. Our results showed that biochar addition increased soil ligninase activity targeting complex phenolic macromolecules by 7.1%, but suppressed cellulase activity degrading simpler polysaccharides by 8.3%. These shifts in enzyme activities explained the most variation of changes in soil C sequestration across a wide range of climatic, edaphic and experimental conditions, with biochar-induced shift in ligninase:cellulase ratio correlating negatively with soil C sequestration. Specifically, short-term (<1 year) biochar addition significantly reduced cellulase activity by 4.6% and enhanced soil organic C sequestration by 87.5%, whereas no significant responses were observed for ligninase activity and ligninase:cellulase ratio. However, long-term (≥1 year) biochar addition significantly enhanced ligninase activity by 5.2% and ligninase:cellulase ratio by 36.1%, leading to a smaller increase in soil organic C sequestration (25.1%). These results suggest that shifts in enzyme activities increased ligninase:cellulase ratio with time after biochar addition, limiting long-term soil C sequestration with biochar addition. Our work provides novel evidence to explain the diminished soil C sequestration with long-term biochar addition and suggests that earlier studies may have overestimated soil C sequestration with biochar addition by failing to consider the physiological acclimation of soil microorganisms over time.

The contribution of abiotic processes to buried litter decomposition in the northern Chihuahuan desert.

Creosobebush (Larrea tridentata) fine litter was treated with either the general biocide HgCl2 and CuSO4 or water (controls) and buried 5 cm beneath the soil surface in the northern Chihuahuan Desert. The treated litter showed significantly less mass loss than controls during the three month summer-autumn field study; controls lost about 20% of the original mass while treated litter lost less than 2%. In addition, the total nitrogen content of the control litter increased from an initial concentration of about 14.08 g kg-1 to 17.62 g kg-1 dry weight by the end of the study, while treated litter nitrogen content decreased to 13.30 g kg-1. Results suggest abiotic processes other than leaching have little effect on the decomposition of buried litter in this environment.

Plants retard litter decay in a nutrient-limited soil: a case of exploitative competition?

Litter was incubated in pasteurized and unpasteurized soils, with and without the presence of prairie grasses (Bouteloua gracilis or Schizachyrium scoparium), to determine if competition between plants and saprophytes altered rates of litter decay. A soil pasteurization treatment was included to ascertain if the presence of vesicular-arbuscular mycorrhizae inocula would affect the competitive interaction. Analyses of variance detected significant effects (P<0.5) of soil pasteurization, plant species and litter presence on root mass, and significant effects of plant species and litter presence on shoot and total plant mass. The degree of mycorrhizal colonization varied little between plant species but mycorrhizae were entirely absent in pasteurized soils; soil pasteurization usually reduced plant growth. Analyses of covariance detected (1) a highly significant negative relationship (P<0.01) between litter mass loss and plant growth (as covariates), when controlling for the effects of time, and (2) a significant positive relationship (P<0.05) between litter nitrogen content and mass loss (as covariates), when controlling for the effects of time and soil pasteurization. These relationships would be expected if exploitative competition for nutrients existed between plants and decomposers such that nutrient uptake by plants reduced concomitant litter decay.

Field and lab conditions alter microbial enzyme and biomass dynamics driving decomposition of the same leaf litter.

Fluctuations in climate and edaphic factors influence field decomposition rates and preclude a complete understanding of how microbial communities respond to plant litter quality. In contrast, laboratory microcosms isolate the intrinsic effects of litter chemistry and microbial community from extrinsic effects of environmental variation. Used together, these paired approaches provide mechanistic insights to decomposition processes. In order to elucidate the microbial mechanisms underlying how environmental conditions alter the trajectory of decay, we characterized microbial biomass, respiration, enzyme activities, and nutrient dynamics during early (<10% mass loss), mid- (10-40% mass loss), and late (>40% mass loss) decay in parallel field and laboratory litter bag incubations for deciduous tree litters with varying recalcitrance (dogwood < maple < maple-oak mixture < oak). In the field, mass loss was minimal (<10%) over the first 50 days (January-February), even for labile litter types, despite above-freezing soil temperatures and adequate moisture during these winter months. In contrast, microcosms displayed high C mineralization rates in the first week. During mid-decay, the labile dogwood and maple litters in the field had higher mass loss per unit enzyme activity than the lab, possibly due to leaching of soluble compounds. Microbial biomass to litter mass (B:C) ratios peaked in the field during late decay, but B:C ratios declined between mid- and late decay in the lab. Thus, microbial biomass did not have a consistent relationship with litter quality between studies. Higher oxidative enzyme activities in oak litters in the field, and higher nitrogen (N) accumulation in the lab microcosms occurred in late decay. We speculate that elevated N suppressed fungal activity and/or biomass in microcosms. Our results suggest that differences in microbial biomass and enzyme dynamics alter the decay trajectory of the same leaf litter under field and lab conditions.

A conceptual model for primary productivity, decomposition and nitrogen cycling in the Chihuahuan creosotebush desert.

The conceptual framework for a simulation model of primary productivity, decomposition and nitrogen cycling in a shrub-dominated desert ecosystem in southern New Mexico is presented. This model is based on our previous attempt to simulate carbon allocation patterns in the desert shrub Larrea tridentata Cov., which demonstrated that moisture patterns alone are insufficient to predict desert productivity. These results, as well as others, suggest that mineral nutrients, especially nitrogen, may also be an important determinant of productivity in arid environments. Our current research in the Chihuahuan desert is directed towards elucidating the numerous biotic and abiotic interactions that determine the rates and directions of carbon, nitrogen and water fluxes in this ecosystem. The development of this working model will serve as a tool to accomplish three major objectives: (1) to synthesize the large amount of existing data on decomposition and nitrogen cycling in deserts, (2) to quantify our present state of knowledge about the structure and function of ecosystem components important in carbon and nitrogen dynamics in deserts, and (3) to address hypotheses concerning the complex mechanisms of interactions and feedbacks among the organisms involved in carbon and nitrogen exchanges in deserts.

Antarctic climate cooling and terrestrial ecosystem response.

The average air temperature at the Earth's surface has increased by 0.06 degrees C per decade during the 20th century, and by 0.19 degrees C per decade from 1979 to 1998. Climate models generally predict amplified warming in polar regions, as observed in Antarctica's peninsula region over the second half of the 20th century. Although previous reports suggest slight recent continental warming, our spatial analysis of Antarctic meteorological data demonstrates a net cooling on the Antarctic continent between 1966 and 2000, particularly during summer and autumn. The McMurdo Dry Valleys have cooled by 0.7 degrees C per decade between 1986 and 2000, with similar pronounced seasonal trends. Summer cooling is particularly important to Antarctic terrestrial ecosystems that are poised at the interface of ice and water. Here we present data from the dry valleys representing evidence of rapid terrestrial ecosystem response to climate cooling in Antarctica, including decreased primary productivity of lakes (6-9% per year) and declining numbers of soil invertebrates (more than 10% per year). Continental Antarctic cooling, especially the seasonality of cooling, poses challenges to models of climate and ecosystem change.