Michael N. Weintraub

Stoichiometry of soil enzyme activity at global scale

Extracellular enzymes are the proximate agents of organic matter decomposition and measures of these activities can be used as indicators of microbial nutrient demand. We conducted a global-scale meta-analysis of the seven-most widely measured soil enzyme activities, using data from 40 ecosystems. The activities of beta-1,4-glucosidase, cellobiohydrolase, beta-1,4-N-acetylglucosaminidase and phosphatase g(-1) soil increased with organic matter concentration; leucine aminopeptidase, phenol oxidase and peroxidase activities showed no relationship. All activities were significantly related to soil pH. Specific activities, i.e. activity g(-1) soil organic matter, also varied in relation to soil pH for all enzymes. Relationships with mean annual temperature (MAT) and precipitation (MAP) were generally weak. For hydrolases, ratios of specific C, N and P acquisition activities converged on 1 : 1 : 1 but across ecosystems, the ratio of C : P acquisition was inversely related to MAP and MAT while the ratio of C : N acquisition increased with MAP. Oxidative activities were more variable than hydrolytic activities and increased with soil pH. Our analyses indicate that the enzymatic potential for hydrolyzing the labile components of soil organic matter is tied to substrate availability, soil pH and the stoichiometry of microbial nutrient demand. The enzymatic potential for oxidizing the recalcitrant fractions of soil organic material, which is a proximate control on soil organic matter accumulation, is most strongly related to soil pH. These trends provide insight into the biogeochemical processes that create global patterns in ecological stoichiometry and organic matter storage.

BIOGEOCHEMICAL CONSEQUENCES OF RAPID MICROBIAL TURNOVER AND SEASONAL SUCCESSION IN SOIL

Soil microbial communities have the metabolic and genetic capability to adapt to changing environmental conditions on very short time scales. In this paper we combine biogeochemical and molecular approaches to reveal this potential, showing that microbial biomass can turn over on time scales of days to months in soil, resulting in a succession of microbial communities over the course of a year. This new understanding of the year-round turnover and succession of microbial communities allows us for the first time to propose a temporally explicit N cycle that provides mechanistic hypotheses to explain both the loss and retention of dissolved organic N (DON) and inorganic N (DIN) throughout the year in terrestrial ecosystems. In addition, our results strongly support the hypothesis that turnover of the microbial community is the largest source of DON and DIN for plant uptake during the plant growing season. While this model of microbial biogeochemistry is derived from observed dynamics in the alpine, we present several examples from other ecosystems to indicate that the general ideas of biogeochemical fluxes being linked to turnover and succession of microbial communities are applicable to a wide range of terrestrial ecosystems.

The effects of tree rhizodeposition on soil exoenzyme activity, dissolved organic carbon, and nutrient availability in a subalpine forest ecosystem

Previous studies have found that root carbon inputs to the soil can stimulate the mineralization of existing soil carbon (C) pools. It is still uncertain, however, whether this “primed” C is derived from elevated rates of soil organic matter (SOM) decomposition, greater C release from microbial pools, or both. The goal of this research was to determine how the activities of the microbial exoenzymes that control SOM decomposition are affected by root C inputs. This was done by manipulating rhizodeposition with tree girdling in a coniferous subalpine forest in the Rocky Mountains of Colorado, USA, and following changes in the activities of nine exoenzymes involved in decomposition, as well as soil dissolved organic C, dissolved organic and inorganic nitrogen (N), and microbial biomass C and N. We found that rhizodeposition is high in the spring, when the soils are still snow-covered, and that there are large ephemeral populations of microorganisms dependent upon this C. Microbial N acquisition from peptide degradation increased with increases in microbial biomass when rhizodeposition was highest. However, our data indicate that the breakdown of cellulose, lignin, chitin, and organic phosphorus are not affected by springtime increases in soil microbial biomass associated with increases in rhizodeposition. We conclude that the priming of soil C mineralization by rhizodeposition is due to growth of the microbial biomass and an increase in the breakdown of N-rich proteins, but not due to increases in the degradation of plant litter constituents such as cellulose and lignin.

The effects of chronic nitrogen fertilization on alpine tundra soil microbial communities: implications for carbon and nitrogen cycling

Many studies have shown that changes in nitrogen (N) availability affect primary productivity in a variety of terrestrial systems, but less is known about the effects of the changing N cycle on soil organic matter (SOM) decomposition. We used a variety of techniques to examine the effects of chronic N amendments on SOM chemistry and microbial community structure and function in an alpine tundra soil. We collected surface soil (0-5 cm) samples from five control and five long-term N-amended plots established and maintained at the Niwot Ridge Long-term Ecological Research (LTER) site. Samples were bulked by treatment and all analyses were conducted on composite samples. The fungal community shifted in response to N amendments, with a decrease in the relative abundance of basidiomycetes. Bacterial community composition also shifted in the fertilized soil, with increases in the relative abundance of sequences related to the Bacteroidetes and Gemmatimonadetes, and decreases in the relative abundance of the Verrucomicrobia. We did not uncover any bacterial sequences that were closely related to known nitrifiers in either soil, but sequences related to archaeal nitrifiers were found in control soils. The ratio of fungi to bacteria did not change in the N-amended soils, but the ratio of archaea to bacteria dropped from 20% to less than 1% in the N-amended plots. Comparisons of aliphatic and aromatic carbon compounds, two broad categories of soil carbon compounds, revealed no between treatment differences. However, G-lignins were found in higher relative abundance in the fertilized soils, while proteins were detected in lower relative abundance. Finally, the activities of two soil enzymes involved in N cycling changed in response to chronic N amendments. These results suggest that chronic N fertilization induces significant shifts in soil carbon dynamics that correspond to shifts in microbial community structure and function.

The earliest stages of ecosystem succession in high-elevation (5000 metres above sea level), recently deglaciated soils

Global climate change has accelerated the pace of glacial retreat in high-latitude and high-elevation environments, exposing lands that remain devoid of vegetation for many years. The exposure of ‘new’ soil is particularly apparent at high elevations (5000 metres above sea level) in the Peruvian Andes, where extreme environmental conditions hinder plant colonization. Nonetheless, these seemingly barren soils contain a diverse microbial community; yet the biogeochemical role of micro-organisms at these extreme elevations remains unknown. Using biogeochemical and molecular techniques, we investigated the biological community structure and ecosystem functioning of the pre-plant stages of primary succession in soils along a high-Andean chronosequence. We found that recently glaciated soils were colonized by a diverse community of cyanobacteria during the first 4–5 years following glacial retreat. This significant increase in cyanobacterial diversity corresponded with equally dramatic increases in soil stability, heterotrophic microbial biomass, soil enzyme activity and the presence and abundance of photosynthetic and photoprotective pigments. Furthermore, we found that soil nitrogen-fixation rates increased almost two orders of magnitude during the first 4–5 years of succession, many years before the establishment of mosses, lichens or vascular plants. Carbon analyses (pyrolysis-gas chromatography/mass spectroscopy) of soil organic matter suggested that soil carbon along the chronosequence was of microbial origin. This indicates that inputs of nutrients and organic matter during early ecosystem development at these sites are dominated by microbial carbon and nitrogen fixation. Overall, our results indicate that photosynthetic and nitrogen-fixing bacteria play important roles in acquiring nutrients and facilitating ecological succession in soils near some of the highest elevation receding glaciers on the Earth.

Nitrogen Cycling and the Spread of Shrubs Control Changes in the Carbon Balance of Arctic Tundra Ecosystems

Abstract Decomposition in the Arctic has been slower than plant growth, causing an accumulation of detritus in tundra soils. Climate warming may result in carbon (C) loss by accelerating the decomposition of soil organic matter (SOM). Nitrogen (N) release from SOM may also enhance plant growth, which is limited by N availability in tundra ecosystems. Since N acquisition varies by plant species, changes in plant community composition resulting from climate change may alter carbon cycling in tundra soils. Shrubs are growing in predominance in tundra communities in response to warming. Since they are the woodiest plants in the tundra, this may increase ecosystem C storage, because wood has the highest C:N ratio of any plant tissue and decomposes slowly. Whether net ecosystem C storage increases or decreases will depend on the balance of (a) C losses from SOM and (b) C storage in plant pools due to higher primary productivity and changes in plant community composition.

Evolutionary-Economic Principles as Regulators of Soil Enzyme Production and Ecosystem Function

Extracellular enzymes allow microbes and plant roots to acquire resources from complex molecules, and thereby catalyze the rate-limiting step in soil carbon and nutrient cycling. We examine the hypothesis that extracellular enzyme producers are under evolutionary pressure to minimize the cost:benefit ratio of enzyme production. Consistent with this prediction, enzyme producers generally allocate more resources to enzymes that target limiting nutrients. Additionally, regulatory systems have evolved to increase enzyme production when substrates are abundant and available resources are scarce. Finally, theoretical models predict that producers should control enzyme diffusion rates and adopt strategies to reduce competition for enzymatic reaction products. Because extracellular enzymes regulate ecosystem processes, enzyme allocation could affect ecosystem responses to environmental change. In particular, shifts in enzyme allocation may result in negative feedbacks to changes in resource availability. Enzyme allocation patterns therefore link ecological and evolutionary constraints at the organismal level with ecosystem-level processes.

The contribution of beneath-snow soil respiration to total ecosystem respiration in a high-elevation, subalpine forest

[1] The respiratory loss of CO 2 from soil microbes beneath winter snow in forests from cold climates can significantly influence the annual carbon budget. We explored the magnitude of winter soil respiration using continuous measurements of beneath-snow CO 2 concentration within the footprint of a flux tower in a subalpine forest in the Rocky Mountains. We used eddy covariance measurements from the tower to obtain estimates of total wintertime ecosystem respiration and compared them to the calculated beneath-snow CO 2 flux. Soil respiration in the winter was estimated to contribute 35-48% of the total wintertime ecosystem respiration, and 7-10% of the total annual ecosystem respiration. The largest increase in soil respiration occurred in the late winter following an earlier-than-normal initiation of snowmelt and increase in snow density. Following this melt event, respiration rates increased approximately sixfold, despite an increase in soil temperature of only 0.3°-0.5°C. We interpret the late-winter surge in soil respiration to be triggered by a strong response of beneath-snow microbes to the pulse of meltwater coupled with extremely high sensitivity of the microbial biomass to increases in soil temperature.

Integrating legacy soil phosphorus into sustainable nutrient management strategies for future food, bioenergy and water security

Legacy phosphorus (P) that has accumulated in soils from past inputs of fertilizers and manures is a large secondary global source of P that could substitute manufactured fertilizers, help preserve critical reserves of finite phosphate rock to ensure future food and bioenergy supply, and gradually improve water quality. We explore the issues and management options to better utilize legacy soil P and conclude that it represents a valuable and largely accessible P resource. The future value and period over which legacy soil P can be accessed depends on the amount present and its distribution, its availability to crops and rates of drawdown determined by the cropping system. Full exploitation of legacy P requires a transition to a more holistic system approach to nutrient management based on technological advances in precision farming, plant breeding and microbial engineering together with a greater reliance on recovered and recycled P. We propose the term ‘agro-engineering’ to encompass this integrated approach. Smaller targeted applications of fertilizer P may still be needed to optimize crop yields where legacy soil P cannot fully meet crop demands. Farm profitability margins, the need to recycle animal manures and the extent of local eutrophication problems will dictate when, where and how quickly legacy P is best exploited. Based on our analysis, we outline the stages and drivers in a transition to the full utilization of legacy soil P as part of more sustainable regional and global nutrient management.

Extracellular enzymes in terrestrial, freshwater, and marine environments: perspectives on system variability and common research needs

Extracellular enzymes produced by heterotrophic microbial communities are major drivers of carbon and nutrient cycling in terrestrial, freshwater, and marine environments. Although carbon and nutrient cycles are coupled on global scales, studies of extracellular enzymes associated with terrestrial, freshwater, and marine microbial communities are not often compared across ecosystems. In part, this disconnect arises because the environmental parameters that control enzyme activities in terrestrial and freshwater systems, such as temperature, pH, and moisture content, have little explanatory power for patterns of enzyme activities in marine systems. Instead, factors such as the functional diversity of microbial communities may explain varying patterns of enzyme activities observed in the ocean to date. In any case, many studies across systems focus on similar issues that highlight the commonalities of microbial community organization. Examples include the effective lifetime of enzymes released into the environment; the extent to which microbial communities coordinate enzyme expression to decompose complex organic substrates; and the influence of microbial community composition on enzyme activities and kinetics. Here we review the often-disparate research foci in terrestrial, freshwater, and marine environments. We consider the extent to which environmental factors may regulate extracellular enzyme activities within each ecosystem, and highlight commonalities and current methodological challenges to identify research questions that may aid in integrating cross-system perspectives in the future.