Stabilization of oxidative enzymes in desert soil may limit organic matter accumulation

doi:10.1016/j.soilbio.2007.09.002

Soil Biology and Biochemistry

Volume 40, Issue 2, February 2008, Pages 550-553

https://doi.org/10.1016/j.soilbio.2007.09.002 Get rights and content

Abstract

Phenol oxidase and peroxidase activities in desert grassland soils at the Sevilleta Long Term Ecological Research site in central New Mexico (USA) are far greater than those of temperate soils. Activity is uniformly distributed across particles ranging from >1 mm to <38 μm and is unaffected by autoclaving, in contrast to hydrolase activities. The sorbed enzymes are readily extractable and inactivated by boiling. High soil pH, high stabilized oxidative enzyme activity, and carbonates create optimal conditions for degradation of phenols which increase decomposition potentials and limit soil organic matter accumulation.

Introduction

The low concentrations of organic matter in desert soils are thought to result from low rates of net primary productivity (NPP) as a consequence of low precipitation. However, across latitudinal gradients, soil organic matter (SOM) concentrations reflect differences in decomposition potential relative to NPP (Horwath, 2007). Tundra ecosystems have annual NPP rates comparable to those of deserts, but accumulate large stores of SOM because decomposition rates are lower than NPP. Tropical forests have high rates of NPP but low SOM because decomposition potentials equal or exceed organic matter inputs.

Recent studies suggest that the decomposition potential of desert ecosystems has been underestimated. Because of photodegradation and physical disturbance, rates of surface litter decomposition are comparable to those of temperate ecosystems despite narrow opportunities for microbial growth (Austin and Vivanco, 2006; Gallo et al., 2006; Brandt et al., 2007). These processes also reduce the incorporation of surface litter into soil, contributing to low SOM stocks.

Another factor contributing to low SOM may be high soil oxidative potentials. Stursova et al. (2006) measured phenol oxidase and peroxidase potentials in desert grassland soils that were an order of magnitude greater than those reported for other biomes. These extreme values are related to soil pH. Because of carbonate accumulation, the pH of arid soils can reach 8 or above, which is optimal for these enzymes. However, pH alone may not account for the extreme values, given the low values for SOM and microbial biomass. To further characterize these activities, we conducted a series of trials to examine the distribution of oxidative potentials within the soil matrix and differentiate mineral from enzymic catalysis.

Section snippets

Site description

Soil samples were collected on Sevilleta National Wildlife Refuge (SNWR) in central New Mexico USA (34.58°N, 106.65°W). The site is desert grassland dominated by C₄ perenial grasses. Mean annual temperature is 13.2 °C; mean annual precipitation is 250 mm; aboveground net primary production averages 51 g m⁻² y⁻¹ (http://sev.lternet.edu). The soils are Typic Haplargids derived from piedmont alluvium. Soil texture in the upper 20 cm is 67.9% sand, 22.5% silt and 9.5% clay, with 2% calcium carbonate (

Sample collection

Soil (top 5 cm) was collected on 20 March 2007 from several locations and mixed to obtain a 5 kg composite sample, which was sieved through 2 mm mesh prior to further analyses. The water content of the soil collected was 0.5%. Subsamples of bulk soil were autoclaved twice for 30 min. Other subsamples were sorted through nested sieves (1000, 600, 355, 250, 150, 106, 75, 63, and 38 μm mesh).

Physical and chemical analyses

For fresh, autoclaved and size-sorted soils, moisture and organic matter content were determined by oven drying at 100 °C and combusting at 500 °C. Bulk soil pH was measured after overnight equilibration in 1:2 suspensions of air dry soil and and deionized water. For fresh and autoclaved soil, extractable phenols were assayed by adding 15 g soil to 30 mL of 50 mM, pH 8.2, bicarbonate buffer, and tumbling the suspensions on an orbital mixer for 1 h. After centrifuging the tubes at 3000g for 10 min,

Extracellular enzyme assays

Phenol oxidase (EC 1.10.3.2) and peroxidase (EC 1.11.1.7) activities in soil suspensions and soil extracts were assayed using l-3,4-dihydroxyphenylalanine (DOPA) and DOPA+0.3% H₂O₂, respectively (Stursova et al., 2006), and expressed as μmol h⁻¹ g OM⁻¹. Enzymes sorbed to soil particles were solubilized in three sequential extractions, following the procedure described above for extraction of phenols. To compare the stability of oxidative enzymes to that of hydrolases, triplicate subsamples of

Results

Soil characteristics were typical of those reported in previous studies (Kieft et al., 1998; Stursova et al., 2006; Crenshaw et al., 2007; Zeglin et al., 2007): pH 8.11, SOM 1.2%, texture 70% sand and 30% silt, inorganic carbon 1.5% (Table 1). No phenols were detected in extracts of fresh or autoclaved soil.

In bulk soil, potential activities for phenol oxidase and peroxidase averaged 288 and 416 μmol h⁻¹ g OM⁻¹, respectively (Table 1). These values were in the low end of the range reported from

Discussion

The oxidative potential of Sevilleta grassland soil is not only high compared to activities measured in other systems, but also very stable. Autoclaving had no effect on activity, even though hydrolases were almost fully inactivated. Mineral catalysis of phenolic oxidation appears unlikely because activity was uniformly distributed across particle size, easily extracted from both fresh and autoclaved soils, and once extracted, readily eliminated by boiling.

The mechanisms for selective

Acknowledgment

This work was supported by the Sevilleta LTER program.

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Citation Excerpt :
Phenolic compounds have hydrolase-inhibiting properties (Wetzel, 1992; Appel, 1993; Freeman et al., 2001; Fenner et al., 2005). Therefore, the increased (decreased) oxidase activities would lead to the reduction (accumulation) of phenolic concentrations, which removed (intensified) the inhibition of phenolic compounds on hydrolytic enzymes with the hydrolase activities subsequently improved (minimized), and then would limit (promote) SOM accumulation (Freeman et al., 2001, 2004; Fenner et al., 2005; Stursova and Sinsabaugh, 2008; Sinsabaugh, 2010). The results described above indicated that the “enzymatic latch” hypothesis could also be applied to the SOM dynamics in chernozem, supporting the third hypothesis.
An enzymatic latch on carbon store in peatlands or desert soils has been verified but has rarely been examined in a cultivated field with a high pH and a high calcium carbonate content. Soil organic matter (SOM) contents of chernozem have decreased over the last few decades in northeast China. However, the enzymatic mechanism of SOM loss in this region remains unclear. An experiment was conducted to investigate the effects of soil oxidases and hydrolases on SOM, the correlations between soil oxidases and hydrolases, and the relationships between soil microbial community and related soil enzymes with 40 soil samples from different cultivated fields in Lishu County, northeastern China. The results showed that SOM increased significantly over the pH range of 5.0–7.0, and decreased sharply in the range of 7.0–8.0. Soil oxidases (peroxidase and total oxidases) activities showed significant and negative correlations with SOM content but positive correlations with hydrolases (β-glucosidase, β-xylosidase and total hydrolases) activities. The SOM content was significantly and negatively correlated with α-glucosidase, β-glucosidase, cellobiohydrolase, β-xylosidase, and total hydrolases activities. Results of redundancy analysis indicated that all soil hydrolases activities had positive relationships with bacteria i15:0, 16:3 ω6c and 16:0. Peroxidase and total oxidases activities were positively associated with bacteria cy17:0 ω7c, 15:0 DMA, i16:0, 18:0, i17:0, 14:0, 15:0 and actinomycetes 17:0 10-methyl, 18:0 10-methyl, while phenol oxidase activity was positively associated with bacteria i17:1 ω9c, 17:1 ω8c, i14:0 and fungi 18:1 ω9c. These findings confirmed the enzymatic latch mechanism of SOM accumulation in this test chernozem, which means that oxidases relieve the inhibition of hydrolases, resulting in SOM hydrolysis by higher hydrolases activities.

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Short CommunicationStabilization of oxidative enzymes in desert soil may limit organic matter accumulation

Abstract

Introduction

Section snippets

Site description

Sample collection

Physical and chemical analyses

Extracellular enzyme assays

Results

Discussion

Acknowledgment

Pedobiologia

Applied Soil Ecology

Phytochemistry

Soil Biology & Biochemistry

Soil Biology & Biochemistry

Plant litter decomposition in a semi-arid ecosystem controlled by photodegradation

Nature

Effects of UV radiation on decomposition depend on precipitation and litter chemistry in a shortgrass steppe ecosystem

Global Change Biology

Short Communication
Stabilization of oxidative enzymes in desert soil may limit organic matter accumulation