Links between microbial population dynamics and nitrogen availability in an alpine ecosystem

Ecology, July, 1999 by David A. Lipson, Steven K. Schmidt, Russel K. Monson

INTRODUCTION

Soil microbial population dynamics have important implications for N availability to plants in many ecosystems. For example, microbial biomass often assimilates N at times when plants are inactive, releasing the N to plants some time later when plants are active and microbial biomass turns over (Singh et al. 1989, Zak et al. 1990). In the Colorado alpine, the link between seasonal fluctuations in microbial biomass and N uptake by plants is still mysterious. Recent work (Fisk and Schmidt 1996, Jaeger et al. 1999) shows that a temporal partitioning of N between plants and microbes exists in this ecosystem, wherein plants take up N in the summer and microbes immobilize N maximally in the autumn. This manifests as an increase in microbial biomass N in the fall, and implies that a release of N from microbial biomass must occur sometime before the plant growing season. Microbial biomass N was observed to decline in the later stages of snow melt in the spring, but no flush of inorganic N was seen in the soil (Brooks et al. 1998). Brooks et al. (1996) found that net N mineralization occurred in soil under the snowpack during the spring; however, net immobilization of N was observed after snow melt. It is still unknown whether a seasonal change in microbial population size causes a flush of available N to plants.

These reported patterns of seasonal N uptake by alpine plants and microbes have not yet been reconciled with recent evidence for organic N utilization by alpine plants. Net N mineralization can account for only a fraction of annual plant N uptake in this ecosystem (Bowman et al. 1993, Fisk and Schmidt 1995). The uptake of amino acids may explain the balance of this N (Raab et al. 1996, Lipson and Monson 1998). However, we lack a description of the seasonal fluxes of amino acids in the soil. Previous work shows that Kobresia myosuroides (Cyperaceae), the dominant plant species of alpine dry meadows in the Rocky Mountains, takes up most of its required N early in the summer, when soils have warmed but are still moist (Theodose et al. 1996, Jaeger et al. 1999). Also, K. myosuroides competes best with microbes for amino acids under these conditions (Lipson and Monson 1998). When taken together, the seasonal studies and observations of plant organic N utilization suggest the following scenario. (1) Microbial populations decline before the plant growing season and release organic N. (2) This organic pulse provides N for plants. (3) N is immobilized into the soil microbial biomass after plants senesce in the fall, and is retained there throughout the winter. To test these hypotheses, we conducted a field study of changes in soil microbial biomass over the year, and the flux rate of amino acids in soil (proteolysis rate) during the plant growing season. To understand the role of the summer microbial community in contributing to proteolysis of soil protein and its potential to compete with plants for amino acids, we measured population sizes of microorganisms capable of growing with amino acids as their sole C source, and studied the amino acid uptake and protease activities of microbes isolated using a dilution culture method. Ultimately, we hoped to understand the links between microbial population dynamics and N availability for alpine plants.

MATERIALS AND METHODS

Study sites and sampling regime

The study site is located at the Niwot Ridge Long Term Ecological Research (LTER) site in the Front Range of the Colorado Rocky Mountains, United States (40 [degrees] 03 [minutes] N, 105 [degrees] 35 [minutes] W). The site is dominated by Kobresia myosuroides (Vill.) Paol. and Fiori, and the soil is classified as a pergellic cryumbrept.

On sampling dates during the first year of the study (1996-1997), at least three soil cores (10 cm deep, 5 cm diameter) were collected randomly across the landscape at each site. The study was extended into 19971998, but because of the sensitive nature of the alpine habitat, a less intensive regime was used. Smaller cores (1 cm diameter) were taken across the landscape and composited, so as to minimize disturbance to the site while providing a single, spatially averaged sample. Because they required a smaller amount of soil, protein measurements in 1997 were performed on the smaller cores before compositing, whereas substrate-induced growth response (SIGR) measurements were performed on the composited samples. On all sampling dates between November and April, soil was frozen solid. On these days, soil was excavated using a trowel, and was allowed to thaw at 3 [degrees] C overnight before processing. Soils were coarsely sieved (mesh size 4.75 mm) to remove rocks and plant material. All population measurements were initiated within 2 d of collection, during which time soils were kept refrigerated.

Microbial population measurements

We chose the substrate-induced growth response (SIGR) method as our primary measure of soil microbial biomass because it is free of some of the uncertainties inherent in other methods. When the chloroform fumigation-extraction (FE) method (Brookes et al. 1985) is used, uncertainty arises from variations in the effectiveness of the fumigation and extraction, and because no guarantee may be made as to the viability of the measured biomass. The substrate-induced respiration (SIR) method (Anderson and Domsch 1978) provides an index of potentially active biomass, but must be calibrated for each soil to yield an actual quantity of microbial biomass. The SIGR method is similar to the SIR method, but utilizes the full kinetics of respiration over time to produce a measurement of microbial biomass that is essentially independent of soil type (Schmidt 1992, Colores et al. 1996). This is the first test of this method in a ecological field study, and so SIR and FE were measured on a subset of samples to validate the SIGR method.