Microbes in nature are limited by carbon and energy: the starving-survival lifestyle in soil and consequences for estimating microbial rates

Abstract

Understanding microbial transformations in soils is important for predicting future carbon sequestration and nutrient cycling. This review questions some methods of assessing one key microbial process, the uptake of labile organic compounds. First, soil microbes have a starving-survival life style of dormancy, arrested activity, and low activity. Yet they are very abundant and remain poised to completely take up all substrates that become available. As a result, dilution assays with the addition of labeled substrates cannot be used. When labeled substrates are transformed into (14)CO2, the first part of the biphasic release follows metabolic rules and is not affected by the environment. As a consequence, when identical amounts of isotopically substrates are added to soils from different climate zones, the same percentage of the substrate is respired and the same half-life of the respired (14)CO2 from the labeled substrate is estimated. Second, when soils are sampled by a variety of methods from taking 10 cm diameter cores to millimeter-scale dialysis chambers, amino acids (and other organic compounds) appear to be released by the severing of fine roots and mycorrhizal networks as well as from pressing or centrifuging treatments. As a result of disturbance as well as of natural root release, concentrations of individual amino acids of ~10 μM are measured. This contrasts with concentrations of a few nanomolar found in aquatic systems and raises questions about possible differences in the bacterial strategy between aquatic and soil ecosystems. The small size of the hyphae (2-10 μm diameter) and of the fine roots (0.2-2 mm diameter), make it very difficult to sample any volume of soil without introducing artifacts. Third, when micromolar amounts of labeled amino acids are added to soil, some of the isotope enters plant roots. This may be an artifact of the high micromolar concentrations applied.

Keywords: activity; amino acids; labeled substrate; microbes; soil; sugars; water.

FIGURE 1

Soil respiration after addition of glucose, glycine, or water. 50 mM glucose (top), 50 mM glycine (middle), or rainwater (bottom) added to grassland soil at time 0. The basal respiration value of 209 μmol CO₂ kg^-1 h^-1 has been subtracted from all treatments. From Jones and Murphy (2007) with permission.

FIGURE 2

Leucine uptake kinetics in Atlantic Ocean. (A) Incorporation into bacteria of ³H-leucine at 6 nM concentrations. (B) The relationships between added amino acid concentrations and their corresponding turnover times. The error bars show single standard errors. The Y-axis intercept of the regression line is an estimate of turnover time at maximum bioavailable ambient concentration of amino acids. From Zubkov et al. (2008) with permission.

FIGURE 3

(A) Amount of ¹⁴C-amino acids remaining in soil sample after various periods of incubation. A mix of eleven labeled amino acids added and ¹⁴CO₂ released also measured. From Jones et al. (2004) with permission. (B) Amount of ¹⁴C-glucose remaining in soil solution after various periods and for various concentrations in final solution. From Hill et al. (2008) with permission.

FIGURE 4

¹⁴C-labeled glycine transformed to¹⁴CO₂ over time. The ¹⁴C-glycine at four concentrations (μM to mM) was added to a grassland soil (eutric cambisol) and transformation to ¹⁴CO₂ measured over time. From Jones et al. (2005b) with permission.

FIGURE 5

Laboratory study of Michaelis–Menten kinetics from the incorporation of glucose at a variety of concentrations by a lake bacteria culture (low K_m, low V_max) and an algal culture (Chlamydomonas sp., high K_m, high V_max). K_m of bacteria is 27 nM; K_m of algae is 27,000 nM. Note that uptake of algae resembles diffusion. Modified from Wright and Hobbie (1966).

FIGURE 6

Uptake of ¹⁴C-glycine at five concentrations from rhizosphere by maize plants. Plant values are means ± SEM (n = 5). From Jones et al. (2005b) with permission.