A consideration of the relative contributions of different microbial subpopulations to the soil N cycle

Abstract

We examine and discuss literature targeted at identifying "active" subpopulations of soil microbial communities with regard to the factors that affect the balance between mineralization and immobilization/assimilation of N. Whereas a large fraction (≥50%) of soil microbial biomass can immediately respire exogenous substrates, it remains unclear what percentage of both bacterial and fungal populations are capable of expressing their growth potential. The factors controlling the relative amounts of respiratorily responsive biomass versus growth-active biomass will impact the balance between N mineralization and N immobilization. Stable isotope probing of de novo DNA synthesis, and pyrosequence analyses of rRNA:rDNA ratios in soils have identified both numerically dominant and rare microbial taxa showing greatest growth potential. The relative growth responses of numerically dominant or rare members of a soil community could influence the amount of N immobilized into biomass during a "growth" event. Recent studies have used selective antibiotics targeted at protein synthesis to measure the relative contributions of fungi and bacteria to ammonification and [Formula: see text] consumption, and of NH(3)-oxidizing archaea (AOA) and bacteria (AOB) to NH(3) oxidation. Evidence was obtained for bacteria to dominate [Formula: see text] assimilation and for fungi to be involved in both consumption of dissolved organic nitrogen (DON) and its ammonification. Soil conditions, phase of cropping system, [Formula: see text] availability, and soil pH influence the relative contributions of AOA and AOB to soil nitrification. A recent discovery that AOA can ammonify organic N sources and oxidize it to [Formula: see text] serves to illustrate roles for AOA in both the production and consumption of [Formula: see text]. Clearly, much remains to be learned about the factors influencing the relative contributions of bacteria, archaea, and fungi to processing organic and inorganic N, and their impact on the balance between mineralization and immobilization of N.

Keywords: N immobilization; N mineralization; ammonium consumption; dominant and rare taxa; growth active subpopulations; nitrification; nitrogen cycling; substrate-responsive subpopulations.

FIGURE 1

Diagram of the microbial N cycle in aerobic soil. Major pools of N are shown in circles, major fluxes by solid arrows, and the dashed arrow represents the production of exoenzymes (e.g., proteases) for the depolymerization of soil organic N. Pools and fluxes in dark gray relate to turnover of dissolved organic N, those in light gray relate to turnover of ${\mathrm{N}\mathrm{H}}_4^{+}$, and unshaded to turnover of ${\mathrm{N}\mathrm{O}}_3^{-}$. Based on Myrold and Bottomley (2008).

FIGURE 2

Conceptual diagram to illustrate how the fate of soil N pools might be controlled by the growth-active fraction (GAF) of the substrate-responsive population (SRP) of microorganisms. The heights of the individual vertical columns represent the SRP of different taxa and their widths represent the relative sizes of each taxa as part of the whole microbial community. The shaded portion of each column represents the GAF of each SRP taxon. The left side depicts that low molecular weight (LMW) dissolved organic N (DON) is taken up and metabolized by the SRP but N is only assimilated by the GAF. The balance between ${\mathrm{N}\mathrm{H}}_4^{+}$ mineralized versus N immobilized will be influenced by the relative amounts of GAF versus SRP and determine the net ${\mathrm{N}\mathrm{H}}_4^{+}$ mineralized. The right panel depicts that growth-active heterotrophs and NH₃-oxidizing archaea (AOA) and bacteria (AOB) will compete for ${\mathrm{N}\mathrm{H}}_4^{+}/{\mathrm{N}\mathrm{H}}_3$ with the outcome being affected by the GAF/SRP ratio of the ${\mathrm{N}\mathrm{H}}_4^{+}/{\mathrm{N}\mathrm{H}}_3$ assimilating heterotrophs (assuming that AOA and AOB only assimilate a small fraction of ${\mathrm{N}\mathrm{H}}_4^{+}$ consumed) and by the relative sizes of and kinetic properties of the SRP populations of AOA and AOB. A similar panel could be drawn to show the assimilation of ${\mathrm{N}\mathrm{O}}_3^{-}$ by the GAF of heterotrophic microorganisms.