Two-Phase Conceptual Framework of Phosphatase Activity and Phosphorus Bioavailability

Abstract

The activity of extracellular phosphatases is a dynamic process controlled by both plant roots and microorganisms, which is responsible for the mineralization of soil phosphorus (P). Plants regulate the availability of soil P through the release of root mucilage and the exudation of low-molecular weight organic acids (LMWOAs). Mucilage increases soil hydraulic conductivity as well as pore connectivity, both of which are associated with increased phosphatase activity. The LMWOAs, in turn, stimulate the mineralization of soil P through their synergistic effects of acidification, chelation, and exchange reactions. This article reviews the catalytic properties of extracellular phosphatases and their interactions with the rhizosphere interfaces. We observed a biphasic effect of root metabolic products on extracellular phosphatases, which notably altered their catalytic mechanism. In accordance with the proposed conceptual framework, soil P is acquired by both plants and microorganisms in a coupled manner that is characterized by the exudation of their metabolic products. Due to inactive or reduced root exudation, plants recycle P through adsorption on the soil matrix, thereby reducing the rhizosphere phosphatase activity. The two-phase conceptual framework might assist in understanding P-acquisition (substrate turnover) and P-restoration (phosphatase adsorption by soil) in various terrestrial ecosystems.

Keywords: LMWOAs; mucilage; phosphatase adsorption; phosphatase-soil interactions; root exudation; substrate catalysis.

Figure 1

A conceptual two-phase framework that integrates root exudation and soil environment as main drivers of soil phosphatase activity. The dotted lines in each block of main sections indicate their combined effects on phosphatase activity. Based on the conceptual framework block, Phase I shows the soil P_o acquisition pathway that is regulated by active root exudation, while Phase II shows soil P_o restoration in the absence or with reduced root exudation effects. Both phases are controlled by the P demand of plants with the initiation of P mining processes (green boxes) or by reducing C investment into P mining (yellow boxes).

Figure 2

A scheme visualizing the coupled relationship between plants and soil microbes for the acquisition of available soil P resources and/or P mineralization induced via phosphatase activity. Root exudation of mucilage and LMWOAs exert favorable physicochemical and hydraulic changes in the rhizosphere for P accessibility. Soil microbes ensure a mutual relationship with plant roots by the production of phosphatases and release of LMWOAs, which favor P supply from soil P reservoir.

Figure 3

A summary of the interactions between soil colloidal and organic matter surfaces and extracellular enzymes and their effect on enzyme–substrate complex formation.

Figure 4

A conceptual two-phase framework for predicting P bioavailability in ecosystems based on phosphatase activity and soil phosphatase interactions. In “Phase I”, plants acquire soil P via phosphatase activity, which is controlled by a coupled relationship (biotic relations) with soil microorganisms in the presence of exuded metabolic products such as mucilage and LMWOAs. The “phase II” is characterized by the conservation of soil P resources under the dominance of biotic and abiotic interaction among microbes, phosphatases, and the different P forms with the soil mineral surfaces in the absence of root exudation. During phase II, extracellular phosphatases are immobilized and adsorbed onto colloidal and mineral soil surfaces, which inhibits their activities through modifications in hydraulic and physicochemical properties. CI, competitive inhibition; non-CI, non–competitive inhibition; ES, enzyme–substrate; EI, enzyme–inhibitor; ESI, enzyme–substrate–inhibitor.