Soil Microorganisms Mediating Phosphorus Availability Update on Microbial Phosphorus

Abstract

Microorganisms are integral to the soil phosphorus (P) cycle and as such play an important role in mediating the availability of P to plants. Understanding the microbial contribution to plant P nutrition and opportunities for manipulating specific microorganisms to enhance P availability in soil has therefore been of considerable interest over many decades. This interest is accentuated by P deficiency being common in weathered and tropical soils throughout the world, by rising costs of P fertilizer, and because the efficiency of P use by plants from soil and fertilizer sources is often poor despite many soils containing a relatively large amount of total P that is only sparingly available to plants. The world’s high-quality sources of rock phosphate are finite and this itself justifies the need to develop plants and/or agricultural systems that are more P efficient. Utilization of microorganisms to increase the availability of P in soil therefore is an attractive proposition for developing a more sustainable agriculture. This is relevant to the high-input production systems of the developed world, and also to developing countries where access to mineral fertilizers is restricted (Sánchez, 2010). The concept of microbial enhancement of P availability to plants is not new. Gerretsen (1948) showed that pure cultures of soil bacteria could increase the P nutrition of plants under controlled conditions through solubilization of precipitated forms of calcium (Ca) phosphates. Since this study, many examples of microbially mediated P mobilization and characterization of different microorganisms have been reported (for review, see Richardson, 2001; Gyaneshwar et al., 2002; Khan et al., 2007, 2010; Harvey et al., 2009; Richardson et al., 2009a; Zaidi et al., 2009). However, despite considerable promise microbial products for P mobilization have not had major application to broad-acre farming systems. An exception to this is the commercialization of fungal-based inoculants in North America and more recently in Australia and Europe. Clearly, interactions between microorganisms and plants in soil environments are complex and with a few exceptions only (such as rhizobia, and to a much lesser extent mycorrhizal fungi), have proven difficult to manage and as a consequence responses to inoculants have been highly variable. In addition, P in soil is subject to extensive physicochemical and biological reactions with only a small component of total soil P being in a form directly available for plant or microbial uptake (Fig. 1). Uptake of P from soil solution occurs as orthophosphate via high-affinity transporters that in plants are localized to the root epidermis and are coordinately expressed in response to P deficiency and through interaction with mycorrhizal fungi (Bucher, 2007). P in soil exists predominantly in inorganic fractions that are either adsorbed to soil mineral surfaces or occur as sparingly available precipitates, and in organic forms that are either adsorbed, incorporated within biomass, or associated with soil organic matter. It is the dissolution (or mobilization) of orthophosphate from these forms, and rates of P diffusion within soil solution that represents the major limitation to adequate supply of P required for plant growth. In this Update we summarize current evidence concerning the role of free-living nonsymbiotic microorganisms in increasing the availability of P to plants. Critical issues that impede our understanding of microbially mediated P dynamics in the rhizosphere are outlined and opportunities for enhancing P mobilization are discussed. Schematic representation of the importance of microorganisms to P availability in soil. Microorganisms and their interactions in soil play a critical role in mediating the distribution of P between the available pool in soil solution and the total soil P through solubilization and mineralization reactions, and through immobilization of P into microbial biomass and/or formation of sparingly available forms of inorganic and organic soil P. Microorganisms can enhance the capacity of plants to acquire P from soil through various mechanisms that can be summarized as: (1) increased root growth through either an extension of existing root systems (e.g. mycorrhizal associations) or by hormonal stimulation of root growth, branching, or root hair development (phytostimulation; e.g. production of indole-3-acetic acid, GAs, or enzymes that alter plant ethylene precursors, such as 1-aminocyclopropane-1-carboxylate deaminase; Richardson et al., 2009a; Hayat et al., 2010); (2) alteration of sorption equilibria that may result in increased net transfer of orthophosphate ions into soil solution or facilitate the mobility of organic P either directly or indirectly through microbial turnover (Seeling and Zasoski, 1993); and (3) through induction of metabolic processes that are effective in directly solubilizing and mineralizing P from sparingly available forms of soil inorgan