Abstract
Soil organic matter (SOM) has a critical role in regulating soil phosphorus (P) dynamics and producing phytoavailable P. However, soil P dynamics are often explained mainly by the effects of soil pH, clay contents, and elemental compositions, such as calcium, iron, and aluminum. Therefore, a better understanding of the mechanisms of how SOM influences phytoavailable P in soils is required for establishing effective agricultural management for soil health and enhancement of soil fertility, especially P-use efficiency. In this review, the following abiotic and biotic mechanisms are discussed; (1) competitive sorption between SOM with P for positively charged adsorption sites of clays and metal oxides (abiotic reaction), (2) competitive complexations between SOM with P for cations (abiotic reaction), (3) competitive complexations between incorporation of P by binary complexations of SOM and bridging cations with the formation of stable P minerals (abiotic reaction), (4) enhanced activities of enzymes, which affects soil P dynamics (biotic reaction), (5) mineralization/immobilization of P during the decay of SOM (biotic reaction), and (6) solubilization of inorganic P mediated by organic acids released by microbes (biotic reaction).
Graphical Abstract
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Introduction
The soil ecosystem has a strong resilience capacity, an essential characteristic of natural ecosystems to resist changes and return to a state of equilibrium after suffering disturbance. Likewise, soil organic matter (SOM) would reach an equilibrium reflecting a certain balance between C inputs and losses if the natural (e.g., climate, topography, and soil parent materials) and human-induced factors (e.g., land-use and degradation) remain unchanged [90]. In reality, however, components of SOM continue to cycle and gradually change their properties over time as the natural and human-induced factors fluctuate, especially through the changes in climate and land management [90]. Currently, agricultural practices have been considered a source of C rather than a sink [64].
Phosphorus is an essential plant nutrient as well as N and K, thereby playing a pivotal role in the C cycle in terrestrial ecosystems [86]. It is known that plants mainly take P as a phosphate ion (i.e., H2PO4− or HPO42− and PO43−) from the soil, which is indicated as phytoavailable P in this review. In agricultural systems, amendments with mineral and organic fertilizers supply the P demands for crop growth and production since phytoavailable P in soil is generally very low [74]. From 2015 to 2020, the average annual growth rate of 2.3% for the global supply of P as P2O5 was applied in the soil–plant system, which is equivalent to 53 billion tons of P fertilizer [18]. However, most of the soluble P-fertilizers applied are quickly converted to forms unavailable for plant uptake. Added to the depletion of P-reserves worldwide, this places the issue of plant P-nutrition as a significant challenge to agricultural sciences and technology [73]. In addition, a large amount of P is considered to be stored with SOM; for example, storing 1000 kg of soil organic C (SOC) sequester ~ 13 kg P and ~ 22 kg P in the topsoil and the subsoil of croplands, respectively [80]. Since P is a macronutrient that limits primary production in many ecosystems, fixing a large amount of P into soils with SOM could be problematic [80]. However, the inorganic P fixed in soils as a part of SOM is unlikely as stable as P minerals fixed in soils, which could quickly become phytoavailable P [4].
Several studies show that adding organic matter (OM), such as organic amendments, prevents soil P fixation and enhances phytoavailable P in soils (e.g., see Table 1 and Fig. 1). However, phytoavailable P dynamics in soils are often explained with the effects of soil pH, clay contents, and elemental compositions of calcium, iron, and aluminum in soil solution, while the contribution of SOM to phytoavailable P is often ignored. The mechanisms of SOM influencing phytoavailable P include (1) competitive sorption between SOM with phosphate for positively charged adsorption sites of clays and metal oxides (abiotic reaction), (2) competitive complexations between SOM with phosphate for cations (abiotic reaction), (3) competitive complexations between incorporation of P by binary complexations of SOM and bridging cations with the formation of stable phosphate minerals (abiotic reaction), (4) enhanced activities of exoenzymes, which affects soil P dynamics (biotic reaction), (5) mineralization/immobilization of P during the decay of SOM (biotic reaction), and (6) solubilization of inorganic P mediated by organic acids released by microbes (biotic reaction) (Fig. 1).
Mechanisms of the effects of organic matter on soil P chemistry. 1. Competitive sorption can occur in three scenarios: (1) OM blocking surface charge on clay or oxide mineral leads to phosphate desorption; (2) OM adsorbing on negatively charged surface of clay or oxide mineral leads to negative phosphate repulsion; (3) OM complexing with Fe adsorbed on clay or oxide mineral surface leads to the formation of Fe–OM which can be released, leaving a positively charged surface available for phosphate sorption. 2. Competitive metal complexation occurs via ternary complexation between SOM and phosphate through cations like Ca2+, depending on SOM structures. In the absence of binary complexation with either Ca2+ or Fe3+ (red circle), the negative charge on SOM is unavailable to adsorb CaPO4−. However, when the negative charge on SOM is accessible, CaPO4− can form a ternary complex (blue circle). 3. Mineralization of Organic P: microbes induce enzymatic activities to break down organic P compounds into inorganic phosphate. This process involves the degradation of mono-, di-, and phosphotriesters by specific enzymes which release inorganic phosphate for plant uptake
We evaluate the abiotic and biotic mechanisms showing how OM or SOM influences phytoavailable P in soils.
Abiotic mechanisms
Competitive sorption reactions
The competitive sorption reactions between low molecular weight organic acids and phosphate were previously covered in the review by Guppy et al. [34], and the role of redox chemistry is discussed for similar systems in the context of wastewater-phosphate recovery by Wilfert et al. [97]. Here, we discuss the competitive sorption reactions for mainly other OM, such as dissolved organic matter (DOM) and SOM, including humic acids (HA) and fulvic acids (FA).
A range of organic amendments to soils, crop residues, animal manures, and other organic fertilizers have been shown to enhance phytoavailable P in soils [12, 38, 48] by reducing the phosphate adsorption while enhancing desorption of phosphate [100, 101]. Negatively charged OM is readily adsorbed onto the surfaces of positively charged clays and oxide minerals [75], thereby blocking adsorption reactions by negatively charged inorganic and organic P compounds. The sorbed OM can as well increase the repulsion of phosphate [38], thereby promoting an increase in phytoavailable P in soils (Fig. 1a). The nature of these competitive sorption reactions between SOM and phytoavailable P is summarized in Table 1.
In contrast, other studies have shown that OM additions to soils can increase phosphate sorption, decreasing phytoavailable P in soils (e.g., see Table 1). However, Guppy et al. [35] observed that the inhibition of phosphate sorption by the addition of DOM derived from decomposing OM was only short term (i.e., < 6 d). In addition, the authors suggested that previous studies of the inhibition of phosphate sorption by adding OM, such as DOM, HA, and FA, could be attributed to the phosphate contained within these OM sources [35]. However, in a study by Hunt et al. [38], which accounted for the phosphate contained in the amendment, inhibition of phosphate sorption onto metal hydroxides (i.e., goethite and gibbsite) by the addition of DOM extracted from plant biomass and dairy manure was shown.
This discrepancy in these contrasting findings can be explained mainly by the various structures of either OM molecules or the sorbing surface [38] and the availability of di- or poly-valent cations in the soils [26]. For example, the adsorption of DOM onto Fe-oxides (i.e., goethite) is mainly through multiple carboxylic functional groups (> 3) located closely spaced in the DOM and structurally specific H-bonding interactions [46]. In addition, phosphate bound to OM is mainly observed in the heavy OM fraction, which refers to organic material bound to mineral matter (i.e., up to 90% of total OM) [1], which means phosphate is likely bound binary OM–cation complexes [1], i.e., OM complexing with cations such as Fe3+, Al3+, Ca2+and Mg2+. Binary OM–cation complexes would incorporate phosphate [27], forming ternary complexes resulting in increasing phosphate sorption capacity (e.g., see Fig. 1b). We will discuss these mechanisms in the next section.
Competitive complexation reactions
Binary complexations between OM and cations
Di- and poly-valent cations, such as Ca2+, Mg2+, Al3+, and Fe3+, complex with OM to form binary complexes [26]. The formation of the binary complex is strongly influenced by C functional group ionization and molecular conformation, both of which are determined by the pH of the soil solution [21]. These di- and poly-valent cations complex with mainly carboxyl and phenolic functional groups in SOM [9, 41, 69]. Phenolic functional groups, especially those containing two or more OH groups on adjacent positions of the aromatic ring, chelate multivalent metal ions, such as Fe3+ and Al3+ [81], while, Ca2+ is assumed to bind mainly to carboxyl functional groups [54]. Previous studies reported that an electrostatic attraction plays an essential role in the bonding between carboxyl functional groups and either ferrihydrite (FH) [61] or Ca2+ [4].
High molecular weight OM consisting of hydrophobicity and aromatic structures can remarkably stabilize SOM [63, 79], thereby reducing mineral formations by enhancing stereochemical effects on blocking active crystal growth sites [37]. The formation of binary complexes is known to delay the transformation of labile inorganic phosphate forms, not strongly adsorbed in the soil. As a result, it may become phytoavailable P relatively quickly to stable phosphate minerals, including Ca–P or Fe–P minerals, such as apatite and strengite, respectively. Examples of these observations are summarized in Table 1. The following mechanisms could explain these reactions. Firstly, kinetically favored labile Ca–P minerals, such as brushite, can overgrow onto adsorbed surfaces of SOM fractions, including HA and FA [31], and thereby transformation of labile Ca–P to stable Ca–P is delayed. Secondly, SOM consisting of multiple negative-charge domains of phenolic or carboxyl functional groups either re-structure stable phosphate minerals such as apatite or strengite into a sponge-like structure or re-crystallize into more labile hydrated structures [101]. Lastly, the complexation of OM and FH is enhanced in the presence of Ca2+, especially pH above 7, by forming FH–Ca–OM ternary complexes, thereby decreasing the formation of stable Fe–P and Ca–P minerals [78].
Ternary complexations of OM, cations, and P
Organic matter forms binary complexes with cations and ternary complexes with anions, including phosphate, via cation bridging [24, 78]. Levesque and Schnitzer were the first to report the ternary formation of FA–metal–P complexes in 1967 [72]. Since then, potential formations of ternary complexes among OM fractions, P, and cations such as Fe3+, Al3+, and Ca2+ have been observed in agricultural lands, calcareous soils, wastewater treatments, and eutrophic lakes (e.g., see Table 1).
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Abbreviations
- Term:
-
Meaning
- SOM:
-
Soil organic matter
- SOC:
-
Soil organic carbon
- OM:
-
Organic matter
- DOM:
-
Dissolved organic matter
- DOC:
-
Dissolved organic carbon
- HA:
-
Humic acids
- FA:
-
Fulvic acids
- FH:
-
Ferrihydrite
- PSM:
-
P solubilizing microorganisms
- SSP:
-
Single superphosphate
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Acknowledgements
Yuki Audette, Scott Smith, and Paul Voroney would like to acknowledge the Ontario Ministry of Agriculture, Food and Rural Affairs (OMAFRA New Direction Grant ND2018-3410), Grain Farmers of Ontario (Grant C2019AG02) and Natural Sciences and Engineering Research Council of Canada (NSERC Discovery Grant 401267) for supporting this study. Keiji **do wishes to acknowledge financial support (3710473400).
Funding
Ontario Ministry of Agriculture, Food and Rural Affairs, OMAFRA New Direction Grant ND2018-3410; Grain Farmers of Ontario, Grant C2019AG02; Natural Sciences and Engineering Research Council of Canada, NSERC Discovery Grant 401267.
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KJ, YA, FLO, LCP, DSS, and RPV wrote the main manuscript text, and FLO prepared Fig. 1. All authors reviewed the manuscript. All authors read and approved the final manuscript.
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**do, K., Audette, Y., Olivares, F.L. et al. Biotic and abiotic effects of soil organic matter on the phytoavailable phosphorus in soils: a review. Chem. Biol. Technol. Agric. 10, 29 (2023). https://doi.org/10.1186/s40538-023-00401-y
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DOI: https://doi.org/10.1186/s40538-023-00401-y