Production of Organic Acids by Arbuscular Mycorrhizal Fungi and Their Contribution in the Mobilization of Phosphorus Bound to Iron Oxides

Abstract

Most plants living in tropical acid soils depend on the arbuscular mycorrhizal (AM) symbiosis for mobilizing low-accessible phosphorus (P), due to its strong bonding by iron (Fe) oxides. The roots release low-molecular-weight organic acids (LMWOAs) as a mechanism to increase soil P availability by ligand exchange or dissolution. However, little is known on the LMWOA production by AM fungi (AMF), since most studies conducted on AM plants do not discriminate on the LMWOA origin. This study aimed to determine whether AMF release significant amounts of LMWOAs to liberate P bound to Fe oxides, which is otherwise unavailable for the plant. Solanum lycopersicum L. plants mycorrhized with Rhizophagus irregularis were placed in a bicompartmental mesocosm, with P sources only accessible by AMF. Fingerprinting of LMWOAs in compartments containing free and goethite-bound orthophosphate (OP or GOE-OP) and phytic acid (PA or GOE-PA) was done. To assess P mobilization via AM symbiosis, P content, photosynthesis, and the degree of mycorrhization were determined in the plant; whereas, AM hyphae abundance was determined using lipid biomarkers. The results showing a higher shoot P content, along with a lower N:P ratio and a higher photosynthetic capacity, may be indicative of a higher photosynthetic P-use efficiency, when AM plants mobilized P from less-accessible sources. The presence of mono-, di-, and tricarboxylic LMWOAs in compartments containing OP or GOE-OP and phytic acid (PA or GOE-PA) points toward the occurrence of reductive dissolution and ligand exchange/dissolution reactions. Furthermore, hyphae grown in goethite loaded with OP and PA exhibited an increased content of unsaturated lipids, pointing to an increased membrane fluidity in order to maintain optimal hyphal functionality and facilitate the incorporation of P. Our results underpin the centrality of AM symbiosis in soil biogeochemical processes, by highlighting the ability of the AMF and accompanying microbiota in releasing significant amounts of LMWOAs to mobilize P bound to Fe oxides.

Root metabolome of plant–arbuscular mycorrhizal symbiosis mirrors the mutualistic or parasitic mycorrhizal phenotype

“…However, previous studies have indicated that the amount of carboxylates in the rhizosphere decreased when the plants were colonized with AMF (Ryan et al ., 2012; Nazeri et al ., 2014). This could be due to the release of organic acids by AMF through hyphal exudates for the uptake of P (Tawaraya et al ., 2006; Andrino et al ., 2021). As we have not measured the rhizosphere carboxylates, we speculate that the higher abundance of organic acids in roots of AMF treatments that exhibited a mutualistic phenotype could be potentially because AMF managed to uptake P by utilizing the hyphal exudates.…”

Genome-wide comparison deciphers lifestyle adaptation and glass biodeterioration property of Curvularia eragrostidis C52

“…Since iron is required for virtually all biological systems, in A. niger , citric acid was demonstrated to function as iron siderophore to increase the bioavailability of iron represented as Fe(III) citrate 38 . Moreover, arbuscular mycorrhizal fungi such as Rhizophagus irregularis secretes a significant amount of organic acids (acetic, butyric, lactic, citric gluconic, malic, and oxalic acids) to sequester low-accessible phosphorus from Fe oxides 39 . Combining our results, it seems that the production of organic acids is such a critical mechanism to help fungi survive under metal-rich environments.…”

Mycorrhizal Symbionts and Associated Bacteria: Potent Allies to Improve Plant Phosphorus Availability and Food Security

“…strains were able to solubilize phosphate and to become strongly attached to R. irregularis mycelium (Taktek et al, 2015 ), while 12 out of 128 bacterial strains isolated from Rhizoglomus irregulare mycelium showed phosphate-solubilizing activity (Sharma et al, 2020 ) and 70% of bacteria isolated from R. irregularis spores were able to mineralize P (Battini et al, 2016 ). The mechanism underlying such activities was ascribed to the production of organic acids by AMF and associated microbiota (Andrino et al, 2021 ). A recent study reported that phosphate solubilising bacteria migrated along extraradical AMF mycelium toward a phytate source, which they were able to mineralise (Jiang et al, 2021 ).…”