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

Alberto Andrino; Georg Guggenberger; Sarmite Kernchen; Robert Mikutta; Leopold Sauheitl; Jens Boy

doi:10.3389/fpls.2021.661842

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

Front Plant Sci. 2021 Jul 15:12:661842. doi: 10.3389/fpls.2021.661842. eCollection 2021.

Authors

Alberto Andrino¹, Georg Guggenberger¹, Sarmite Kernchen², Robert Mikutta³, Leopold Sauheitl¹, Jens Boy¹

Affiliations

¹ Institute of Soil Science, Leibniz Universität Hannover, Hanover, Germany.
² Bayreuth Center of Ecology and Environmental Research, University of Bayreuth, Bayreuth, Germany.
³ Soil Science and Soil Protection, Martin Luther University Halle-Wittenberg, Halle (Saale), Germany.

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.

Keywords: arbuscular mycorrhiza; inorganic P; iron oxides; ligand exchange; low-molecular-weight organic acid; membrane fluidity; organic P; reductive dissolution.