TY - JOUR

T1 - From rock eating to vegetarian ecosystems

T2 - Disentangling processes of phosphorus acquisition across biomes

AU - Koester, Moritz

AU - Stock, Svenja C.

AU - Nájera, Francisco

AU - Abdallah, Khaled

AU - Gorbushina, Anna

AU - Prietzel, Jörg

AU - Matus, Francisco

AU - Klysubun, Wantana

AU - Boy, Jens

AU - Kuzyakov, Yakov

AU - Dippold, Michaela A.

AU - Spielvogel, Sandra

N1 - Funding Information: We thank the Chilean National Park Service Corporaci?n Nacional Forestal (CONAF) for granting permission to work in the National parks Nahuelbuta and La Campana. We also thank the Center for Advanced Research in Arid Zones (CEAZA) for the opportunity to work in the Nacional Reserve Santa Gracia. We express gratitude to the team of Beamline 8 at the Synchrotron Light Research Institute Nakhon Ratchasima. Without their help in setting up the beamline we would not have been able to produce high quality spectra. We thank the Robert Bosch Foundation for supporting this research within the framework of the junior professorship in 2017. Last but not least we thank Karin Schmidt for her help with laboratory analysis. This study was funded by the German Research Foundation (DFG) within the frame of the priority program 1803, EarthShape: Earth surface shaping by biota (DFG SPP 1803; project number 255469939) under the subprojects KU 1184/36-1 and DI 2136-11.

PY - 2021/4/15

Y1 - 2021/4/15

N2 - Low-molecular-weight organic acids (LMWOAs) are crucial for the mobilization and acquisition of mineral phosphorus by plants. However, the role of LMWOAs in mobilizing organic phosphorus, which is the predominant phosphorus form in at least half of the world's ecosystems, especially in humid climates, is unclear. The mechanisms of phosphorus mobilization by LMWOAs depend on climate, mainly precipitation, and shape the phosphorus nutrition strategies of plants. We disentangled the impact of roots and associated microorganisms on mechanisms of phosphorus cycling mediated by LMWOAs by studying soils along an ecosystem-sequence (ecosequence) from arid shrubland (~70 mm yr −1), and Mediterranean woodland (~370 mm yr −1) to humid-temperate forest (~1470 mm yr −1). Phosphorus speciation in soil was examined by X-ray absorption near edge structure analysis (XANES). LMWOAs were quantified as biological rock-weathering and organic phosphorus mobilization agents and compared to kinetics of acid phosphatase as a proxy for organic phosphorus mineralization. Calcium-bound phosphorus in topsoils decreased from 126 mg kg −1 in the arid shrubland, to 19 mg kg −1 in the Mediterranean woodland and was undetectable in the humid-temperate forest. In contrast, organic phosphorus in topsoils in close root proximity (0–2 mm distance to roots) was absent in the arid shrubland but raised to 220 mg kg −1 in the Mediterranean woodland and to 291 mg kg - 1 in the humid-temperate forest. The organic phosphorus content in topsoils was 1.6 to 2.4 times higher in close root proximity (0–2 mm distance to roots) compared to bulk soil (4–6 mm distance to roots) in the Mediterranean woodland and humid-temperate forest, showing intensive phosphorus bioaccumulation in the rhizosphere. Redundancy analysis (RDA) revealed that LMWOAs were explained by the content of hydroxyapatite and variscite phosphorus-species in the arid shrubland, indicating that LMWOAs contribute to mineral weathering in this soil. LMWOA contents, phosphatase activity, and microbial biomass carbon correlated strongly with organic phosphorus in the humid-temperate forest soil, which implies a high relevance of LMWOAs for organic phosphorus recycling. In the Mediterranean woodland soil, however, oxalic acid correlated with organic phosphorus in the topsoil (suggesting phosphorus recycling), whereas in the subsoil malic and citric acid were correlated with primary and secondary phosphorus minerals (implying mineral weathering). We conclude that phosphorus acquisition and cycling depend strongly on climate and that the functions of LMWOAs in the rhizosphere change fundamentally along the precipitation gradient. In the arid shrubland LMWOAs facilitate biochemical weathering (rock eating), while in the humid-temperate forest their functions change towards supporting organic phosphorus recycling (vegetarian).

AB - Low-molecular-weight organic acids (LMWOAs) are crucial for the mobilization and acquisition of mineral phosphorus by plants. However, the role of LMWOAs in mobilizing organic phosphorus, which is the predominant phosphorus form in at least half of the world's ecosystems, especially in humid climates, is unclear. The mechanisms of phosphorus mobilization by LMWOAs depend on climate, mainly precipitation, and shape the phosphorus nutrition strategies of plants. We disentangled the impact of roots and associated microorganisms on mechanisms of phosphorus cycling mediated by LMWOAs by studying soils along an ecosystem-sequence (ecosequence) from arid shrubland (~70 mm yr −1), and Mediterranean woodland (~370 mm yr −1) to humid-temperate forest (~1470 mm yr −1). Phosphorus speciation in soil was examined by X-ray absorption near edge structure analysis (XANES). LMWOAs were quantified as biological rock-weathering and organic phosphorus mobilization agents and compared to kinetics of acid phosphatase as a proxy for organic phosphorus mineralization. Calcium-bound phosphorus in topsoils decreased from 126 mg kg −1 in the arid shrubland, to 19 mg kg −1 in the Mediterranean woodland and was undetectable in the humid-temperate forest. In contrast, organic phosphorus in topsoils in close root proximity (0–2 mm distance to roots) was absent in the arid shrubland but raised to 220 mg kg −1 in the Mediterranean woodland and to 291 mg kg - 1 in the humid-temperate forest. The organic phosphorus content in topsoils was 1.6 to 2.4 times higher in close root proximity (0–2 mm distance to roots) compared to bulk soil (4–6 mm distance to roots) in the Mediterranean woodland and humid-temperate forest, showing intensive phosphorus bioaccumulation in the rhizosphere. Redundancy analysis (RDA) revealed that LMWOAs were explained by the content of hydroxyapatite and variscite phosphorus-species in the arid shrubland, indicating that LMWOAs contribute to mineral weathering in this soil. LMWOA contents, phosphatase activity, and microbial biomass carbon correlated strongly with organic phosphorus in the humid-temperate forest soil, which implies a high relevance of LMWOAs for organic phosphorus recycling. In the Mediterranean woodland soil, however, oxalic acid correlated with organic phosphorus in the topsoil (suggesting phosphorus recycling), whereas in the subsoil malic and citric acid were correlated with primary and secondary phosphorus minerals (implying mineral weathering). We conclude that phosphorus acquisition and cycling depend strongly on climate and that the functions of LMWOAs in the rhizosphere change fundamentally along the precipitation gradient. In the arid shrubland LMWOAs facilitate biochemical weathering (rock eating), while in the humid-temperate forest their functions change towards supporting organic phosphorus recycling (vegetarian).

KW - Biogenic weathering

KW - Climate gradient

KW - Low-molecular-weight organic substances

KW - Organic phosphorus breakdown

KW - Phosphorus K-edge-XANES spectroscopy

KW - Rhizosphere processes

UR - http://www.scopus.com/inward/record.url?scp=85096877627&partnerID=8YFLogxK

U2 - 10.1016/j.geoderma.2020.114827

DO - 10.1016/j.geoderma.2020.114827

M3 - Article

VL - 388

JO - GEODERMA

JF - GEODERMA

SN - 0016-7061

M1 - 114827

ER -