Inoculation of phosphate-solubilizing bacteria improves soil phosphorus mobilization and maize productivity

Nutr Cycl Agroecosyst https://doi.org/10.1007/s10705-023-10268-y ORIGINAL ARTICLE Inoculation of phosphate‑solubilizing bacteria improves soil phosphorus mobilization and maize productivity Isidro Beltran‑Medina · Felipe Romero‑Perdomo · Lady Molano‑Chavez · Angelica Y. Gutiérrez · Antonio M. M. Silva German Estrada‑Bonilla · Received: 1 August 2022 / Accepted: 20 February 2023 © The Author(s) 2023 Abstract Phosphate-solubilizing bacteria represent a bioalternative in making soil-immobilized phosphorus (P) available to plants, and consequently improve agriculture sustainability and reduce nutrient pollution. In this study, we examined whether Rhizobium sp. B02 inoculation can affect the soil P fractions. Moreover, we investigated how inoculation influences the growth, physiological traits, and productivity of the maize crop. Field tests were carried out to evaluate the combined application of strain B02 and reduced doses of P fertilizer. Soil P fractionation was performed after crop harvesting, assessing the Isidro Beltran-Medina and Felipe Romero-Perdomo have contributed equally. Supplementary Information The online version contains supplementary material available at https://doi. org/10.1007/s10705-023-10268-y. I. Beltran‑Medina Corporación Colombiana de Investigación Agropecuaria AGROSAVIA - C.I. Nataima, Espinal, Tolima, Colombia F. Romero‑Perdomo · L. Molano‑Chavez · A. Y. Gutiérrez · G. Estrada‑Bonilla (*) Corporación Colombiana de Investigación Agropecuaria AGROSAVIA - C.I. Tibaitatá, Mosquera, Cundinamarca, Colombia e-mail: ; A. M. M. Silva Departamento de Ciência do Solo, Escola Superior de Agricultura “Luiz de Queiroz”, Universidade de São Paulo, Piracicaba, São Paulo, Brazil P dynamics. To study the plant response, samplings were carried out in three phenological stages—the vegetative stage of the 7 fully emerged leaves with leaf collars (V7), the vegetative stage of the tassel (VT), and the reproductive stage of physiological maturity (R6). Using 50% of P fertilizer recommended, the strain inoculation increased the labile inorganic P fraction by 14% compared to the control treatment at the same dose, indicating that it favored the Pi mobility. Under these same conditions in the V7 and VT phenological stages, the inoculation significantly improved shoot length (28 and 3%) and shoot dry weight (9.8 and 12%). B02 inoculation increased grain yield by 696 kg ha−1 using 50% of the recommended rate of P fertilizer, phenocopying the complete P fertilization treatment without inoculation. Therefore, Rhizobium sp. B02 inoculation replaced 50% of P fertilizer in maize and increased the soil P availability. Keywords Fertilization · PGPB · Phosphorus availability · Phosphorus legacy · Phosphorus recovery Introduction Phosphorus (P) is a fundamental and irreplaceable element for living organisms. It impacts agricultural productivity and environmental pollution. Large amounts of P have accumulated in soils, but Vol.: (0123456789) 13 Nutr Cycl Agroecosyst less than 5% are available for use by plants (Lambers 2022). It has been estimated that 5.7 billion hectares of land globally contain insufficient amounts of available P for crop production, thus demanding P fertilizer inputs (Drohan et al. 2019). However, part of the applied P is fixed in soils due to high-affinity reactions with soil particles. The amount of P applied to the soil is markedly higher than the amount of P absorbed by plants, leading to a surplus of soil P over time (Gatiboni et al. 2020), and in some cases excessive doses of P fertilizers are applied to compensate for P fixation (Alewell et al. 2020). Excess P in soil causes deficiencies of micronutrients such as zinc and iron (Xu et al. 2022). It also generates P runoff, which causes nutrient over-enrichment in agricultural watersheds and possibly results in irreversible effects on aquatic ecosystems (Wildemeersch et al. 2022). Therefore, improving P management is a priority when it comes to sustaining future food supplies and sustainably managing the environment (Haygarth et al. 2021). Soil P recovery is an approach that closes the P cycling and thus increases P availability (Withers 2019). One of the most crucial roles in this approach is played by legacy P (Yuille et al. 2022). This represents the accumulated P in soil over the years (Doydora et al. 2020). Legacy P can be found in soils in various chemical fractions, classified as labile, moderately labile, and non-labile P (Mezeli et al. 2020). Legacy P in arable lands (i.e., Africa, South America, and Eastern Europe) is estimated at a minimum of 347 kg P h a−1 within a 0–0.2 m deep soil layer, which could be sufficient to sustain global P demands for approximately 9–22 years (Rowe et al. 2015; Liu et al. 2017). The potential use of legacy P would reduce harmful P accumulation, provide economic benefits in P fertilizer inputs, mitigate pressure on phosphate rock reserves, and improve crop P use efficiency (Withers et al. 2020). Cereal production worldwide stands out as having a low efficiency of P use, which varies between 9 and 12% (Yu et al. 2021). In particular, P is the second most demanded nutrient by maize plants (Zea mays L.) and its lack critically limits crop development and yield (Yan et al. 2021). Low soil P availability for maize strongly decreases root growth, stem strength, crop quality, and grain yield and leads to non-uniform and later crop maturity (Zhang et al. 2021). Tropical and subtropical soils Vol:. (1234567890) 13 usually have strong P adsorption caused by hydroxides of aluminum and iron, as well as crystalline and amorphous oxides, alongside accumulation processes or organic matter stabilization (Damian et al. 2020). Consequently, many countries are facing cost overruns and non-self-sufficient production when it comes to maize (Barbieri et al. 2022). Soil microorganisms such as phosphate-solubilizing bacteria (PSB) are able to access legacy P, making it available to plants, and thus leading to a reduction in the P fertilizer needs of crops (de-Bashan et al. 2021). The most representative PSB genera are Pseudomonas, Bacillus, Gluconobacter, and Burkholderia, while other genera, such as Rhizobium, have been less investigated (Alori et al. 2017). The metabolic mechanisms of PSB to mineralize organic phosphorus (Po) are the production of phytases, phosphomonoesterases, and phospholipases, while those to solubilize inorganic phosphorus (Pi) are the synthesis of organic acids and release of protons and hydroxyl or bicarbonate ions (Granada et al. 2018; Hinsinger 2001). The metabolic activities of PSB have been widely investigated, mainly under in vitro conditions with insoluble Pi sources (Zeng et al. 2022). Numerous studies have focused on the influence of inoculation both on plant development and the total P accumulation in the soil (De Zutter et al. 2022; Bargaz et al. 2021). However, whether PSB inoculation increases the availability of soil legacy P remains largel (...truncated)