sustainability Article Fertilizer Potential of Struvite as Affected by Nitrogen Form in the Rhizosphere Andrea Danaé Gómez-Suárez 1,2,Cécile Nobile 1 , Michel-Pierre Faucon 1, Olivier Pourret 1 and David Houben 1,* 1 UniLaSalle, AGHYLE, 60026 Beauvais, France; [email protected] (A.D.G.-S.); [email protected] (C.N.); [email protected] (M.-P.F.); [email protected] (O.P.) 2 Facultad de Ciencias Químicas, Universidad La Salle, Mexico City 06140, Mexico * Correspondence: [email protected]; Tel.: +33-3-44-06-93-45 Received: 14 February 2020; Accepted: 10 March 2020; Published: 12 March 2020 Abstract: Struvite is increasingly considered a promising alternative to mined phosphorus (P) fertilizer. However, its solubility is very low under neutral to alkaline pH while it increases with acidification. Here, we investigated whether supplying ammonium to stimulate rhizosphere acidification might improve struvite solubility at the vicinity of roots and, ultimately, enhance P uptake by plants. Using a RHIZOtest design, we studied changes in soil pH, P availability and P uptake by ryegrass in the rhizosphere and bulk soil supplied with either ammonium or nitrate under three P treatments: no-P, triple super phosphate and struvite. We found that supplying ammonium decreased rhizosphere pH by more than three units, which in turn increased soluble P concentrations by three times compared with nitrate treatments. However, there was no difference between P treatments, which was attributed to the increase of soluble Al concentration in the rhizosphere, which subsequently controlled P availability by precipitating it under the form of variscite-like minerals (predicted using Visual MINTEQ). Moreover, although ammonium supply increased soluble P concentration, it did not improve P uptake by plants, likely due to the absence of P deficiency. Further studies, especially in low-P soils, are thus needed to elucidate the role of nitrogen form on P uptake in the presence of struvite. More generally, our results highlight the complexity of manipulating rhizosphere processes and stress the need to consider all the components of the soil-plant system. Keywords: phosphorus management; ammonium; nitrate; recycled phosphorus; RHIZOtest; acidification 1. Introduction Phosphorus (P) is a major nutrient limiting crop production of many agroecosystems [1]. Currently, P fertilization mainly relies on the use of chemical fertilizers which are derived from phosphate rocks [2]. However, this resource is finite and is located in only a few places on Earth [3]. Developing sustainable fertilization practices based on the reuse of P is thus crucial to achieve the high yields required to feed an ever-increasing human population [4,5]. In this context, it has been increasingly suggested to replace conventional fertilizer with P-rich materials originating from waste materials [6], especially to achieve United Nations Sustainable Development Goals [7]. Considerable interest in the P removal from effluent and recovery in the form of struvite (magnesium ammonium phosphate hexahydrate, MgNH PO 6H O) has arisen in recent years 4 4· 2 worldwide [8–10]. Struvite production has been considered a promising alternative to conventional P removal technologies (e.g., metal precipitation with Fe or Al salts) in which P precipitates are virtually impossible to recycle in an economical manner [11–13]. Once applied to soil, struvite may act as a Sustainability 2020, 12, 2212; doi:10.3390/su12062212 www.mdpi.com/journal/sustainability Sustainability 2020, 12, 2212 2 of 11 “slow-release fertilizer”, providing a longer-term source of P for crop growth than readily soluble forms of P whileSustainability preventing 2020, 12, Px FOR from PEER sorption REVIEW on soil constituents or loss by leaching or runoff [14,15].2 However, of 12 the use of struvite might also result in an insufficient supply of P to crops, especially at the early stage of growth,virtually if impossible the release to is recycle slower in thanan economical the plant manner requirements [11–13]. Once for P applied [15–17 ].to Struvitesoil, struvite solubility may is predominantlyact as a “slow-release controlled fertilizer”, by pH [9]. providing High pH a favorslonger-term the formation source of ofP for struvite crop growth crystals than (pH readily range of 7 soluble forms of P while preventing P from sorption on soil constituents or loss by leaching or runoff to 11), whereas low pH favors its solubilization [18]. As a result, unlike the highly soluble commercial [14,15]. However, the use of struvite might also result in an insufficient supply of P to crops, especially P fertilizersat the early such stage as potassium of growth, if phosphate, the release is which slower are than bioavailable the plant requirements over a broad for pH P [15–17]. range, Struvite uptake of P fromsolubility struvite canis predominantly be low at neutral controlled to alkaline by pH pH [9]. [High19]. pH favors the formation of struvite crystals Rhizosphere(pH range of 7 processes to 11), whereas such aslow root-induced pH favors its changes solubilization in pH [18]. or redox As a result, potential unlike and the root highly exudate releasesoluble play acommercial key role in P nutrientfertilizers acquisition such as potassiu [20].m It phosphate, has long been which known are bioavailable that rhizosphere over a broad chemistry can bepH significantly range, uptake changed of P from according struvite can to be the low form at neutral of N takento alkaline up. AmmoniumpH [19]. (NH4+) supply may + decrease rhizosphereRhizosphere processes pH by promotingsuch as root-induced H release, changes whereas in pH nitrateor redox (NO potential3−) supply and root may exudate increase release play a key role in nutrient acquisition [20]. It has long been known that rhizosphere chemistry rhizosphere pH through releasing OH− [21], which can in turn affect the availability of sparingly can be significantly changed according to the form of N taken up. Ammonium (NH4+) supply may soluble P compounds [22]. For instance, supplying plants with NH4-N could increase the solubility decrease rhizosphere pH by promoting H+ release, whereas nitrate (NO3-) supply may increase of sparingly soluble P compounds such as apatite, resulting in higher P availability compared with rhizosphere pH through releasing OH− [21], which can in turn affect the availability of sparingly the supply of NO -N [23,24]. Since struvite solubility is strongly dependent on pH, such observation soluble P compounds3 [22]. For instance, supplying plants with NH4-N could increase the solubility raisesof the sparingly question soluble of whether P compounds manipulation such as apatite, of rhizosphere resulting in processeshigher P availability by stimulating compared rhizosphere with acidificationthe supply through of NO3-N NH [23,24].4-N supply Since struvite might besolubility an effective is strongly approach dependent to improve on pH, struvitesuch observation solubility at the vicinityraises the of roots.question On of the whether other hand, manipulation root-induced of rhizosphere acidification proc inesses the by rhizosphere stimulating of rhizosphere NH4-fed plants may increaseacidification the through concentration NH4-N supply of Al inmight solution be an [effective25], potentially approach resulting to improve in struvite toxicity solubility for plants at [26] and Pthe precipitation vicinity of roots. as variscite, On the AlPOother hand,2H O[root27-induced]. acidification in the rhizosphere of NH4-fed 4· 2 Inplants order may to increase optimize the concentration the use of more of Al in sustainable solution [25], P potentially sources, the resulting objective in toxicity of this for studyplants was therefore[26] and to gain P precipitation a better insight as variscite, on how AlPO the4.2H N2O form [27]. a ffects P availability in the presence of struvite. In order to optimize the use of more sustainable P sources, the objective of this study was We hypothesize that adding NH -N would acidify the rhizosphere, resulting in higher P uptake as therefore to gain a better insight4 on how the N form affects P availability in the presence of struvite. compared to the supply of NO -N. We hypothesize that adding3 NH4-N would acidify the rhizosphere, resulting in higher P uptake as compared to the supply of NO3-N. 2. Materials and Methods 2. Materials and Methods 2.1. Experimental Design The2.1. Experimental studied soil Design was sampled in Beauvais (Northern France; Figure1) and was classified as a Haplic LuvisolThe studied [28]. Asoil total was mass sampled of 100 in kgBeauvais was obtained (Northern by France; composite Figure sampling 1) and was (0–10 classified cm depth; as a five randomHaplic samplings) Luvisol [28]. in a A long-term total mass (> of20 100 years) kg was cropland obtained field by composite with an oilseed sampling rape–winter (0–10 cm depth; wheat–winter five barleyrandom rotation samplings) and organic in a andlong-term mineral (> 20 fertilization years) cropland based field on soilwith tests, an oilseed crop requirementsrape–winter wheat– and timed to cropwinter uptake barley [5, 29rotation]. and organic and mineral fertilization based on soil tests, crop requirements and timed to crop uptake [5,29]. Figure 1. Location of the sampling site. Figure 1. Location of the sampling site. Sustainability 2020, 12, 2212 3 of 11 After sampling, the soil was air-dried, crushed and sieved at 2 mm for further use at the laboratory. Particle size analysis using the pipette method revealed that the soil was a silt loam (USDA classification) with 16% sand, 67% silt, and 17% clay. Organic C, total N, available concentrations as assessed using the acetate ammonium-ethylenediamine tetraacetic acid (AA-EDTA), pH and cation exchange capacity (CEC) are presented in Table1. Table 1. Soil characteristics. Organic C Total N CaAA-EDTA MgAA-EDTA KAA-EDTA PAA-EDTA CEC 1 1 1 1 pH 1 (%) (%) (mg kg− ) (mg kg− ) (mg kg− ) (mg kg− ) (cmolc kg− ) 1.54 0.18 3869 101 292 72 7.8 12.5 At the laboratory, the soil was amended with an appropriate amount of powder of struvite or 1 triple superphosphate (TSP) corresponding to 50 mg P kg− soil, as recommended by Bonvin et al.