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Article

Sewage Sludge Ash-Based Biofertilizers as a Circular Approach to Phosphorus: The Issue of Fe and Al in Soil and Wheat and Weed Plants

by
Magdalena Jastrzębska
1,*,
Marta K. Kostrzewska
1 and
Agnieszka Saeid
2
1
Department of Agroecosystems and Horticulture, Faculty of Agriculture and Forestry, University of Warmia and Mazury in Olsztyn, Plac Łódzki 3, 10-718 Olsztyn, Poland
2
Department of Engineering and Technology of Chemical Processes, Faculty of Chemistry, Wrocław University of Science and Technology, Wyspiańskiego 42, 50-376 Wrocław, Poland
*
Author to whom correspondence should be addressed.
Agronomy 2022, 12(6), 1475; https://doi.org/10.3390/agronomy12061475
Submission received: 23 May 2022 / Revised: 15 June 2022 / Accepted: 17 June 2022 / Published: 19 June 2022
(This article belongs to the Special Issue New Advances on Nutrient Recovery from Municipal, Agro-Industrial and Livestock Wastes for Sustainable Farming 2.0)
Versions Notes

Abstract

:
Sewage sludge management for fertilizer purposes can be a step in the circular phosphorus (P) economy. Using microbial solubilization in manufacturing fertilizers from recycled materials is an innovative approach with the potential to increase P compounds’ bioavailability, and fertilizers from sewage sludge ash and P-solubilizing bacteria are promising products of this technology. In addition to P and a range of macronutrients, these fertilizers contain small amounts of micronutrients and potentially toxic elements. This paper discusses the effects of fertilizer on iron (Fe) and aluminum (Al) content in soil, test plants (spring or winter wheat; grain and straw), weeds and post-harvest residues, based on field experiments. Treatments with conventional P fertilizers (superphosphate, phosphorite) and without P fertilization provided references. The tested biofertilizers containing the Bacillus megaterium or Acidithiobacillus ferrooxidans strain had no effect on total Fe and Al content in the soil or on the concentration of these elements in plant biomass when applied at P doses up to 35.2 kg ha–1. Fe and Al levels in grain did not suggest a potential risk to consumers.

1. Introduction

Sewage sludge is a problematic but so far unavoidable by-product of human civilization, generated during wastewater treatment. Information on the global production of sewage sludge is incomplete [1,2]. However, it is estimated at 45 million tons of dry matter per year, and Europe, East Asia, and North America are the main producers of sewage sludge globally [3]. It seems self-evident that the quantity of sludge produced will increase with the growing population and ongoing urbanization [4]. Following this, the need for the appropriate environmentally friendly management of this waste biomass will become more and more pressing. Different methods can be used to dispose of sewage sludge [5], and the choice of method mainly depends on the properties of the sludge [6], including organic and inorganic pollutant concentrations [7].
Increasing environmental awareness has resulted in legal limitations on sewage sludge disposal practices, especially in Europe. In 1986, substantial limitations for the application of sewage sludge in agriculture (as fertilizer/soil improver) were implemented [8]. In 1998, waste disposal in the sea/ocean was prohibited [9]. In 1999, limits were introduced for biodegradable wastes going into landfills [10].
In view of these legal aspects, sludge incineration is an increasingly widely accepted waste disposal option [11]. This method effectively reduces the volume of sewage sludge and eliminates pathogens and organic pollutants while producing heat and/or electricity [5]. Around 20% of sewage sludge produced in the US is incinerated, while in European Union member countries incineration levels are nearly 25% [11]. The rising amount of sludge being incinerated [2] necessitates the search for means to beneficially manage the incineration residue, i.e., sewage sludge ash (SSA).
SSA has been explored in recent years as a potential renewable raw material for phosphorus fertilizers and thus as a pathway to the re-inclusion of P in the food system [11,12,13,14,15].
Phosphorus is a crucial element for life (and food production). Still, the natural P cycle has been disrupted so much that humanity faces two linked problems: the dwindling supply of phosphate rock as a resource, and the overabundance of phosphate in water systems, leading to eutrophication [16]. Moreover, with a growing population, the United Nations’ Sustainable Development Goal number two (zero hunger) will be difficult to achieve if the waste of phosphorus resources continues and the P cycle is not closed through its recovery and recycling [17]. These rationales call for increased efforts toward creating a circular economy for P [17], especially in Europe, for which phosphorus and phosphate rocks are among the most important critical raw materials [18]. Most European countries, including Poland, have to import phosphate rocks for mineral phosphate fertilizer production. Moreover, phosphate rock and the resulting mineral fertilizers contain relevant amounts of heavy metals (e.g., Cd and U) that transfer to the soil and could be a potential risk [19].
Although the idea of P recovery is fully theoretically justified, the practice of its implementation, however, faces many obstacles. Most importantly, nutrient prices in waste-based products are generally higher than in mineral fertilizers, and waste materials require additional post-treatment to increase nutrient concentration and availability [20]. Over the past years, numerous approaches to P recovery from SSA have been developed, such as thermo-chemical, acidic wet-chemical leaching, thermo-electric, and acidic wet-chemical extraction [14]. They are expected to enable the use of SSA for fertilizer production, mainly to enhance P bioavailability and reduce inorganic contaminant amounts [15].
An alternative for treating SSA with acids obtained from the chemical industry is using acids produced by microorganisms occurring in natural environments, e.g., soil [21], making P accessible for plants to absorb. Lowering environment pH by microbial production of organic acids (including acetic, citric, formic, fumaric, gluconic, lactic, malic, propionic, succinic, tartaric, valeric, and others) or release of protons is considered the principal mechanism for microbial solubilization of unavailable inorganic P compounds. Other mechanisms of mineral phosphate solubilization by microorganisms are the production of inorganic acids (such as sulfuric, nitric, and carbonic) and chelating substances [22]. A large number of autotrophic and heterotrophic soil microorganisms, aerobic and anaerobic, are able to solubilize various forms of insoluble phosphate compounds [23]. They can belong to diverse phyla, the most common of which are Proteobacteria, Firmicutes, Ascomycota, Euryarchaeota, Actinobacteria, Basidiomycota, Bacteroidetes, and Mucoromycota [24].
The mechanisms of microbial solubilization and mineralization of phosphorus compounds, the importance of these processes in agriculture, and the many strains of microorganisms capable of performing them have been described extensively in the existing literature [22,25,26]. Using microbial solubilization in the valorizing of secondary raw materials (including SSA) has also been discussed [21,27]. Innovative technology has been developed to produce biofertilizers following this concept and the favorable results of laboratory-scale studies. The major P source was SSA, and the biological agent activating this raw material was P-solubilizing bacteria [28]. The obtained bioproducts were evaluated under field conditions, and many of the findings have already been published [29,30]. Considering the chemical composition of SSA, in addition to P and a range of macronutrients, the biofertilizers contain small amounts of micronutrients and potentially toxic elements (PTEs). Therefore, introducing them into the soil–plant system can bring additional benefits (essential micronutrients) or contamination risks (toxic elements). The effect of SSA-based biofertilizers on the content of several PTEs (Cd, Pb, As, Cr, Ni, Cu, and Zn) in this system has been previously reported [31,32]. This paper addresses the issues of iron (Fe) and aluminum (Al). Fe and Al are usually abundant metal elements in SSA, which is associated with Fe-based or Al-based salts for the precipitation of P from wastewater during the wastewater treatment process [33].
Iron (Fe) is an essential element for almost all living organisms, as it participates in a wide variety of metabolic processes, including oxygen transport, deoxyribonucleic acid (DNA) synthesis, and electron transport [34]. Fe deficiency remains a major threat to peoples’ health around the world [35]. Thus, agronomic food bio-fortification (through crop fertilization) can be the key approach for mitigation of this micronutrient shortage [36]. However, excess accumulation of Fe can easily be toxic for plants [37] and animals [38]. Aluminum (Al) is not considered an essential element, and thus far no experimental evidence has been put forward for a biological role. In plants and other organisms, Al can have a beneficial or toxic effect, depending on factors such as metal concentration, the chemical form of Al, growth conditions, and plant species [39].
The aim of this paper is to assess the effect of biofertilizers from SSA and Bacillus megaterium (Firmicutes, Gram-positive) or Acidithiobacillus ferrooxidans (Proteobacteria, Gram-negative) bacteria on the content of Fe and Al in the soil, test plants (wheat grain and straw), weeds, and post-harvest residue biomass. It was hypothesized that the amounts of Fe and Al contributed by biofertilizers would not cause a threat to the soil–plant system in the agroecosystem.

2. Materials and Methods

In the years 2014–2016, five phosphorus biofertilizers produced from SSA were tested in field experiments conducted in Bałcyny (Poland, 53.60° N, 19.85° E). In some of them, the additional raw material was animal (poultry) bones or dried animal blood. Phosphorus-solubilizing bacteria from Bacillus megaterium (PCM 1855) or Acidithiobacillus ferrooxidans (F7-01) strains were used as biological activators of the phosphorus feedstock. General information about the studied biofertilizers is shown in Table 1, and their detailed chemical composition is provided in Table S1. The biofertilizers were produced by the New Chemical Syntheses Institute in Puławy (Poland) based on the formula developed by the Department of Advanced Material Technologies of the Wrocław University of Science and Technology (Poland). The production process is described elsewhere [40,41].
In the experiments, common wheat (Triticum aestivum ssp. vulgare Mac Key), winter or spring, was used as a test plant. The referential P carriers for the tested biofertilizers were superphosphate Fosdar 40 (SP: 17.6% mass P; Grupa Azoty FOSFORY Sp. z o.o., Gdańsk, Poland), Syrian phosphorite (PR: 12.2–12.9% mass P, 0.79–1.61 g kg–1 Fe, 0.80–1.69 g kg–1 Al; Luvena, Luboń, Poland), an ash–water solution (A + H2O: 0.176% mass P, 1.68 g kg–1 Fe, 1.77 g kg–1 Al), and granular fertilizers from SSA + bones and SSA + blood without bacteria (ABg: 6.10% mass P, 15.4 g kg–1 Fe, 12.8 g kg–1 Al; AHg: 8.68% mass P, 26.9 g kg–1 Fe, 23.7 g kg–1 Al; New Chemical Syntheses Institute in Puławy, Poland). In each experiment, the reference treatment without phosphorus fertilization (No P) was also included. The experimental details are summarized in Table 2, while basic agricultural data for the experiments are given in Table S2.
Wheat was grown on Luvisols [43] formed from sandy clay loam or sandy loam. The soil pHKCl of the arable layer (0–30 cm) was 5.23–6.28, and the total C, N, P, K, Mg, and P contents were 7.15–8.90 g kg–1, 1.09–1.42 g kg–1, 0.43–0.61 g kg–1, 2.90–3.30 g kg–1, 2.01–2.25 g kg–1, and 0.433–0.610 g kg–1, respectively (Table S3). Precipitation and thermal conditions in the growing seasons differed from those typical of the region, being too dry for wheat in experiments I–III, but too wet for this species in experiments IV and V (Table S4).
Soil samples for chemical analyses were taken from the 0–30 cm soil layer twice, i.e., before the start of the experiment and after wheat harvest. The samples of wheat straw (i.e., wheat stems with leaves) and weeds were collected shortly before wheat harvest, while wheat grain and the post-harvest residues (wheat roots, bottom stem segments, weed remnants) were sampled after harvest.
Soil total C and N contents were determined using a Vario Macro Cube Elementar (C, H, N) analyzer (Elementar Analysensysteme, Langenselbold, Germany) and D-phenylalanine (C = 65.44%; N = 8.48%) as a standard solution. The contents of total P, K, Mg, Fe, and Al in the soil and Fe and Al contents in plant material were determined using an inductively coupled plasma-optical emission spectrometer (ICP–OES with a pneumatic nebulizer with an axial view—iCAP Duo Thermo Scientific, Waltham, MA, USA). The levels of detection (LOD) for P, K, Mg, Fe, and Al for the soil material were 3.59, 2.55, 1.17, 0.72, and 2.34 mg kg–1, respectively, and for the plant material, the detection levels for Fe and Al were: 0.040 and 0.015 mg kg–1, respectively. More detailed descriptions of soil and plant sampling, preparation, and chemical analyses are provided in the Supporting Information.
The raw data were submitted to an analysis of variance (ANOVA) or the alternative Kruskal–Wallis test (if ANOVA assumptions were not met). The normality of variable distribution was checked using the Shapiro–Wilk W-test, and the homogeneity of variance was checked using Levene’s test. Finally, the differences between objects were assessed using Duncan’s or multiple comparison test. The calculations were performed using Statistica 13.3 software [44].

3. Results and Discussion

3.1. Iron (Fe)

The level of total Fe content in the soil in the conducted experiments (Table 3) was within the region-specific range (4.0–25.8 g kg–1) and closer to the national average value (9.0 g kg–1) than the median (6.6 g kg–1) [45]. It also corresponded with the average natural Fe content in the parent rocks of soils in Poland (geochemical background—12.9 g kg–1) [46]. The parent material primarily determines the total amount of iron in the soil [47]; however, Fe can also enter the soil from anthropogenic sources, including fertilizers or soil improvers derived from sewage sludge [48].
In the present study, in none of the experiments conducted did P fertilization in the form of conventional and SSA-based fertilizers, at different P rates, differentiate the total Fe content in the soil. Such an effect is not surprising. Previous reports by other authors show that the application of fertilizers or soil amendments containing Fe even for a long period does not bring a significant change in the total Fe content in the soil but rather affects the amount of its mobile/available forms [48,49,50]. Assuming that the weight of dry soil from a 0–30 cm deep layer and an area of 1 ha equals 4500 t, the amount of Fe added with conventional and SSA-based fertilizers ranged from 0.025 mg kg–1 of soil (applied with PR at the P dose of 17.6 kg ha–1) to 7.46 mg kg–1 of soil (applied with AsBm at the P dose of 35.2 kg ha–1). Some amounts of Fe are also introduced with SP (Fe content not defined in the commercial label). Nevertheless, these amounts were low compared with the high background total soil Fe content and thus negligible for statistical analysis. Furthermore, the level of total soil Fe after crop harvest was strongly influenced by plant uptake (wheat and weeds). Leaching of Fe from the soil could not be excluded either [48,51], but this was not the subject of the present study.
A decrease in the total Fe content in the soil compared to the initial state was observed after wheat harvest in experiments II–IV, i.e., where the soil pH was 5.23–5.51. In experiments I and V, where soil pH exceeded 6.0, no significant change in the total Fe content over time was found. This situation is explained by the dependence of the solubility of Fe compounds on soil pH. It is well known that the concentration of Fe in the soil solution decreases sharply as the soil pH increases [52]. Thus, in acidic soils (experiments II–IV), a higher abundance of mobile Fe (both from soil reserves and from fertilizers) resulted in a depletion of the total pool of this element by plant uptake or leaching deep into the soil profile.
None of the conducted experiments confirmed an increase in Fe content in plant biomass (wheat grains and straw, weeds, post-harvest residues) under P fertilization compared to the control. No differences were found between the effects of conventional and SSA-based fertilizers, regardless of the P dose. Such a result should be explained by the fact that Fe in SSA is present in the form of hematite [53], which is poorly soluble, and the potential of P-solubilizing bacteria contained in biofertilizers in making Fe available to plants (lowering pH by acid production [28], production of Fe chelating siderophores [54]) did not become apparent under the given experimental conditions. For comparison, in the study by Płaza et al. [55], an application of the Bacillus megaterium var. phosphaticum bacteria (dose of biological preparation: 1 L ha–1) increased Fe concentration in spring wheat grain and straw.
The Fe concentration in the studied plant biomass elements was arranged according to the following pattern: wheat grain < wheat straw < weed aboveground biomass < post-harvest residues. The presented results concerning Fe levels in wheat grain and straw were close to those obtained by other authors from Poland [55,56,57,58]. According to Kabata-Pendias and Pendias [59], the concentration of Fe in cereal grains fluctuates but rarely exceeds 100 mg kg−1 DM. In national or international regulations, there are no set limits for Fe content in cereal grains for food and feed purposes [60,61,62,63,64]. Moreover, Fe content in wheat grain is generally considered low, and attempts have been made worldwide to increase it through agronomic and genetic biofortification [65]. In the present study, Fe content in wheat grain obtained in experiments II and III was close to, and sometimes even higher than, the target Fe content in wheat grain assumed in the HarvestPlus program (59 mg kg–1 DM) [66]. However, this was not related to the application of the tested biofertilizers, unlike in the study by Płaza et al. [55], which reported an increase in Fe content in spring wheat grain from 34.2 to 68.6 mg kg–1 after Bacillus megaterium application. Fe content in wheat straw oscillated around the value reported by Kirkby [67] as the average concentration of Fe in plant shoot dry matter sufficient for adequate growth (100 mg kg–1) and fell within the range of contents considered by Schulte [52] to be sufficient for wheat growth (20–250 mg kg–1; top leaves, boot stage).
The Fe content of aboveground weed biomass in experiments II–V seems to be high compared to the values presented by Liwski [68] and Głowacka [69]. It corresponds, however, with the ranges of Fe content reported by Rogóż and Niemiec [70] for different weed species growing on soils of similar pH and total Fe content to the present study. The Fe content of the biomass of post-harvest residue in all experiments was very high compared to that of wheat grain and straw. This was primarily due to the Fe levels in plant roots, which can contain up to several times more Fe than their aboveground parts [71,72]. There are no precisely defined critical levels of iron deficiency or excess/toxicity in plants. According to Kabata-Pendias [73], injured leaves indicated an accumulation of Fe above 1000 mg kg–1, while no information on toxic Fe levels in plant roots was found. With contemporary knowledge, plant response to Fe deficiency/toxicity is highly dependent on plant species, soil, and nutritional and climatic factors [73,74], and plants have developed effective mechanisms to maintain Fe homeostasis [75]. After absorption by roots, Fe first accumulates at the basal part of the shoot (discrimination center), and then to translocated shoots and to parts with a high Fe demand. Fe is readily oxidized and precipitated in the apoplast of both roots and shoots. The results of the present study suggest that much of the Fe uptake was retained in the roots.
In experiment II, plant protection effects on Fe content of weed and post-harvest residue biomass were found. In the case of weeds, the differences (PP− vs. PP+) are probably due to a change in the species structure of the weed community under the influence of herbicides, as different weed species can accumulate different amounts of Fe [69,70]. In turn, the differences between Fe contents in post-harvest residues under PP+ versus PP– conditions were mainly due to the ratio of roots to aboveground plant parts in the residue biomass. Under PP+ conditions, roots (mainly wheat) had higher biomass and, at the same time, a higher contribution to the total biomass of the residues, and these can store larger amounts of Fe [70,72].

3.2. Aluminum (Al)

The contents of total Al in soils in the present study (Table 4) were quite high considering the ranges established for Poland (range 1.2–18.1 g kg–1; average 5.7 g kg–1; median 4.5 g kg–1) and the region (2.9–11.2 g kg–1) within the framework of national monitoring [45]. These values seemed more optimistic compared to the range commonly cited in the literature, i.e., 10–250 g kg–1 [76,77]. Total Al content in soils depends on both natural (parent rock, soil type) and anthropogenic sources (including P fertilizers); however, for agriculture, the most important are active Al forms [39,76,77]. National and EU regulations do not set limits for Al content in soils or fertilizers [78,79,80]. However, the use of sewage sludge, which typically contains Al compounds, is limited to soils whose pH is above 5.6 [81]. Some authors have called for bioavailable Al to be added to lists of standardized elements and for monitoring bioavailable Al content [82].
As in the case of Fe, P fertilization variants did not differentiate the content of total Al in the soil in the presented experiments, and the amounts of Al brought with P fertilizers (0.025–7.88 mg kg–1 of soil, applied with PR at P dose of 17.6 kg ha–1 and AsBm at the P dose of 35.2 kg ha–1, respectively; assumptions as specified in Section 3.1.) should be considered small against the initial Al content in the soil. However, it is thought that high concentrations of Al compounds may pose a greater threat to the environment than high concentrations of Fe compounds [83].
Similar to Fe, in the experiments established on acidic soils (experiments II–IV), a decrease in total Al content after harvesting the test plant was recorded in relation to the initial level, and this decrease was irrespective of P fertilization. It has long been known that the concentration of soluble Al increases rapidly in acidic soils (pH < 5.5) and that this soluble Al is potentially toxic for plant growth [39]. In the present study, the content of a mobile and bioavailable Al fractions in soil and fertilizers was not investigated. The amount of Al migrating deep into the soil profile [84] was also not studied.
Of the active forms of Al, some portion was taken up by field plants (wheat and weeds) and accumulated in their biomass, with the highest concentration of Al in post-harvest residues, followed by aboveground organs of weeds, less in wheat straw, and by far the least in wheat grain (Table 4). The Al content of these plant biomass components was not differentiated by P fertilization variants/treatments in any of the experiments conducted. In contrast, Kępka et al. [85] reported that the application of municipal sewage sludge to soil had a significant effect on increasing Al content in grain and straw of spring barley. In the present study, however, the main raw material of the biofertilizers tested was SSA, in which Al occurs typically in the form of anorthite and berlinite [86] and thus is hardly available to plants. Therefore, it can be inferred that the form and amount of Al entering the soil with the applied fertilizers did not contribute to the increase of bioavailable Al in the soil. Moreover, the activity of the P-solubilizing bacteria contained in the biofertilizers did not lower the soil pH, e.g., [87], which could promote the release of active Al into the soil solution and its uptake by plants.
In relation to the range given by Kabata-Pendias and Pendias [59] for cereal grains, as well as the results of other authors [85,88,89,90], the Al content in wheat grains in the present study should be assessed as particularly low. In Experiments II and III it was even below the level of detection. The values obtained in the present study correspond rather with those reported by Kolbaum et al. [91]. Although the beneficial effects of Al on plants are mentioned in the literature [39], even its indispensability [92], neither the deficiency level nor the range of its optimal content in plants has been established [59,85]. The issue of Al toxicity to plants and plant tolerance to Al has been addressed more frequently [39,93]. However, unlike many other PTEs (e.g., Cd, Pb), excessive or toxic Al content in plant biomass is not rigorously defined, since the extent of tolerance to excess Al and the ability to uptake and translocate it vary within plant species and even within cultivars of the same species [73]. In addition, despite its proven toxicity to animals and humans [94], current national and international legislation does not specify maximum levels of Al in cereals for food and feed purposes [60,61,62,63,64]. Earlier studies suggested 200 mg kg–1 as the maximum allowable Al content for cereals [95]. Today, some authors also advise food safety authorities to set a maximum limit for the content of this element in cereals and cereal products [94].
The level of Al in aboveground weed biomass is not surprising when considering the range of values reported by Kabata-Pendias (X0-X00 mg/kg) [73], as well as the fact that some species of natural plants are known to accumulate more than 1000 mg kg−1 dry mass of Al in their stems and leaves [96].
The high Al content in the biomass of post-harvest residues is a consequence of the Al concentration in plant roots. The root is seen to be the main region of Al accumulation in the plant, and the content of this metal in the root can be from several dozen up to 100 times higher than in shoots [77,90]. Root retention of Al, preventing its transport to the shoot, was proposed as one mechanism of plant tolerance to Al [97].
As in the case of Fe, in experiment II, higher Al content in weed biomass was found under PP+ conditions than under PP– conditions, which was also likely due to modification of the weed community structure under the influence of the applied herbicide. Surprisingly, there was no similar differentiation in Al content in post-harvest residues under the influence of the plant protection factor.

4. Conclusions

The SSA-based biofertilizers containing P-solubilizing bacteria (B. megaterium or A. ferrooxidans) did not affect the total Fe and Al content in the soil or the concentration of these elements in plant biomass (wheat grain and straw, weeds, post-harvest residues) when applied at P doses up to 35.2 kg ha–1. The Fe and Al concentrations in the studied plant biomass components were arranged according to the following pattern: wheat grain < wheat straw < weed aboveground biomass < post-harvest residues. The tested preparations failed as a strategy to biofortify wheat grain in Fe, but Fe and Al levels in grain did not suggest a potential risk to consumers.
The results presented here, and the biofertilizers’ yield-forming performance and other environmental effects, allow them to be seen as a promising approach to a sustainable circular P economy. However, further research on elemental mobility due to biological activators is advisable. Furthermore, long-term studies with repeated applications of SSA-based biofertilizers are still necessary.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/agronomy12061475/s1, Table S1: Elemental composition of SSA-based P-fertilizers; Table S2: Basic agricultural data for the experiments; Table S3: Soil characteristics before the start of the experiments; Table S4: Precipitation and air temperature during the study period according to the Meteorological Station in Bałcyny, Poland; Soil and plant sampling and preparation; Chemical analyses.

Author Contributions

Conceptualization, M.J., M.K.K. and A.S.; methodology, M.J., M.K.K. and A.S.; validation, M.J., M.K.K. and A.S.; formal analysis, M.J.; investigation, M.J., M.K.K. and A.S.; resources, M.J., M.K.K. and A.S.; writing—original draft preparation, M.J.; writing—review and editing, M.K.K. and A.S.; visualization, M.J.; funding acquisition, A.S., M.J. and M.K.K. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by National Center for Research and Development, Poland, grant number PBS 2/A1/11/2013. The APC was funded by the University of Warmia and Mazury in Olsztyn, Faculty of Agriculture and Forestry, Department of Agroecosystems and Horticulture (grant No. 30.610.015-110).

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Not applicable.

Acknowledgments

The Institute of New Chemical Synthesis in Puławy is highly acknowledged for providing fertilizer batches for field experiments.

Conflicts of Interest

The authors declare no conflict of interest.

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Table
Table 1. Biofertilizers tested in the experiments.
Table 1. Biofertilizers tested in the experiments.
SymbolRaw MaterialBacteriaFormP, % MassFe, g kg–1Al, g kg–1
AsBmsewage sludge ash (SSA) 1Bacillus megaterium 3suspension0.1761.681.78
AgAfSSAAcidithiobacillus ferrooxidans 4granules9.2433.024.4
ABgAfSSA + bones 2Acidithiobacillus ferrooxidansgranules7.5015.113.9
ABgBmSSA + bonesBacillus megateriumgranules5.8714.411.3
AHgBmSSA + blood 2Bacillus megateriumgranules9.5529.025.5
1 Obtained from Municipal Wastewater Treatment Plant ‘Łyna’ in Olsztyn, Poland; 2 obtained from the meat industry; 3 obtained from the Polish Collection of Microorganisms at the Institute of Immunology and Experimental Therapy of the Polish Academy of Sciences in Wrocław, Poland; 4 obtained from Professor Zygmunt Sadowski from Wroclaw University of Science and Technology; the strain is autochthonous, isolated from the tailings impoundment “Iron Bridge”, Poland [42].
Table
Table 2. Field experiments conducted—trial details.
Table 2. Field experiments conducted—trial details.
ItemExperiment
IIIIIIIVV
Year20142015201520162016
Test Plantspring wheatspring wheatwinter wheatwinter wheatspring wheat
Biofertilizers testedAsBmAsBmAgAfABgBmAHgBm
ABgAf
Reference treatmentsno P no Pno Pno Pno P
SPSPSPSPSP
PRPR ABgAHg
A + H2O
P doses, kg ha–12117.617.6 17.617.6
26.426.426.426.4
35.235.235.235.2
Plant Protection (PP)PP−PP−PP+PP+PP+
PP+
Number of treatment combinations520101010
Experimental designrandomized blockparallel striprandomized block randomized block randomized block
Number of replications 44444
Number of plots2080404040
PP−: no plant protection treatments; PP+: full plant protection (see Table S2).
Table
Table 3. Total Fe content in soil and plant biomass (average ± standard error).
Table 3. Total Fe content in soil and plant biomass (average ± standard error).
ExperimentP-FertilizerP-Dose, kg ha–1Plant ProtectionSoil, g kg–1 DMPlant Biomass, mg kg–1 DM
StartEndWheat GrainWheat StrawWeedsPost-Harvest Residues
INo P0PP−11.2 ± 0.810.8 ± 0.539.4 ± 1.454 ± 5181 ± 242441 ± 155
SP21 11.5 ± 0.611.5 ± 0.839.4 ± 1.454 ± 2157 ± 192519 ± 254
PR21 10.9 ± 0.311.1 ± 0.639.4 ± 0.861 ± 6209 ± 292370 ± 176
A + H2O21 11.4 ± 0.811.3 ± 0.539.2 ± 1.153 ± 6192 ± 152699 ± 217
AsBm21 11.3 ± 1.011.3 ± 0.741.1 ± 1.851 ± 3198 ± 212603 ± 162
IINo P0PP−11.1 ± 0.49.2 ± 0.9↓ 162.1 ± 8.4102 ± 8442 ± 1252080 ± 394
SP17.6 11.0 ± 0.39.1 ± 0.9↓51.1 ± 2.198 ± 14418 ± 691798 ± 286
26.4 10.7 ± 0.69.2 ± 0.9↓55.5 ± 7.9100 ± 3425 ± 1331761 ± 204
35.2 11.2 ± 0.39.1 ± 0.8↓54.0 ± 6.894 ± 11514 ± 1491970 ± 222
PR17.6 10.6 ± 0.49.2 ± 0.9↓53.6 ± 7.3118 ± 14640 ± 1881846 ± 176
26.4 11.0 ± 0.59.2 ± 0.5↓62.7± 8.3103 ± 20495 ± 1141926 ± 229
35.2 10.5 ± 0.59.1 ± 0.8↓48.0± 5.8100 ± 14492 ± 861638 ± 347
AsBm17.6 11.3 ± 0.49.2 ± 0.9↓57.5 ± 11.990 ± 5416 ± 961740 ± 269
26.4 10.7 ± 0.59.1 ± 0.9↓57.6 ± 7.4101 ± 19669 ± 1922143 ± 296
35.2 11.1 ± 0.49.3 ± 1.1↓53.9 ± 7.399 ± 15724 ± 2741691 ± 234
average 10.9 ± 0.19.2 ± 0.2↓55.6 ± 2.3101 ± 4524 ± 46 b 21859 ± 80 b
No P0PP+11.5 ± 0.79.3 ± 0.7↓57.9 ± 4.292 ± 12638 ± 292284 ± 520
SP17.6 11.1 ± 0.69.3 ± 0.6↓51.3 ± 7.792 ± 6603 ± 1592253 ± 159
26.4 10.9 ± 0.39.7 ± 0.5↓60.8 ± 11.499 ± 13666 ± 992154 ± 262
35.2 11.5 ± 0.59.5 ± 0.5↓55.5 ± 9.4106 ± 15633 ± 1622177 ± 88
PR17.6 11.0 ± 0.59.0 ± 0.4↓51.6 ± 6.186 ± 8662 ± 32655 ± 494
26.4 10.7 ± 0.29.2 ± 0.5↓56.2 ± 1.293 ± 9608 ± 1242502 ± 368
35.2 11.0 ± 0.39.0 ± 0.6↓63.7 ± 9.684 ± 5597 ± 1712291 ± 330
AsBm17.6 10.7 ± 0.38.6 ± 0.2↓59.1 ± 2.7105 ± 10553 ± 1312422 ± 221
26.4 10.7 ± 0.29.1 ± 0.3↓59.6 ± 0.484 ± 10917 ± 1642201 ± 186
35.2 10.2 ± 0.19.3 ± 0.3↓57.9 ± 7.0103 ± 11797 ± 342408 ± 315
average 10.9 ± 0.19.2 ± 0.1↓57.0 ± 2.195 ± 3667 ± 38 a2335 ± 93 a
IIINo P0PP+11.9 ± 0.510.8 ± 0.6↓69.0 ± 7.880 ± 14572 ± 1023398 ± 489
SP17.6 11.6 ± 0.610.1 ± 0.5↓53.3 ± 3.369 ± 13527 ± 973171 ± 120
26.4 11.8 ± 0.810.4 ± 0.6↓52.4 ± 3.879 ± 12493 ± 913546 ± 507
35.2 11.5 ± 0.510.6 ± 0.5↓61.8 ± 9.372 ± 9503 ± 1123493 ± 351
AgAf17.6 11.3 ± 0.910.2 ± 0.4↓64.8 ± 5.579 ± 9528 ± 1033238 ± 343
26.4 11.3 ± 0.510.2 ± 0.4↓53.0 ± 3.879 ± 5632 ± 1163628 ± 215
35.2 11.5 ± 0.810.4 ± 0.5↓69.1 ± 9.971 ± 7577 ± 523187 ± 372
ABgAf17.6 11.7 ± 0.510.4 ± 0.5↓59.4 ± 8.985 ± 8596 ± 262975 ± 190
26.4 11.6 ± 0.710.5 ± 0.5↓55.6 ± 4.689 ± 13619 ± 933633 ± 475
35.2 11.3 ± 0.410.6 ± 0.5↓57.6 ± 5.266 ± 9673 ± 743230 ± 440
IVNo P0PP+12.1 ± 0.610.1 ± 0.4↓31.4 ± 1.1105 ± 9386 ± 661737 ± 285
SP17.6 11.4 ± 0.310.7 ± 0.7↓31.9 ± 0.9104 ± 18417 ± 471948 ± 274
26.4 12.1 ± 0.610.4 ± 0.3↓31.3 ± 1.1118 ± 19392 ± 822273 ± 389
35.2 11.6 ± 0.410.2 ± 0.4↓29.2 ± 0.3117 ± 23452 ± 1821757 ± 243
ABg17.6 11.7 ± 0.810.8 ± 0.5↓35.3 ± 1.0126 ± 12457 ± 762138 ± 204
26.4 11.8 ± 0.510.6 ± 0.3↓30.9 ± 0.4118 ± 12565 ± 732172 ± 114
35.2 12.0 ± 0.810.7 ± 0.6↓32.1 ± 0.9135 ± 26410 ± 141908 ± 185
ABgBm17.6 11.6 ± 0.510.7 ± 0.6↓34.5 ± 1.9114 ± 24395 ± 902118 ± 153
26.4 11.5 ± 0.411.1 ± 0.7↓33.0 ± 2.3115 ± 26545 ± 322055 ± 285
35.2 11.8 ± 0.810.9 ± 0.5↓37.4 ± 6.0100 ± 19482 ± 1372151 ± 355
VNo P0PP+11.0 ± 0.910.8 ± 0.741.4 ± 1.6101 ± 19552 ± 852071 ± 62
SP17.6 10.4 ± 0.510.5 ± 0.337.7 ± 1.197 ± 28721 ± 1072646 ± 190
26.4 10.9 ± 0.611.0 ± 0.538.2 ± 2.394 ± 21581 ± 261969 ± 303
35.2 11.2 ± 0.710.8 ± 0.638.4 ± 1.1136 ± 25781 ± 1762278 ± 454
AHg17.6 10.6 ± 0.811.0 ± 0.446.6 ± 4.4122 ± 30613 ± 702121 ± 489
26.4 10.6 ± 0.510.6 ± 0.440.9 ± 2.1129 ± 33493 ± 942595 ± 423
35.2 11.1 ± 0.610.8 ± 0.445.6 ± 7.7112 ± 24812 ± 3422101 ± 333
AHgBm17.6 10.3 ± 0.510.6 ± 0.537.6 ± 2.0136 ± 25630 ± 1022498 ± 435
26.4 10.6 ± 0.810.6 ± 0.543.4 ± 2.2129 ± 37715 ± 1721747 ± 182
35.2 10.4 ± 0.610.7 ± 0.538.2 ± 1.3115 ± 19538 ± 1221763 ± 141
1 arrows (↓) indicate significant decrease in relation to the starting state; 2 different letters indicate significant differences at p < 0.05; no letters—no significant differences for plant protection treatments or for P-fertilization treatments.
Table
Table 4. Total Al content in soil and plant biomass (average ± standard error).
Table 4. Total Al content in soil and plant biomass (average ± standard error).
ExperimentP-FertilizerP-dose, kg ha–1Plant ProtectionSoil, g kg–1 DMPlant Biomass, mg kg–1 DM
StartEndWheat GrainWheat StrawWeedsPost-Harvest Residues
INo P0PP–11.6 ± 0.910.8 ± 0.48.98 ± 0.8163.1 ± 4.4226 ± 473159 ± 309
SP21 11.2 ± 0.511.8 ± 1.08.18 ± 0.6859.0 ± 2.7160 ± 203267 ± 449
PR21 11.1 ± 0.211.3 ± 0.510.26 ± 1.5968.8 ± 9.3257 ± 343020 ± 298
A + H2O21 11.4 ± 0.811.3 ± 0.48.83 ± 0.2561.9 ± 9.8411 ± 1133444 ± 255
AsBm21 11.9 ± 1.111.6 ± 0.88.77 ± 0.8255.3 ± 1.1218 ± 183255 ± 257
IINo P0PP–12.1 ± 0.510.0 ± 1.3↓ 1<LOD121 ± 11464 ± 1362177 ± 443
SP17.6 11.3 ± 0.79.9 ± 1.2↓<LOD132 ± 26434 ± 661578 ± 303
26.4 11.2 ± 0.69.5 ± 0.8↓<LOD93 ± 9416 ± 1481615 ± 162
35.2 12.0 ± 0.49.8 ± 1.1↓<LOD91 ± 10535 ± 1671978 ± 251
PR17.6 11.7 ± 0.69.5 ± 0.8↓<LOD150 ± 41614 ± 2021816 ± 178
26.4 11.6 ± 0.810.0 ± 1.0↓<LOD178 ± 13530 ± 1311895 ± 160
35.2 11.5 ± 0.79.5 ± 0.8↓<LOD103 ± 17499 ± 861546 ± 265
AsBm17.6 12.5 ± 0.58.9 ± 0.2↓<LOD100 ± 13425 ± 931933 ± 378
26.4 11.1 ± 0.89.7 ± 1.0↓<LOD106 ± 15705 ± 2092628 ± 453
35.2 12.1 ± 0.69.8 ± 1.1↓<LOD110 ± 14559 ± 1851552 ± 181
average 11.7 ± 0.29.7 ± 0.3↓<LOD118 ± 7518 ± 44 b 21872 ± 97
No P0PP+12.4 ± 0.710.3 ± 1.0↓<LOD95 ± 11744 ± 291926 ± 626
SP17.6 11.9 ± 0.610.4 ± 0.9↓<LOD119 ± 35653 ± 1611786 ± 172
26.4 11.5 ± 0.311.1 ± 0.7↓<LOD99 ± 23670 ± 1051397 ± 82
35.2 12.2 ± 0.510.8 ± 0.7↓<LOD119 ± 19708 ± 2001719 ± 230
PR17.6 11.9 ± 0.410.0 ± 0.6↓<LOD131 ± 52756 ± 172117 ± 409
26.4 11.4 ± 0.310.3 ± 0.8↓<LOD99 ± 3667 ± 1382592 ± 234
35.2 11.9 ± 0.39.9 ± 0.9↓<LOD91 ± 10655 ± 1991818 ± 353
AsBm17.6 11.5 ± 0.29.2 ± 0.4↓<LOD99 ± 11601 ± 1332446 ± 666
26.4 11.4 ± 0.29.8 ± 0.7↓<LOD90 ± 12985 ± 1601691 ± 221
35.2 11.0 ± 0.110.2 ± 0.6↓<LOD107 ± 11907 ± 642077 ± 267
average 11.7 ± 0.110.2 ± 0.2↓<LOD105 ± 7735 ± 42 a1957 ± 117
IIINo P0PP+13.5 ± 0.712.4 ± 0.6↓<LOD121 ± 20430 ± 973155 ± 411
SP17.6 12.8 ± 0.711.7 ± 1.0↓<LOD99 ± 29423 ± 922950 ± 238
26.4 13.2 ± 0.911.9 ± 1.3↓<LOD102 ± 17376 ± 923143 ± 510
35.2 12.6 ± 0.612.1 ± 0.5↓<LOD97 ± 15495 ± 1603225 ± 302
AgAf17.6 12.7 ± 1.112.2 ± 0.5↓<LOD106 ± 11530 ± 1453080 ± 319
26.4 12.8 ± 0.612.0 ± 0.8↓<LOD125 ± 15537 ± 1133236 ± 196
35.2 12.8 ± 1.012.1 ± 0.6↓<LOD96 ± 14562 ± 1082797 ± 297
ABgAf17.6 13.1 ± 0.712.5 ± 0.5↓<LOD119 ± 10492 ± 253040 ± 153
26.4 13.1 ± 0.812.5 ± 0.8↓<LOD117 ± 22474 ± 723310 ± 417
35.2 12.6 ± 0.712.2 ± 0.5↓<LOD93 ± 9596 ± 593141 ± 404
IVNo P0PP+13.4 ± 1.011.0 ± 0.3↓2.13 ± 1.54137 ± 19457 ± 861256 ± 212
SP17.6 13.2 ± 0.411.8 ± 0.9↓1.85 ± 0.81131 ± 31528 ± 821427 ± 220
26.4 13.6 ± 0.611.9 ± 0.3↓2.11 ± 0.78165 ± 37483 ± 1141362 ± 204
35.2 13.3 ± 0.511.5 ± 0.6↓2.89 ± 1.10149 ± 27405 ± 951414 ± 100
ABg17.6 13.3 ± 0.912.0 ± 0.6↓2.21 ± 0.93156 ± 17489 ± 1461662 ± 116
26.4 13.3 ± 0.711.6 ± 0.4↓1.72 ± 0.84162 ± 29676 ± 651435 ± 124
35.2 13.7 ± 1.011.9 ± 0.7↓4.09 ± 1.65169 ± 30514 ± 261402 ± 131
ABgBm17.6 12.6 ± 1.011.6 ± 0.9↓5.80 ± 1.31142 ± 17417 ± 1051459 ± 108
26.4 12.9 ± 0.312.7 ± 0.7↓1.52 ± 0.17134 ± 26662 ± 421409 ± 236
35.2 13.5 ± 1.212.3 ± 0.8↓2.62 ± 0.42179 ± 30488 ± 1031411 ± 193
VNo P0PP+12.5 ± 1.012.0 ± 0.92.36 ± 1.55139 ± 25785 ± 1462445 ± 43
SP17.6 12.1 ± 0.312.0 ± 0.54.31 ± 1.04159 ± 36964 ± 1623013 ± 200
26.4 12.2 ± 0.912.2 ± 0.73.33 ± 0.74125 ± 31756 ± 182232 ± 362
35.2 12.7 ± 0.712.0 ± 0.42.71 ± 1.42181 ± 41911 ± 1832404 ± 443
AHg17.6 12.9 ± 0.512.2 ± 0.33.18 ± 1.01166 ± 47824 ± 1402337 ± 344
26.4 11.7 ± 0.512.0 ± 0.52.74 ± 0.84184 ± 47707 ± 1453049 ± 450
35.2 12.1 ± 0.812.0 ± 0.51.40 ± 0.82152 ± 40902 ± 2512392 ± 327
AHgBm17.6 12.6 ± 0.011.9 ± 0.61.35 ± 0.77186 ± 36871 ± 1662797 ± 437
26.4 12.2 ± 0.811.5 ± 0.62.23 ± 1.26154 ± 41922 ± 2271956 ± 168
35.2 11.2 ± 1.012.0 ± 0.61.47 ± 0.57190 ± 46681 ± 1412006 ± 150
1 arrows indicate significant decrease in relation to the starting state; 2 different letters indicate significant differences at p < 0.05; no letters—no significant differences for plant protection treatments or for P-fertilization treatments.
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Jastrzębska, M.; Kostrzewska, M.K.; Saeid, A. Sewage Sludge Ash-Based Biofertilizers as a Circular Approach to Phosphorus: The Issue of Fe and Al in Soil and Wheat and Weed Plants. Agronomy 2022, 12, 1475. https://doi.org/10.3390/agronomy12061475

AMA Style

Jastrzębska M, Kostrzewska MK, Saeid A. Sewage Sludge Ash-Based Biofertilizers as a Circular Approach to Phosphorus: The Issue of Fe and Al in Soil and Wheat and Weed Plants. Agronomy. 2022; 12(6):1475. https://doi.org/10.3390/agronomy12061475

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Jastrzębska, Magdalena, Marta K. Kostrzewska, and Agnieszka Saeid. 2022. "Sewage Sludge Ash-Based Biofertilizers as a Circular Approach to Phosphorus: The Issue of Fe and Al in Soil and Wheat and Weed Plants" Agronomy 12, no. 6: 1475. https://doi.org/10.3390/agronomy12061475

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