Next Article in Journal
Multiple Virtual Power Plants Transaction Matching Strategy Based on Alliance Blockchain
Previous Article in Journal
The Impact of Digital Technology Innovation Network Embedding on Firms’ Innovation Performance: The Role of Knowledge Acquisition and Digital Transformation
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Sustainability
Volume 15
Issue 8
10.3390/su15086940
sustainability-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

Aspergillus niger Enhances the Efficiency of Sewage Sludge Biochar as a Sustainable Phosphorus Source

by
Kamila Fernanda Rossati
1,
Cícero Célio de Figueiredo
2 and
Gilberto de Oliveira Mendes
1,*
1
Instituto de Ciências Agrárias, Universidade Federal de Uberlândia, Rodovia LMG-746, km 1, Bloco 1A-MC, Monte Carmelo 38500-000, MG, Brazil
2
Faculdade de Agronomia e Medicina Veterinária, Universidade de Brasília, Campus Darcy Ribeiro, Asa Norte, Brasília 70910-970, DF, Brazil
*
Author to whom correspondence should be addressed.
Sustainability 2023, 15(8), 6940; https://doi.org/10.3390/su15086940
Submission received: 17 January 2023 / Revised: 11 April 2023 / Accepted: 18 April 2023 / Published: 20 April 2023
Browse Figures
Review Reports Versions Notes

Abstract

:
Phosphorus-rich biochar derived from sewage sludge (SS) could be a sustainable alternative P source for agriculture. However, most of biochar P is not readily available to plants. We evaluated the potential of P release from SS biochar into soil solution by Aspergillus niger. Additionally, we assessed the effect of SS biochar on the solubilization of phosphate minerals by the fungus. An incubation study was performed for 7 days in shaken flasks containing culture medium supplemented, or not, with a P-fixing soil. Biochar showed a dual role in phosphate solubilization by A. niger: (i) improved solubilization of AlPO4 and rock phosphate; and (ii) acted as a P source. Aspergillus niger solubilized up to 50% of the P contained in the biochar. A combined application of SS biochar and A. niger increased P availability by 500 times in a solution containing P-fixing soil. These results suggest that P-use efficiency from SS biochar could be improved by A. niger, allowing for the use of lower doses of this soil amendment. These findings contribute to a better understanding of the role of phosphate-solubilizing microorganisms in the interaction between soil and biochar. Furthermore, the results underpin the potential P fertilizer value of the SS biochar. Finally, our results present a win–win environmental benefit as it reduces SS accumulation and improves P-use efficiency.

1. Introduction

The excessive use of chemical fertilizers is one of the biggest environmental problems in the world. When used improperly, high-solubility fertilizers increase greenhouse gas emissions, cause water pollution, and increase production costs. Global fertilizer consumption is forecasted to increase by some 58% from 2005 to 2050 to meet the rising global food demand due to population growth [1]. Phosphorus is the fertilizer which is the second-most applied in the world, with an average annual application rate of 44 Mt in the last decade [2]. While tropical regions harbor most croplands with potential for agricultural intensification, most soils in these regions are highly weathered, presenting low levels of available nutrients, especially phosphorus, and thus, soil fertilization is a mandatory practice to increase crop productivity [3]. However, tropical soils show high P-fixing capacity due to the adsorption of phosphate ions onto aluminum and iron oxides, making P less available to plants [3]. Therefore, agricultural intensification in tropical areas is estimated to require an average surplus of 3.8 Tg P year−1 to “feed” the soil sink [3]. This scenario will put enormous pressure on natural reserves of rock phosphate, the main source of P for fertilizer production. At the same time, rock phosphate reserves are forecasted to last for a few centuries [4]. Thus, strategies to use alternative and renewable P sources, as well as improving their efficiency, are crucial to achieving P sustainability [5,6,7,8].
The accumulation of sludge in sewage treatment plants is another growing environmental problem. Despite being a rich source of P for recycling, the presence of pollutants reduces the use of sewage sludge (SS) in agriculture. Suitable treatment can enable the application of SS as a fertilizer. Phosphorus recovery from wastewater can be carried out by various physicochemical processes, biological treatments, or combinations of both [6,9,10,11,12,13]. After treatment, most of the P is retained in the sludge, usually adding up to ~3% P (dry basis) in SS [6,14]. Thus, the application of SS as an alternative P source in croplands provides the double benefit of recycling P while avoiding environmental damages caused by eutrophication [6,7,11,12]. However, the direct land application of SS has some constraints due to potential contamination by heavy metals (HMs), organic pollutants, and pathogens [6,14,15,16]. Thermal treatment via pyrolysis can overcome these limitations and at the same time recover energy from SS [15,17]. Furthermore, thermal processing of SS by pyrolysis represents an important alternative to allow for the agricultural use of this residue and presents advantages such as a reduction in volume and transport costs in addition to the elimination of undesirable microorganisms [18]. The product of SS pyrolysis is a biochar enriched in P, which is found in several organic and inorganic fractions with different degrees of stability [14,15,19,20]. Although the relative concentration of HMs increases after pyrolysis, their bioavailability in biochar decreases as a consequence of thermal treatment [14,15,18].
Biochar has been used as a soil amendment, producing benefits on chemical, physical, and biological soil attributes [15,21,22]. The environmental benefits of biochar as a soil amendment include carbon sequestration, reduction in greenhouse gas emissions [23], remediation of pollutants [24,25], and increased availability of nutrients to plants [18]. P-rich biochars such as SS biochar can also be an alternative P source for agriculture [14,19]. However, most of the P contained in SS biochar is not readily available to plants due to the formation of sparingly soluble phosphates with Ca, Al, and Fe during wastewater treatment and sludge pyrolysis [6,14,26,27]. Furthermore, the concentration and chemical forms of P in SS biochar are influenced by the pyrolysis temperature [27]. In general, while Fe and Al phosphates decrease, Ca phosphates increase with rising temperatures [28]. This may reduce the bioavailability of P from SS biochar.
Population growth has also led to an increase in waste generation. Therefore, developing sustainable agricultural inputs from urban waste is an increasing demand from society. In this sense, the complete use of P from pyrolyzed SS still lacks detailed studies. The use of phosphate-solubilizing microorganisms is an alternative to enable the complete adoption of SS biochar as a P source for plants. Furthermore, elucidating the effects of combining biochar and microorganisms can create technological routes for the development of novel fertilizers. The fungus Aspergillus niger can solubilize Ca-, Al-, and Fe-phosphates [29,30] and, therefore, could be an alternative to increase the effectiveness of biochar as a P fertilizer. Moreover, it was demonstrated that biochar with a low P content boosted mineral phosphate solubilization by A. niger [31,32]. Thus, we hypothesized that a P-rich biochar could both boost P release from phosphate minerals and act as a P source itself. Therefore, this study is aimed at evaluating the effect of SS biochar on the solubilization of phosphate minerals by A. niger and testing the potential of P release from this biochar into soil solution by the fungus.

2. Materials and Methods

2.1. Microorganism and Cultivation Conditions

The phosphate-solubilizing fungus A. niger strain FS1 was isolated previously from soil under native forest in Viçosa, Minas Gerais state, Brazil (20°46′4.2′′ S 42°52′40.9′′ W) [29]. The fungus was maintained on potato dextrose agar (PDA) at 30 °C.
Solubilization assays were carried out in 250 mL Erlenmeyer flasks filled with 100 mL of the National Botanical Research Institute’s phosphate growth medium (NBRIP medium) without the P source, containing (per litre): 10 g glucose, 5 g MgCl2·6H2O, 0.25 g MgSO4·7H2O, 0.2 g KCl, 0.1 g (NH4)2SO4 [33]. The pH was adjusted to 7.0 with 0.1 M NaOH before adding the biochar, the P source, or soil. The medium was sterilized by autoclaving at 121 °C for 30 min. Flasks were inoculated with ~107 A. niger conidia from a conidial suspension prepared in 0.1% (v/v) Tween 80. Culture flasks were incubated for 7 days in an orbital shaker at 160 rpm and 30 °C.

2.2. Experiment I: Effect of Biochars on the Solubilization of P Sources

Biochars and P sources were weighted individually and added at 3 g L−1 each to Erlenmeyer flasks containing NBRIP medium. The P source was either AlPO4, Ca3(PO4)2, FePO4.2H2O, Araxá rock phosphate (RP) (particle size < 75 µm), or Bayóvar RP (particle size < 75 µm) (Table 1). Biochars were produced by pyrolysis of SS at 300 or 500 °C. Pyrolysis was performed in a muffle furnace (Linn ElektroTherm, Eschenfelden, Germany) at a mean temperature increase rate of 11 °C min−1 and residence time of 30 min. The furnace was equipped with a mechanism to prevent oxygen flow (via forced draft fan, helping gas and oil vapors exit the furnace). Samples of biochar were sieved through a 2 mm sieve before use. The main characteristics of biochars are presented in Table 2 (for detailed characterization of biochars, see Figueiredo et al. [17]). Background information on SS and biochar physicochemical characterization is available in our previous work [15]. In summary, the pH was determined in a CaCl2 0.01 M solution, using a 1:5 (w/v) biochar:solution ratio suspension. Total C, H, and N contents in the SS and biochars were determined using a CHN Elemental analyzer (model PE 2400, series II CHNS/O, PerkinElmer, Norwalk, CT, USA). Nitrate and ammonium were determined by the Kjeldahl method (Bremner and Keeney, 1965). After drying, grounding, and sieving through a 0.50 mm mesh sieve, samples were subjected to acid digestion with concentrated HCl/HNO3 according to USEPA 3050B [34]. Macronutrient, micronutrient, and heavy metal contents were determined after nitric-perchloric acid digestion and quantified according to the following procedures: phosphorus was determined by the molybdovanadate phosphoric acid method, potassium by flame photometry and macronutrients, micronutrients and heavy metals were analyzed by ICP-OES (ICPE-9000, Shimadzu, Kyoto, Japan). The biochar specific surface area (SSA) and pore volumes were determined by N2 adsorption isotherms at −196.2 °C in a surface area analyzer, NOVA 2200. The volatile matter (VM) and ash contents were determined by heating in muffle furnace (Model KK 260 SO 4060, Linn-Elektro Therm, Eschenfelden, Germany). VM was determined as the weight loss after heating at 550 °C in a muffle furnace for 1 h. Ash was also measured as the residual remaining after heating to 600 °C and holding this temperature until the weight of the sample stabilized, while fixed carbon was calculated from the equation: 100–ash (%)–(VM)–moisture content (%).
The experiment was set up in a factorial scheme with combinations of P sources [AlPO4, Ca3(PO4)2, FePO4.2H2O, Araxá RP, Bayóvar RP, no P (control)] and biochar [SB300, SB500, no biochar (control)], adding up to 18 treatments. Experimental controls consisted of treatments with no P source and no biochar added. The experiment was performed in triplicate using a completely randomized design (CRD).
Flasks were sterilized, inoculated, and incubated as described above. At the end of the incubation period, the spent medium was filtered through a quantitative filter paper (pores 25 µm) and the filtrate analyzed for soluble P and pH. Soluble phosphate (expressed as mg P L−1) was determined by the spectrophotometric molybdenum blue method [35].

2.3. Experiment II: P Release from Sewage Sludge Biochar by A. niger into Soil Solution

The experiment was carried out in the NBRIP medium supplemented with soil (10 g L−1) with high P-fixing capacity. The soil was an Oxisol collected in Monte Carmelo, Minas Gerais state, Brazil (18°42′31.5′′ S 47°33′23.3′′ W). The soil was sieved through a 2 mm sieve and presented the following characteristics: pH in water 5.1, P (extracted by Mehlich-1) 4.6 mg dm−3, total P 47 mg dm−3 [36], maximum P adsorption capacity (MPAC) 1667 mg P kg−1 (determined according to Oliveira et al. [37]), texture (51% clay, 36.5% sand, and 12.5% silt).
The SS biochar (pyrolyzed at 500 °C) was added at 3 g L−1 as the only P source or in combination with the triple superphosphate fertilizer (TSP, 19% P, particle size < 75 µm) at a dose corresponding to 25 mg P L−1. The experiment consisted of combinations of three factors (An: Aspergillus niger, B: biochar, and TSP: triple superphosphate) in a 23 factorial: An + B + TSP, An + B, An + TSP, An, B + TSP, B, TSP. The control treatment consisted of absence of all factors. The experiment was carried out under a CRD with four repetitions.
Flasks were sterilized, inoculated, and incubated as described above. At the end of the incubation period, the medium was filtered through a quantitative filter paper (pores 25 µm) and the filtrate analyzed for soluble P [35] and pH.

2.4. Statistical Analyses

For both experiments, data normality was validated by the Kolmogorov–Smirnov test and the homogeneity of variance by Brown–Forsythe test (p < 0.05). Data were subjected to analysis of variance (ANOVA) and the Fisher’s least significant difference (LSD) test was used to compare treatment means (p < 0.05). In experiment II, data were square-root transformed to fit a normal distribution.

3. Results

Treatments containing SS biochars showed a higher (p < 0.05) soluble P concentration at the end of the incubation period for the P sources AlPO4 and Araxá RP, reaching up to a 55 and 234% increase over the controls without biochar, respectively (Figure 1). Aspergillus niger was also able to extract P from the SS biochars, as evidenced in the treatments with no P source. Except for Araxá RP, the SS biochars produced at 300 or 500 °C showed a similar soluble P concentration at the end of the incubation period. For Araxá RP, the SS biochar produced at 300 °C promoted a higher soluble P than the biochar at 500 °C (p < 0.05). Regardless of the P source or biochar, Aspergillus niger acidified the medium to an average pH of 2.1.
Table 3 shows the percentage of the total P solubilized by A. niger in each P source after the incubation period. All P sources were solubilized by A. niger, releasing up to 73, 96, 78, 107, and 58% of the P contained in AlPO4, Ca3(PO4)2, FePO4.2H2O, Araxá RP, and Bayóvar RP, respectively. After discounting the amount of P solubilized from the SS biochars, the sources AlPO4 and Araxá RP showed average percentages of P solubilization of 73 and 83%, respectively, which were higher than the treatment with no biochar. On the other hand, the amount of P solubilized from Ca3(PO4)2 and FePO4.2H2O were not affected by the addition of the biochars.
To further evaluate SS biochar as an alternative P source, an experiment was carried out to simulate P release into the soil solution by A. niger (Experiment II). It was demonstrated that A. niger was efficient in solubilizing P from SS biochar. About 34% of the P contained in the SS biochar was solubilized by A. niger (Figure 2a). Interestingly, the addition of biochar combined with A. niger increased the amount of P from TSP that remained in the solution after contact with the soil particles. When TSP was applied singly, 62% of the added P was fixed by the soil particles. On the other hand, when TSP was combined with A. niger and biochar, apparently 100% of the P remained in the solution, as inferred from the difference between the treatments An + B + TSP and An + B (Figure 2a).
The pH values of the culture medium supplemented with biochar and TSP after the incubation period are shown in Figure 2b. In general, the presence of A. niger reduced the pH values, varying from 1.7 to 2.5 in the inoculated medium and an average pH of 4.7 in the absence of A. niger.

4. Discussion

Biochar derived from SS showed a dual role in phosphate solubilization by A. niger: (i) improved solubilization of AlPO4 and Araxá RP; and (ii) acted as a P source itself. The mechanism of phosphate solubilization by A. niger is the production of organic acids such as citric, oxalic, and gluconic acid [29,30,38]. These acids supply the protons (H+) that react with the sparingly soluble phosphate mineral and release soluble phosphate ions. Moreover, organic acids form stable complexes with the metal cations present in the mineral structure, favoring the forward reaction by removing this reaction product [39,40]. As previously reported, biochar can increase fungal phosphate solubilization by promoting organic acid production and by mitigating the toxicity of elements released from the P source [31]. Ionic forms of Al, F, and HMs are released concomitantly with P during the solubilization of Araxá RP [41]. Likewise, Al3+ is one of the reaction products of AlPO4 solubilization. Biochar can adsorb such ions [31,42,43] and, therefore, remove reaction products potentially inhibitory for A. niger, allowing for the increased solubilization of AlPO4 and Araxá RP. These results suggest that SS biochar could improve bioprocesses aimed at producing fertilizer by the microbial solubilization of Al and F-containing phosphate ores, such as crandallite and fluorapatite [38,41,44].
The biochars produced at 300 and 500 °C presented 4.11 and 6.13% total P, respectively. However, water-soluble P was negligible. Most of the P contained in SS biochars is in the form of insoluble calcium–phosphate compounds [26,27], similar to the P minerals found in rock phosphates [45]. Calcium phosphates are promptly solubilized by A. niger as a result of medium acidification [29,44,46]. In the present study, A. niger acidified the medium to a pH of 2.1, resulting in the solubilization of nearly 50% of the P contained in the SS biochar after 7 days. This value is substantially higher than observed in a solid-state system with A. niger, which reached only 5% P extraction [47]. Although a solid-state system resembles soil in terms of aeration and moisture content, the lack of a diluent or sink for potentially inhibitory compounds released from biochar during its solubilization can make the environment unfavorable for microbial growth.
The pyrolysis temperature did not affect the amount of P solubilized from the biochar by A. niger. Even though the biochar produced at 500 °C presented a P content nearly 50% higher, the soluble P concentration at the end of the incubation was similar for the biochar produced at 300 and 500 °C. Likewise, in a soil–plant study, the soil-available P level was not affected by different pyrolysis temperatures employed to produce biochar from SS [14]. More stable forms of P are formed in SS biochar produced at higher pyrolysis temperatures [27], which may have impaired further fungal solubilization of the biochar produced at 500 °C. Indeed, extremely stable P–Al compounds presenting low solubility in citric acid have been found in SS biochar produced at 500 °C [28]. Moreover, in a previous study, SS biochar produced at the lowest temperature (300 °C) presented P more readily available by distinct extractant solutions, including neutral ammonium citrate + water and Mehlich-1, as influenced by higher levels of carbon and nitrogen in the biochar [48].
Our results suggest that a joint application of SS biochar and A. niger could improve P availability in P-fixing soils due to P solubilization from the biochar. Previous research has shown that SS biochar increased the available P content in soil [14,19]. However, based on the biochar P content, doses were high (~2 t P2O5 ha−1) while less than 0.01% of the P contained in the biochar was released in the first cropping seasons [14]. Although a residual effect on the soil P content was observed along the cropping seasons, the fraction of the P in the biochar that became available was low [14]. Therefore, the data obtained in the present study suggest that the P-use efficiency from biochar could be improved by A. niger inoculation and, thus, similar benefits could be obtained with lower doses. These results are limited to in vitro conditions, ensuring the need to expand the evaluations to include soil and plant components.
Oxisols show a high P-fixing capacity, being able to sorb more than 2 mg P g−1 [3,49,50]. Interestingly, biochar and A. niger improved the efficiency of the soluble fertilizer TSP in contact with an Oxisol. Taking into account the soil maximum P adsorption capacity (MPAC), 16.7 mg P L−1 was expected to be sorbed by soil, i.e., 67% of the P contained in TSP, which is in good agreement with the value observed (62%). On the other hand, in the presence of biochar and A. niger, all the P contained in TSP remained available. Therefore, a joint application of TSP, SS biochar, and A. niger could supply readily available P from TSP to fulfill initial crop requirements and afterward slowly release P from biochar [14,27] to later stages of crop development. This strategy would be particularly interesting for perennial crops in which long-term benefits could be obtained [51]. Moreover, increased P availability was observed in a soil receiving a combined application of mineral P fertilizer and biochar, which was attributed to chemical and physical changes caused by biochar in the soil [52]. Our results suggest that soil microorganisms can also play a role in this process, being another significant component in the interaction between soil and biochar.

5. Conclusions

The results of the present study show for the first time the action of A. niger in the solubilization of P from SS biochar. In addition, this study demonstrated that the SS biochar potentiates the P solubilization from rock phosphate by A. niger. Therefore, the results confirm the hypothesis that P-rich biochars can both boost P release from phosphate minerals and act as a P source itself. SS biochar improves the solubilization of AlPO4 and rock phosphate by A. niger. Additionally, A. niger can solubilize up to 50% of the P contained in the SS biochar. The joint application of SS biochar and A. niger in a solution containing P-fixing soil promotes P solubilization and improves TSP efficiency, increasing the amount of P that remained in the solution after contact with the soil particles. As a perspective, these in vitro findings need to be further evaluated in a soil–plant system. Therefore, for agronomic and environmental applications, an additional evaluation must be performed in field experiments. Finally, the scaling-up process and economic analysis need to be better understood.

Author Contributions

Conceptualization, K.F.R. and G.d.O.M.; methodology, K.F.R., C.C.d.F. and G.d.O.M.; validation, K.F.R. and G.d.O.M.; formal analysis, K.F.R., C.C.d.F. and G.d.O.M.; investigation, K.F.R.; resources, C.C.d.F. and G.d.O.M.; writing—original draft preparation, K.F.R.; writing—review and editing, C.C.d.F. and G.d.O.M.; visualization, C.C.d.F. and G.d.O.M.; supervision, G.d.O.M.; project administration, G.d.O.M.; funding acquisition, G.d.O.M. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the Fundação de Amparo à Pesquisa do Estado de Minas Gerais (FAPEMIG), grant number APQ-01842-17, and the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), grant number 407793/2021-6.

Data Availability Statement

The data presented in this study are openly available in Mendeley Data at dx.doi.org/10.17632/2gtt93zx5z.2 (accessed on 11 April 2023).

Conflicts of Interest

The authors declare no conflict of interest. The funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript; or in the decision to publish the results.

References

  1. Alexandratos, N.; Bruinsma, J. World Agriculture towards 2030/2050: The 2012 Revision; FAO: Rome, Italy, 2012. [Google Scholar]
  2. FAO. FAOSTAT: Fertilizers by Nutrient. Available online: http://www.fao.org/faostat/en/#data/RFN (accessed on 12 March 2023).
  3. Roy, E.D.; Richards, P.D.; Martinelli, L.A.; Coletta, L.D.; Lins, S.R.M.; Vazquez, F.F.; Willig, E.; Spera, S.A.; VanWey, L.K.; Porder, S. The Phosphorus Cost of Agricultural Intensification in the Tropics. Nat. Plants 2016, 2, 16043. [Google Scholar] [CrossRef] [PubMed]
  4. Cordell, D.; White, S. Peak Phosphorus: Clarifying the Key Issues of a Vigorous Debate about Long-Term Phosphorus Security. Sustainability 2011, 3, 2027–2049. [Google Scholar] [CrossRef]
  5. Vassilev, N.; Martos, E.; Mendes, G.; Martos, V.; Vassileva, M. Biochar of Animal Origin: A Sustainable Solution to the Global Problem of High-Grade Rock Phosphate Scarcity? J. Sci. Food Agric. 2013, 93, 1799–1804. [Google Scholar] [CrossRef]
  6. Mayer, B.K.; Baker, L.A.; Boyer, T.H.; Drechsel, P.; Gifford, M.; Hanjra, M.A.; Parameswaran, P.; Stoltzfus, J.; Westerhoff, P.; Rittmann, B.E. Total Value of Phosphorus Recovery. Environ. Sci. Technol. 2016, 50, 6606–6620. [Google Scholar] [CrossRef]
  7. Rockström, J.; Steffen, W.; Noone, K.; Persson, A.; Chapin, F.S.; Lambin, E.F.; Lenton, T.M.; Scheffer, M.; Folke, C.; Schellnhuber, H.J.; et al. A Safe Operating Space for Humanity. Nature 2009, 461, 472–475. [Google Scholar] [CrossRef]
  8. Withers, P.J.A.; Elser, J.J.; Hilton, J.; Ohtake, H.; Schipper, W.J.; Van Dijk, K.C. Greening the Global Phosphorus Cycle: How Green Chemistry Can Help Achieve Planetary P Sustainability. Green Chem. 2015, 17, 2087–2099. [Google Scholar] [CrossRef]
  9. Bunce, J.T.; Ndam, E.; Ofiteru, I.D.; Moore, A.; Graham, D.W. A Review of Phosphorus Removal Technologies and Their Applicability to Small-Scale Domestic Wastewater Treatment Systems. Front. Environ. Sci. 2018, 6, 8. [Google Scholar] [CrossRef]
  10. Peng, L.; Dai, H.; Wu, Y.; Peng, Y.; Lu, X. A Comprehensive Review of Phosphorus Recovery from Wastewater by Crystallization Processes. Chemosphere 2018, 197, 768–781. [Google Scholar] [CrossRef]
  11. Chrispim, M.C.; Scholz, M.; Nolasco, M.A. Phosphorus Recovery from Municipal Wastewater Treatment: Critical Review of Challenges and Opportunities for Developing Countries. J. Environ. Manag. 2019, 248, 109268. [Google Scholar] [CrossRef]
  12. De-Bashan, L.E.; Bashan, Y. Recent Advances in Removing Phosphorus from Wastewater and Its Future Use as Fertilizer (1997–2003). Water Res. 2004, 38, 4222–4246. [Google Scholar] [CrossRef]
  13. Zhu, F.; Cakmak, E.K.; Cetecioglu, Z. Phosphorus Recovery for Circular Economy: Application Potential of Feasible Resources and Engineering Processes in Europe. Chem. Eng. J. 2023, 454, 140153. [Google Scholar] [CrossRef]
  14. Figueiredo, C.C.; Pinheiro, T.D.; de Oliveira, L.E.Z.; de Araujo, A.S.; Coser, T.R.; Paz-Ferreiro, J. Direct and Residual Effect of Biochar Derived from Biosolids on Soil Phosphorus Pools: A Four-Year Field Assessment. Sci. Total Environ. 2020, 739, 140013. [Google Scholar] [CrossRef] [PubMed]
  15. Figueiredo, C.C.; Chagas, J.K.M.; da Silva, J.; Paz-Ferreiro, J. Short-Term Effects of a Sewage Sludge Biochar Amendment on Total and Available Heavy Metal Content of a Tropical Soil. Geoderma 2019, 344, 31–39. [Google Scholar] [CrossRef]
  16. Liang, S.; Chen, H.; Zeng, X.; Li, Z.; Yu, W.; Xiao, K.; Hu, J.; Hou, H.; Liu, B.; Tao, S.; et al. A Comparison between Sulfuric Acid and Oxalic Acid Leaching with Subsequent Purification and Precipitation for Phosphorus Recovery from Sewage Sludge Incineration Ash. Water Res. 2019, 159, 242–251. [Google Scholar] [CrossRef] [PubMed]
  17. Bridle, T.R.; Pritchard, D. Energy and Nutrient Recovery from Sewage Sludge via Pyrolysis. Water Sci. Technol. 2004, 50, 169–175. [Google Scholar] [CrossRef]
  18. Paz-Ferreiro, J.; Nieto, A.; Méndez, A.; Askeland, M.; Gascó, G. Biochar from Biosolids Pyrolysis: A Review. Int. J. Environ. Res. Public Health 2018, 15, 956. [Google Scholar] [CrossRef] [PubMed]
  19. Sousa, A.A.T.C.; Figueiredo, C.C. Sewage Sludge Biochar: Effects on Soil Fertility and Growth of Radish. Biol. Agric. Hortic. 2016, 32, 127–138. [Google Scholar] [CrossRef]
  20. Li, F.; Liang, X.; Niyungeko, C.; Sun, T.; Liu, F.; Arai, Y. Effects of Biochar Amendments on Soil Phosphorus Transformation in Agricultural Soils. Adv. Agron. 2019, 158, 131–172. [Google Scholar] [CrossRef]
  21. Lehmann, J.; Rillig, M.C.; Thies, J.; Masiello, C.A.; Hockaday, W.C.; Crowley, D. Biochar Effects on Soil Biota—A Review. Soil Biol. Biochem. 2011, 43, 1812–1836. [Google Scholar] [CrossRef]
  22. Figueiredo, C.C.; Farias, W.M.; Coser, T.R.; Monteiro de Paula, A.; Sartori da Silva, M.R.; Paz-Ferreiro, J. Sewage Sludge Biochar Alters Root Colonization of Mycorrhizal Fungi in a Soil Cultivated with Corn. Eur. J. Soil Biol. 2019, 93, 103092. [Google Scholar] [CrossRef]
  23. Zhou, Y.; Li, D.; Li, Z.; Guo, S.; Chen, Z.; Wu, L.; Zhao, Y. Greenhouse Gas Emissions from Soils Amended with Cornstalk Biochar at Different Addition Ratios. Int. J. Environ. Res. Public Health 2023, 20, 927. [Google Scholar] [CrossRef] [PubMed]
  24. Zhu, Y.; Ma, J.; Chen, F.; Yu, R.; Hu, G.; Zhang, S. Remediation of Soil Polluted with Cd in a Postmining Area Using Thiourea-Modified Biochar. Int. J. Environ. Res. Public Health 2020, 17, 7654. [Google Scholar] [CrossRef] [PubMed]
  25. Bashir, M.A.; Wang, X.; Naveed, M.; Mustafa, A.; Ashraf, S.; Samreen, T.; Nadeem, S.M.; Jamil, M. Biochar Mediated-Alleviation of Chromium Stress and Growth Improvement of Different Maize Cultivars in Tannery Polluted Soils. Int. J. Environ. Res. Public Health 2021, 18, 4461. [Google Scholar] [CrossRef] [PubMed]
  26. Schneider, F.; Haderlein, S.B. Potential Effects of Biochar on the Availability of Phosphorus—Mechanistic Insights. Geoderma 2016, 277, 83–90. [Google Scholar] [CrossRef]
  27. Adhikari, S.; Gascó, G.; Méndez, A.; Surapaneni, A.; Jegatheesan, V.; Shah, K.; Paz-Ferreiro, J. Influence of Pyrolysis Parameters on Phosphorus Fractions of Biosolids Derived Biochar. Sci. Total Environ. 2019, 695, 133846. [Google Scholar] [CrossRef] [PubMed]
  28. Steckenmesser, D.; Vogel, C.; Adam, C.; Steffens, D. Effect of Various Types of Thermochemical Processing of Sewage Sludges on Phosphorus Speciation, Solubility, and Fertilization Performance. Waste Manag. 2017, 62, 194–203. [Google Scholar] [CrossRef] [PubMed]
  29. Mendes, G.O.; Freitas, A.L.M.; Pereira, O.L.; Silva, I.R.; Vassilev, N.B.; Costa, M.D. Mechanisms of Phosphate Solubilization by Fungal Isolates When Exposed to Different P Sources. Ann. Microbiol. 2014, 64, 239–249. [Google Scholar] [CrossRef]
  30. Mendes, G.O.; Bahri-Esfahani, J.; Csetenyi, L.; Hillier, S.; George, T.S.; Gadd, G.M. Chemical and Physical Mechanisms of Fungal Bioweathering of Rock Phosphate. Geomicrobiol. J. 2021, 38, 384–394. [Google Scholar] [CrossRef]
  31. Mendes, G.O.; Zafra, D.L.; Vassilev, N.B.; da Silva, I.R.; Ribeiro, J.I.; Costa, M.D. Biochar Enhances Aspergillus Niger Rock Phosphate Solubilization by Increasing Organic Acid Production and Alleviating Fluoride Toxicity. Appl. Environ. Microbiol. 2014, 80, 3081–3085. [Google Scholar] [CrossRef]
  32. Mendes, G.O.; da Silva, N.M.R.M.; Anastácio, T.C.; Vassilev, N.B.; Ribeiro, J.I.; da Silva, I.R.; Costa, M.D. Optimization of Aspergillus Niger Rock Phosphate Solubilization in Solid-State Fermentation and Use of the Resulting Product as a P Fertilizer. Microb. Biotechnol. 2015, 8, 930–939. [Google Scholar] [CrossRef]
  33. Nautiyal, C.S. An Efficient Microbiological Growth Medium for Screening Phosphate Solubilizing Microorganisms. FEMS Microbiol. Lett. 1999, 170, 265–270. [Google Scholar] [CrossRef] [PubMed]
  34. USEPA Method 3050B: Acid Digestion of Sediments, Sludges, and Soils. Available online: https://www.epa.gov/hw-sw846/sw-846-test-method-3050b-acid-digestion-sediments-sludges-and-soils (accessed on 9 April 2023).
  35. Braga, J.M.; Defelipo, B. V Determinação Espectrofotométrica de Fósforo Em Extratos de Solo e Material Vegetal. Rev. Ceres 1974, 21, 73–85. [Google Scholar]
  36. Manual de Métodos de Análise de Solo, 3rd ed.; Teixeira, P.C.; Donagemma, G.K.; Fontana, A.; Teixeira, W.G. (Eds.) Embrapa: Brasília, Brazil, 2017; ISBN 9788570357717. [Google Scholar]
  37. Oliveira, C.M.B.; Gatiboni, L.C.; Miquelluti, D.J.; Smyth, T.J.; Almeida, J.A. Maximum Phosphorus Adsorption Capacity and Binding Energy Constant of an Oxisol Fitting Different Langmuir Models. Rev. Bras. Cienc. Solo 2014, 38, 1805–1815. [Google Scholar] [CrossRef]
  38. Mendes, G.O.; Murta, H.M.; Valadares, R.V.; Silveira, W.B.d.; Silva, I.R.d.; Costa, M.D. Oxalic Acid Is More Efficient than Sulfuric Acid for Rock Phosphate Solubilization. Miner. Eng. 2020, 155, 106458. [Google Scholar] [CrossRef]
  39. Robinson, J.S.; Syers, J.K.; Bolan, N.S. Importance of Proton Supply and Calcium-Sink Size in the Dissolution of Phosphate Rock Materials of Different Reactivity in Soil. J. Soil Sci. 1992, 43, 447–459. [Google Scholar] [CrossRef]
  40. Mendes, G.d.O.; Dyer, T.; Csetenyi, L.; Gadd, G.M. Rock Phosphate Solubilization by Abiotic and Fungal-produced Oxalic Acid: Reaction Parameters and Bioleaching Potential. Microb. Biotechnol. 2022, 15, 1189–1202. [Google Scholar] [CrossRef]
  41. Mendes, G.O.; Vassilev, N.B.; Bonduki, V.H.A.; Silva, I.R.; Ribeiro, J.I.; Costa, M.D. Inhibition of Aspergillus Niger Phosphate Solubilization by Fluoride Released from Rock Phosphate. Appl. Environ. Microbiol. 2013, 79, 4906–4913. [Google Scholar] [CrossRef]
  42. Chen, H.; Zhang, J.; Tang, L.; Su, M.; Tian, D.; Zhang, L.; Li, Z.; Hu, S. Enhanced Pb Immobilization via the Combination of Biochar and Phosphate Solubilizing Bacteria. Environ. Int. 2019, 127, 395–401. [Google Scholar] [CrossRef]
  43. Qian, L.; Chen, B.; Hu, D. Effective Alleviation of Aluminum Phytotoxicity by Manure-Derived Biochar. Environ. Sci. Technol. 2013, 47, 2737–2745. [Google Scholar] [CrossRef]
  44. Silva, U.d.C.C.; Mendes, G.d.O.; Silva, N.M.R.M.; Duarte, J.L.; Silva, I.R.; Tótola, M.R.; Costa, M.D.M.D.; Totola, M.R.; Costa, M.D.M.D. Fluoride-Tolerant Mutants of Aspergillus Niger Show Enhanced Phosphate Solubilization Capacity. PLoS ONE 2014, 9, e110246. [Google Scholar] [CrossRef]
  45. Smith, E.A.; Mayfield, C.I.; Wong, P.T.S. Physical and Chemical Characterization of Selected Natural Apatites in Synthetic and Natural Aqueous Solutions. Water Air Soil Pollut. 1977, 8, 401–415. [Google Scholar] [CrossRef]
  46. Schneider, K.D.; van Straaten, P.; de Orduna, R.M.; Glasauer, S.; Trevors, J.; Fallow, D.; Smith, P.S. Comparing Phosphorus Mobilization Strategies Using Aspergillus Niger for the Mineral Dissolution of Three Phosphate Rocks. J. Appl. Microbiol. 2010, 108, 366–374. [Google Scholar] [CrossRef] [PubMed]
  47. Raymond, N.S.; Jensen, L.S.; Müller Stöver, D. Enhancing the Phosphorus Bioavailability of Thermally Converted Sewage Sludge by Phosphate-Solubilising Fungi. Ecol. Eng. 2018, 120, 44–53. [Google Scholar] [CrossRef]
  48. Figueiredo, C.C.d.; Reis, A.d.S.P.J.; Araujo, A.S.d.; Blum, L.E.B.; Shah, K.; Paz-Ferreiro, J. Assessing the Potential of Sewage Sludge-Derived Biochar as a Novel Phosphorus Fertilizer: Influence of Extractant Solutions and Pyrolysis Temperatures. Waste Manag. 2021, 124, 144–153. [Google Scholar] [CrossRef] [PubMed]
  49. Ker, J.C.; Fontes, M.P.F.; Souza, A.R.; Resende, M. Adsorção de Fósforo Em Alguns Solos Latossólicos: Relação Entre Mineralogia e Efeito de Calagem. Rev. Ceres 1996, 43, 216–226. [Google Scholar]
  50. Novais, R.F.; Smith, T.J. Fósforo Em Solo e Planta Em Condições Tropicais; Editora UFV: Viçosa, Brazil, 1999. [Google Scholar]
  51. Araújo, V.C.; Rossati, K.F.; Xavier, L.V.; Oliveira, V.A.d.; Carmo, G.J.d.S.; Assis, G.A.d.; Mendes, G.d.O. Enhanced Growth in Nursery of Coffee Seedlings Inoculated with the Rhizosphere Fungus Aspergillus Niger for Field Transplantation. Rhizosphere 2020, 15, 100236. [Google Scholar] [CrossRef]
  52. Wang, Q.; Xu, L.; Guo, D.; Wang, G.; Song, X.; Ma, Y. The Continuous Application of Biochar in Field: Effects on P Fraction, P Sorption and Release. Chemosphere 2020, 263, 128084. [Google Scholar] [CrossRef]
Sustainability 15 06940 g001 550
Figure 1. Soluble P after 7-day incubation of Aspergillus niger in culture medium with sparingly soluble P sources and sewage sludge biochar. Different letters in the same P source indicate statistical difference between treatments according to Fisher’s LSD test (p < 0.05). Error bars denote standard deviation (n = 3).
Figure 1. Soluble P after 7-day incubation of Aspergillus niger in culture medium with sparingly soluble P sources and sewage sludge biochar. Different letters in the same P source indicate statistical difference between treatments according to Fisher’s LSD test (p < 0.05). Error bars denote standard deviation (n = 3).
Sustainability 15 06940 g001
Sustainability 15 06940 g002 550
Figure 2. Soluble P (a) and pH (b) after 7-day incubation of culture medium supplemented with a P-fixing soil as affected by addition of Aspergillus niger (An), sewage sludge biochar 500 °C (B), and triple superphosphate (TSP). Different letters indicate statistical difference between treatments according to Fisher’s LSD test (p < 0.05). Error bars denote standard deviation (n = 4).
Figure 2. Soluble P (a) and pH (b) after 7-day incubation of culture medium supplemented with a P-fixing soil as affected by addition of Aspergillus niger (An), sewage sludge biochar 500 °C (B), and triple superphosphate (TSP). Different letters indicate statistical difference between treatments according to Fisher’s LSD test (p < 0.05). Error bars denote standard deviation (n = 4).
Sustainability 15 06940 g002
Table
Table 1. Phosphorus sources used in the experiments.
Table 1. Phosphorus sources used in the experiments.
P SourceTotal P
(g kg−1)		Water-Soluble P
(g kg−1)		pH (H2O)
AlPO42540.596.86
Ca3(PO4)22000.136.36
FePO4.2H2O1660.396.74
Araxá RP1400.396.88
Bayóvar RP1460.026.78
Table
Table 2. Physicochemical characteristics (average ± standard deviation, n = 3) of sewage sludge (SS) and biochars produced at 300 °C (biochar 300) and 500 °C (biochar 500).
Table 2. Physicochemical characteristics (average ± standard deviation, n = 3) of sewage sludge (SS) and biochars produced at 300 °C (biochar 300) and 500 °C (biochar 500).
PropertyUnitsSSBiochar 300Biochar 500
pH (CaCl2)-4.8 ± 0.45.8 ± 0.26.5 ± 0.3
C%21.0 ± 0.423.4 ± 0.419.0 ± 0.2
H%4.2 ± 0.13.6 ± 0.11.7 ± 0.1
N%3.0 ± 0.13.3 ± 0.12.3 ± 0.1
NO3-mg kg−123.3 ± 3.417.5 ± 1.25.84 ± 0.5
NH4+mg kg−1461.2 ± 36.0431.9 ± 20.2169.3 ± 10.5
H/C-2.4 ± 0.11.8 ± 0.11.1 ± 0.1
C/N-7.0 ± 0.17.0 ± 0.18.3 ± 0.1
Total Pg kg−135.7 ± 2.841.1 ± 3.261.3 ± 5.6
Water-soluble Pg kg−1nd0.02 ± 0.020.04 ± 0.02
Kg kg−10.8 ± 0.11.1 ± 0.11.3 ± 0.1
Cag kg−16.6 ± 0.16.7 ± 0.28.2 ± 0.3
Mgg kg−10.8 ± 0.11.8 ± 0.11.7 ± 0.1
Sg kg−16.7 ± 0.215.1 ± 1.07.4 ± 0.4
Total Cumg kg−1115 ± 1.0148 ± 1.0145 ± 1.0
Total Pbmg kg−1207 ± 1.0256 ± 3.0265 ± 1.0
Total Znmg kg−1306 ± 1.0321 ± 1.0411 ± 5.0
Total Crmg kg−1100 ± 1.0106 ± 2.0136 ± 1.0
Total Comg kg−120 ± 1.022 ± 1.025 ± 1.0
Total Mnmg kg−156 ± 1.058 ± 1.080 ± 2.0
Total Cumg kg−1115 ± 1.0148 ± 1.0145 ± 1.0
PVmL g−10.022 ± 0.0010.027 ± 0.0010.053 ± 0.002
SSAm² g−118.2 ± 1.220.2 ± 1.852.5 ± 4.3
Volatile matter% (db)45 ± 4.036.8 ± 4.417.8 ± 0.6
Ash% (db)54 ± 3.056.6 ± 2.677.6 ± 0.6
Fixed carbon% (db)-6.5 ± 1.84.7 ± 0.1
PV: pore volume; SSA: specific surface area; nd: not determined; db: on dry basis. Modified from Figueiredo et al. [14]. Reprinted with permission from Ref. [14]. 2023, Cícero Célio de Figueiredo.
Table
Table 3. Solubilized P (expressed as a percentage of the total P in each P source) from sparingly soluble P sources by Aspergillus niger after 7-day incubation in culture media supplemented with sewage sludge biochar.
Table 3. Solubilized P (expressed as a percentage of the total P in each P source) from sparingly soluble P sources by Aspergillus niger after 7-day incubation in culture media supplemented with sewage sludge biochar.
P SourceSS Biochar 300 °C aSS Biochar 500 °C aNo Biochar
AlPO4727353
Ca3(PO4)2928296
FePO4.2H2O505278
Araxá RP1075833
Bayóvar RP585141
a Values had the amount of P solubilized from the biochar discounted.
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

Rossati, K.F.; Figueiredo, C.C.d.; Mendes, G.d.O. Aspergillus niger Enhances the Efficiency of Sewage Sludge Biochar as a Sustainable Phosphorus Source. Sustainability 2023, 15, 6940. https://doi.org/10.3390/su15086940

AMA Style

Rossati KF, Figueiredo CCd, Mendes GdO. Aspergillus niger Enhances the Efficiency of Sewage Sludge Biochar as a Sustainable Phosphorus Source. Sustainability. 2023; 15(8):6940. https://doi.org/10.3390/su15086940

Chicago/Turabian Style

Rossati, Kamila Fernanda, Cícero Célio de Figueiredo, and Gilberto de Oliveira Mendes. 2023. "Aspergillus niger Enhances the Efficiency of Sewage Sludge Biochar as a Sustainable Phosphorus Source" Sustainability 15, no. 8: 6940. https://doi.org/10.3390/su15086940

APA Style

Rossati, K. F., Figueiredo, C. C. d., & Mendes, G. d. O. (2023). Aspergillus niger Enhances the Efficiency of Sewage Sludge Biochar as a Sustainable Phosphorus Source. Sustainability, 15(8), 6940. https://doi.org/10.3390/su15086940

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop