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Article

Elevating Sorghum Prosperity: Unveiling Growth Trends through Phosphate-Solubilizing Bacteria and Arbuscular Mycorrhizal Fungi Inoculation in Phosphate-Enriched Substrates

by
Fatima Zahra Aliyat
1,
Mohammed El Guilli
2,
Laila Nassiri
1,
Rachid Lahlali
3,*,
Essaid Ait Barka
4,* and
Jamal Ibijbijen
1
1
Environment and Valorization of Microbial and Plant Resources Unit, Faculty of Sciences, Moulay Ismail University, Meknes 50050, Morocco
2
National Institute of Agricultural Research, Regional Center for Agricultural Research, Kenitra 14000, Morocco
3
Phytopathology Unit, Department of Plant Protection, Ecole Nationale d’Agriculture de Menkes, Km10, Rte Haj Kaddour, BP S/40, Meknes 50001, Morocco
4
Unité de Recherche Résistance Induite et Bioprotection des Plantes, Université de Reims Champagne-Ardenne, USC 1488, 51100 Reims, France
*
Authors to whom correspondence should be addressed.
Agronomy 2024, 14(2), 370; https://doi.org/10.3390/agronomy14020370
Submission received: 30 December 2023 / Revised: 3 February 2024 / Accepted: 10 February 2024 / Published: 14 February 2024
(This article belongs to the Section Plant-Crop Biology and Biochemistry)
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Abstract

:
This study aimed to elucidate the impact of phosphate-solubilizing bacteria (PSB) and arbuscular mycorrhizal fungi (AMF) inoculation on sorghum growth within substrates derived from phosphate solid sludge, with the overarching objective of repurposing phosphate sludge to be a viable agricultural substrate. Four PSB strains (Serratia rubidaea, Enterobacter bugandensis, Pantoea agglomerans, Pseudomonas sp.) were meticulously selected from phosphate solid sludge, along with two AMF strains (Rhizophagus intraradices and Funneliformis mosseae), constituting the experimental inocula. Phosphate solid sludge was judiciously blended with peat at varying volumetric proportions (0%, 10%, 20%, 40%, and 60%), providing the matrix for sorghum cultivation, and concomitantly subjected to inoculation with PSB and AMF. Following a meticulously monitored two-month duration, a comprehensive evaluation of diverse morphological parameters, biomass accrual, nitrogen content, total phosphorus concentration, potassium levels, calcium content, and root colonization in sorghum plants was conducted. The empirical findings underscored a discernible decline in the assessed parameters with escalating concentrations of phosphate solid sludge. Particularly noteworthy was the pronounced amelioration observed in plants inoculated with AMF in comparison to both the control and PSB-inoculated counterparts. In conclusion, the application of raw phosphate solid sludge as an agricultural substrate is deemed unsuitable, prompting the imperative need for further in-depth investigations to ascertain the nuanced intricacies underlying these outcomes.

1. Introduction

Soils, regarded as the foundational bedrock underpinning food and agricultural production security, play a critical role in providing plants with essential elements—nutrients, water, and structural support for their intricate root systems. Recent insights accentuate the nuanced ecosystem services offered by soils, going beyond the mere sustenance of food production to encompass the vital role they play in ensuring the stability and resilience of the Earth’s environment [1,2].
Despite the varied origins of soils across ecosystems, they serve as thriving habitats for an extensive diversity of microorganisms, including bacteria, fungi, microalgae, and protists [3]. Within this rich microbial tapestry, bacteria and fungi inhabit the soil matrix, undertaking diverse roles, among which is the production of secondary metabolites [4]. Microorganisms, whether introduced into seeds, leaves, seedling roots, or the soil itself—individually or in combination—take residence in the rhizosphere or within the plants, actively promoting growth and imparting resilience to abiotic stresses.
Bacteria, in particular, contribute significantly to plant development through mechanisms such as enhancing nutrient availability (e.g., nitrogen, phosphorus, and potassium), secreting phytohormones, and indirectly fostering systemic resistance [5,6,7,8,9,10]. In this intricate interplay, phosphate-solubilizing bacteria (PSB), a specific subset of soil bacteria, emerge as promising agents capable of improving phosphorus utilization efficiency, thereby promoting economically and environmentally sustainable crop development [11,12,13].
The collaborative relationship between plants and microorganisms in the soil highlights the intrinsic interplay of the ecosystem, where the microbial community acts as a crucial ally in enhancing plant health and productivity [14]. Understanding and harnessing the potential of these microscopic partners, such as phosphate-solubilizing bacteria, holds the key to advancing agricultural practices that are not only productive but also environmentally conscientious. As we explore this symbiotic relationship further, we discover opportunities for promoting sustainable agriculture that align with the complex dynamics of our planet’s ecosystems.
Mycorrhiza, a symbiotic association between plant roots and fungi, further contributes to plant health [15,16]. Arbuscular mycorrhizal fungi (AMF) represent a prevalent fungal group in agricultural soils, forming mutually beneficial associations with approximately 80% of terrestrial plants, including a significant proportion of crops [17,18]. Studies demonstrate the effectiveness of AMF in promoting the development of various crops, such as maize, sorghum, and soybeans [19,20,21,22]. Additionally, arbuscular mycorrhizal fungi boost the accessibility of slowly diffusing ions, notably phosphorus (P), contributing an estimated 80% to P uptake in mycorrhizal plants. These fungi also play a crucial role in providing both macro- and micronutrients, encompassing nitrogen, potassium, magnesium, copper, and zinc [23,24].
Morocco, as the world’s leading exporter and the third-largest producer of natural phosphates, commands an impressive share exceeding 70% of the global phosphate deposits. The annual extraction of over 23 million tons of minerals leads to a substantial generation of phosphate sludge, constituting 90% of the treatment plant’s discharges [25,26]. The volume of this waste becomes increasingly significant with rising phosphate production, resulting in P loss during treatment. This not only diminishes yield productivity but also adversely impacts P recovery efficiency. Furthermore, the disposal of substantial amounts of phosphate sludge into the environment carries severe environmental consequences. Recent efforts have focused on recovering the lost P fraction from phosphate sludge through various approaches, such as thermo-chemical, thermo-reductive, composting, by introducing it as a source of phosphorus in phosphorous-poor soils, and wet chemical leaching [26,27,28,29]. Despite their efficacy, these methods entail considerable energy consumption, posing significant environmental challenges. Consequently, there is a pressing need for environmentally sustainable technologies for P recycling and recovery [28].
The Plant Growth-Promoting (PGP) characteristics of microorganisms, particularly their ability to solubilize P, present a potentially eco-sustainable solution for recovering P from phosphate sludge. Notably, phosphate sludge tends to have a high concentration of calcium, which immobilizes bioavailable P. We hypothesize that the P-solubilizing capacity of PSB isolated from solid phosphate sludge or AMF associated with the sludge can enhance the availability of soluble phosphate in sludge. This, in turn, could enable the reuse of phosphate sludge as an agricultural substrate, with the potential to promote plant growth. Consequently, our study addresses the following key questions: Can PSB or AMF, when combined with phosphate solid sludge, provide a viable solution for reusing phosphate sludge? Is it feasible to employ phosphate solid sludge as an agricultural substrate?

2. Materials and Methods

2.1. Physico-Chemical Analysis of Phosphate Sludge

Phosphate sludge samples were collected from Khouribga (Morocco; 32°45′17.7645″, 006°51′14.5182″) near to the phosphate mining center and maintained in a refrigerator at 4 °C until examined. Samples were air-dried. The physicochemical properties of the sludge such as organic matter, conductivity, ammonium, nitrate, chloride, sodium, pH, total limestone, active limestone, calcium, phosphorus, potassium, magnesia, copper, manganese, iron, zinc, sulfur, were analyzed following the methods by Tabrika et al. [30]. Also, pH (water) and pH (KCl) of the different mixtures (0%, 10%, 20%, 40%, and 60%), were measured. The pH (water) and pH KCl were extracted with distilled water at a ratio of 2:5 soil/water, and KCl 1.0 M at a ratio of 2:5 soil/KCl 1.0 M, respectively, and measured through a pH meter.

2.2. Inoculum Preparation

2.2.1. Bacterial Strains

Four bacterial strains (BM11, BM28, CB13, and BT125) (Table 1) were selected to perform the experiment. Their strains were isolated and identified as described by Aliyat et al. [5]. The strains were selected according to their phosphate solubilization efficiency and PGP traits. It is mainly potassium solubilization, the production of Indole-3-acetic acid (IAA), siderophores, and Hydrogen Cyanide Production.
Each strain was cultured in 100 mL of the National Botanical Research Institute’s phosphate growth medium (NBRIP) for 4 days at 28 °C under shaking (150 rpm). Then, cells bacteria were collected by centrifugation at 6 415 rpm for 5 min, washed with sterile saline solution with 0.9%, and re-suspended to obtain an inoculum with 1.5 × 108 CFU/mL, following the McFarland nephelometer standard [31].

2.2.2. Mycorrhizal Strains

To initiate mycorrhizal inoculation, two strains, namely Rhizophagus intraradices and Funneliformis mosseae, were employed. We used an inoculum purchased from a private company containing 25 spores/g of Rhizoglomus intraradices and 25 spores/g of Funneliformis mosseae, whose viability has been checked before application in the experimentation.

2.3. Sowing, Preparation of Plants and Inoculation

Sorghum seeds (99% viability) were disinfected with 80% (v/v) ethanol and 5% (v/v) sodium hypochlorite, and rinsed multiple times. Then, the seeds were placed in plastic pots containing the substrate. Four seeds were sown per pot. On the fifth day after germination, the seedlings were thinned to one seedling per pot. For inoculation with bacterial strains, the inoculation was performed by injection of 5 mL of bacterial suspension (form each isolate) with a micropipette to the sorghum seedlings to the bottom of the stem, while for treatment inoculated by AMF, the inoculation was performed within each pot; 3 g of the mixture was introduced into the seed holes during sowing and the seedlings were regularly irrigated with tap water.

2.4. Experimental Design

In this experiment, and according to the objective of the study, peat was chosen as a substrate to make mixtures of phosphate solid sludge with different concentrations (0, 10, 20, 40, and 60%) which were inoculated with the 4 PSB, selected separately, and a mixture with AMF. The peat and phosphate sludges were autoclaved, separately, for 20 min at 121 °C, which was repeated three times, and after autoclaving, the substrates were used 10 days later. The experiment was performed in a greenhouse (Figure 1) and treatments were arranged using the randomized complete block approach with 5 replicates for each treatment. Plants not inoculated served as control.

2.5. Morphological Traits of Plants Growth

At the two-month mark following the experiment, we carried out a thorough assessment of the morphological characteristics of plant growth. This involved measuring the plant height, as well as determining the fresh and dry weights (achieved through a 70 °C drying process for 72 h). Subsequently, the roots were carefully severed, thoroughly shaken, and meticulously cleansed with water to remove any adhering soil particles.

2.6. Photosynthetic Pigment Determination

Sorghum leaf samples were taken from the plants, in triplicate, six weeks after germination to evaluate the chlorophyll pigments (chlorophyll a and chlorophyll b) by the spectrophotometric method [32]. After crushing the leaf samples with a porcelain mortar, 50 mg of the ground material was stirred in 1 mL of 80% acetone in Eppendorf tubes for 90 min to ensure the extraction of all pigments. Then, the mixture was centrifuged at 14,000 rpm for 15 min at 4 °C. The optical density (OD) of the supernatant obtained was measured at 645 nm and 663 nm using a UV–visible spectrophotometer (UV-2005, SELECTA, Spain). Concentrations of Chlorophyll a and b were calculated as follows: Cha = 15.65 OD663 − 7.340 OD645, Chb = 27.05 OD645 − 11.21 OD663; Cha and Chb represents the concentration of chlorophyll a, b, respectively, and OD represents optical density at a given wavelength.

2.7. Determination of Total Nitrogen, Total Phosphorus, Potassium Calcium Content in Plant Shoots

Plant tissue (sorghum) was dried at 70 °C. The materials were mixed and crushed to obtain a homogenous sample from which appropriate subsamples could be easily extracted [33]. The Kjeldahl method was used to determine the total nitrogen content in the shoot plants [34]. The total P analysis was performed using the colorimetric method developed by Bataglia et al. [35], 100–200 mg of shoot samples were digested using a nitric/perchloric acid. Inductively coupled plasma ICP-OES was used to measure potassium and calcium after complete digestion of 0.3 g of plant material using HNO3-HClO4−H2SO4 [36].

2.8. Mycorrhizal Root Colonization and Infection Assessment

The root segments were cleaned with distilled water, then placed in capsules containing a 10% KOH solution and boiled in a water bath for 1 h at 90 °C to remove the cytoplasmic content. The roots were then washed with distilled water. The samples were then immersed in 2% hydrochloric acid for 5 min to remove the KOH residues. These samples were washed again with distilled water before being placed in a lactoglycerol solution containing 0.05% trypan blue and left in a 90 °C water bath for 15 to 40 min, after which the excess color was removed with a lactoglycerol solution [37]. For microscopic examination, the roots were cut to 1 cm long. The mycorrhizal infection was carried out as previously described [38].

2.9. Statistical Analysis

The SPSS analytical software (SPSS 23.0) was used to evaluate the experimental data. Five biological replicates were used to collect the experimental data. The data were presented as a mean with a standard deviation (SE). The data were subjected to ANOVA procedure with p levels as the factor and Duncan’s test was used for means separation (p < 0.05). Heatmaps were made using Pearson correlation to evaluate the correlation between all parameters studied in the experiments. The package “ggplot2” was used to create the heatmaps using “corr” to perform coefficient matrices. The software R (version 3.5.3) was used to create the heatmap.

3. Results

3.1. Physico-Chemical Parameters of Phosphate Solid Sludge

The results of the different physical and chemical tests on the phosphate solid sludges are shown in Table 2. The pH (water) and pH (KCl) show that the phosphate solid sludge is predominantly alkaline, includes a significant amount of phosphate limestone, and is poor in organic matter. The pH of the different mixtures used in this study with different concentrations of phosphate sludge (0%, 10%, 20%, 40%, and 60%) was determined (Table S1). The results showed that, overall, the mixtures with a low percentage are slightly acidic (0%, 10%, and 20%), while the mixtures with a high percentage (40% and 60%) have an alkaline pH, based on pH (water) and pH (KCl).

3.2. Morphological Traits of Plant Growth and Photosynthetic Pigments

In Table 3, the comprehensive results of all treatments are detailed, encompassing parameters such as shoot length, shoot and root dry weights, and photosynthetic pigments in sorghum. The data consistently show decreasing morphological characteristics and photosynthetic pigment concentrations in sorghum growth as the amount of phosphate solid sludge increases across all treatments. A statistically significant difference (p < 0.05) is evident when comparing the control group with all other treatments. Notably, a marked difference in plant growth was observed between the control treatment and treatments inoculated with PSBs. Sorghum plant height and biomass exhibited a noteworthy improvement, reaching up to 15% compared to the control. Nevertheless, upon comparing the inoculation effects of the four PSBs, no discernible differences were observed.
Conversely, sorghum plants inoculated with AMF demonstrated a substantial improvement in growth compared to both the control group and those inoculated with PSBs. The growth increase for sorghum ranges from 46 to 75%, depending on the concentration of solid phosphate sludge (0, 10, 20, 40, and 60%, respectively).
Furthermore, the escalation in phosphate solid sludge concentration exerts a detrimental influence on Chlorophyll a and b in the sorghum shoot, as depicted in Table 3, with pigment content decreasing with rising phosphate sludge concentration. At lower concentrations, a significant reduction in Chlorophyll a and b was observed in the sorghum shoot for all PSB-inoculated treatments. The most pronounced decrease in Chlorophyll content occurs when seedlings are exposed to the highest concentrations of phosphate sludge (60%). In contrast, plants inoculated with AMF demonstrated improvements across all treatments compared to controls and PSB inoculation.

3.3. Plant Mineral Nutrient Content

Table S2 presents a comprehensive overview of the effects of varying proportions of solid phosphate sludge on the nutrient content of plants, specifically focusing on Nitrogen, Phosphorus, Potassium, and Calcium. The absorption rates of nutrients N, P, K, and Ca++ by sorghum exhibited significant differences (p < 0.05) among all treatments. Notably, mineral element concentrations exhibited a discernible decline with the increasing fraction of phosphate solid sludge. Table S2 details the effects of varying proportions of solid phosphate sludge on the nutrient content of plants, specifically focusing on Nitrogen, Phosphorus, Potassium, and Calcium. In terms of Nitrogen content, there is notable variation across treatments, and the 10% AMF treatment stands out with the highest Nitrogen levels. Regarding Phosphorus, the 10% AMF treatment again demonstrates superiority, with elevated levels also observed in BT125 at 10%. The 10% AMF treatment consistently exhibits the highest Potassium content, with additional noteworthy effects seen in BT125 at 10%. In terms of Calcium, the 10% AMF treatment leads to the highest content, while BM28 also shows elevated levels. However, caution is warranted as the 40% and 60% treatment levels return “Not Detected” values for nutrient levels, showing that the quantities of plant matter in the 40% and 60% treatments were too low.

3.4. Mycorrhizal Root Colonization

We tracked the progression of arbuscular mycorrhizal fungi during the growth of sorghum by assessing the specific variable of mycorrhizal root colonization (Figure 2). The intensity of mycorrhizal colonization exhibited noteworthy variations due to the different treatments, as indicated in Table 4. In particular, the treatment with 20% solid phosphate sludge demonstrated the highest root colonization by AMF, reaching 79%.

3.5. Heatmap and Correlation between Parameters

Pearson correlation analysis was carried out to quantify the relationship between the application of phosphate sludge inoculated with PSB and AMF strains and the parameters studied: plant morphology, biomass, photosynthetic pigments, minerals uptakes (N, P, K and Ca). A negative correlation was observed between phosphate sludge concentrations and all parameters studied (Figure 3).

4. Discussion

Phosphate sludge is a byproduct of phosphate extraction and rock phosphate treatment. Considering its high residual phosphate complex content, it could be an important source of PSB biomass and Phosphorus in soils lacking in P, which is crucial for plant growth [26,27,39]. This study aimed to assess the inoculation effect of BSPs isolated from phosphate sludge and AMF in substrates based on sludge, with an increasing rate of sludge up to 60% mixed with peat; with increasing phosphate solid sludge rates, all of the parameters tested, including morphological traits, biomass, Chlorophyll a and b, and nutrient contents (N, P, K, and calcium), declined. The observed decline in these traits implies a compromised structural integrity and functionality, indicative of the detrimental effects exerted by increasing levels of phosphate solid sludge. This decline is not limited to external features alone; rather, it extends to the fundamental physiological processes that govern plant growth and development. Further, Phosphate solid sludge affects plant health and elemental composition, affecting nutrient uptake, assimilation, and overall balance. It reduces essential nutrients like N, P, K, and Ca, affecting plant nutrition and metabolic processes.
Phosphate sludge’s negative impacts on plant health are caused by ultrafine particles, which compact the substrate and impede root network and aerial plant growth. This causes soil water saturation concerns and an oxygen-deficient environment. In more severe cases, this condition can lead to a diminished availability of oxygen and poses a risk of asphyxiation. These incidents offer significant insights into the decline of plants in our study.
The ultrafine particles inherent in phosphate sludge play a pivotal role in substrate compaction. As these particles accumulate, they reduce soil porosity and increase soil density, creating a physical barrier that constrains the expansion of plant roots [40]. The intricate network of roots, crucial for nutrient absorption and water uptake, encounters impediments, leading to compromised plant vitality. Soil water saturation is a direct consequence of substrate compaction induced by ultrafine particles. As the soil becomes compacted, its ability to drain excess water diminishes, resulting in prolonged saturation [41]. This saturation exacerbates the challenges faced by plants by contributing to oxygen deficiency in the root zone. Oxygen is vital for various metabolic processes, and its scarcity impairs cellular respiration, ultimately impacting overall plant health. The elevated risk of asphyxiation is a noteworthy consequence of soil water saturation and oxygen deficiency. Plants, particularly their roots, require a well-aerated soil environment to function optimally. The compacted substrate, coupled with waterlogged conditions, hinders the diffusion of gases, leading to a reduced availability of oxygen [42]. This creates an environment where plant roots face challenges in obtaining the essential oxygen they need for cellular respiration and other energy-related processes.
Furthermore, the compaction-induced limitations extend beyond physical hindrances; they also affect the availability of essential soluble nutrients crucial for robust root development [43,44]. The compacted soil restricts the movement of water and nutrients, leading to an uneven distribution and decreased accessibility for plant roots. This restricted access to essential nutrients further exacerbates the stress imposed on plants by phosphate sludge, hindering their ability to establish strong and healthy root systems.
Upon conducting a thorough physico-chemical analysis, we unveiled a remarkably elevated calcium concentration in the phosphate solid sludge (11,200 mg/kg), twice the standard agricultural substrate rate. As elucidated by Burstrom [45], calcium plays a pivotal role in cell growth for both shoots and roots; however, an excess of calcium hinders overall plant growth. Furthermore, compelling evidence from various studies suggests that an abundance of calcium obstructs the mineralization of organic matter, thereby impeding the release of nitrogen from the soil [46,47]. This intricate web of interactions underscores the nuanced and far-reaching consequences of phosphate solid sludge on plant health, underscoring the imperative for a holistic comprehension of the underlying mechanisms at play.
The examination of diverse proportions of solid phosphate sludge on plant nutrient content, particularly emphasizing Nitrogen, Phosphorus, Potassium, and Calcium, reveals substantial variation among treatments. Notably, the incorporation of AMF emerges as the most effective treatment, showcasing superior performance in multiple nutrient categories. The remarkable effectiveness of the 10% AMF treatment suggests its potential in augmenting plant nutrient content comprehensively. Arbuscular mycorrhizal fungi are widely acknowledged for their pivotal role in facilitating the acquisition of essential nutrients, including Nitrogen, Phosphorus, Potassium, and other elements, through hyphal translocation [48]. In the context of faba bean colonization by Funneliformis mosseae, substantial enhancements in Phosphorus (P) and Potassium (K) accumulation in both shoot and overall plant biomass were observed compared to non-mycorrhizal controls [49]. This observation suggests that AMF contributes significantly to the plant’s uptake of P and K. Moreover, AMF’s reliance on host plant carbon (C) is well-established, with approximately 10–20% of recently photosynthesized C being allocated from host plants to support AMF growth. Concurrently, AMF plays a dual role by absorbing and transferring substantial amounts of N and P to the host plant. This intricate nutrient exchange mechanism orchestrated by AMF not only enhances plant growth but also improves nutrient absorption and water-use efficiency, underscoring the multifaceted contributions of AMF to plant–mycorrhizal symbioses [50].
Our findings reveal the superior efficiency of AMF over bacteria in augmenting nutrient uptake, especially for essential elements such as Phosphorus, Calcium, and Potassium. This heightened efficacy is attributed to the AMF’s capacity to extend hyphae into the soil, accessing nutrient sources that extend beyond the plant’s immediate reach. While bacteria undoubtedly play crucial roles in nutrient cycling and can contribute significantly to nutrient availability through various mechanisms, our data indicate a contrary trend in this specific study. This may be attributed to the specific bacterial strain utilized, potentially influencing nutrient interactions or microbial dynamics in a manner that contrasts with the typical bacterial contributions observed in nutrient cycling processes. Further investigations are warranted to explore the underlying factors contributing to this unexpected outcome, potentially shedding light on the intricate interplay between microbial communities and nutrient availability in the studied system.
This approach provides important insights into the complex interactions between solid phosphate sludge proportions and plant nutrition content. The prominence of the 10% AMF treatment not only emphasizes its efficacy but also acts as a focus point for understanding the complex dynamics of nutrient uptake. These discoveries not only contribute to our understanding of plant responses to various treatments but also serve as a foundation for future research. There is a pressing need for additional research to uncover the underlying mechanisms causing the reported impacts. Such thorough investigations will aid in the optimization of solid phosphate sludge treatments, opening the way for more sustainable and effective agricultural methods. This work opens up interesting opportunities for developing tactics that leverage the benefits of solid phosphate sludge in fostering. This study thus opens up promising avenues for refining strategies that harness the benefits of solid phosphate sludge in fostering robust plant growth and nutrient enrichment.

5. Conclusions

In conclusion, our study explored the potential of phosphorus-solubilizing microorganisms, specifically phosphorus-solubilizing bacteria (PSB) and arbuscular mycorrhizal fungi (AMF), to alleviate the detrimental impacts of phosphate solid sludge on plant growth. Physico-chemical analysis revealed the alkaline nature of the sludge, characterized by high phosphate limestone content but low organic matter. The study demonstrated a consistent decline in sorghum morphological traits, biomass, and photosynthetic pigments with increasing sludge concentrations, with AMF outperforming PSBs in enhancing plant growth.
An analysis of plant nutrient content highlighted significant differences among treatments, with the 10% AMF treatment consistently exhibiting superior performance. As sludge concentrations increased, nutrient absorption rates decreased. Mycorrhizal root colonization varied among treatments, with the 20% solid phosphate sludge treatment showing the highest AMF colonization.
Pearson correlation analysis underscored the negative impact of sludge concentrations on plant morphology, biomass, pigments, and nutrient uptake. Overall, the study concluded that phosphate sludge adversely affects plant health, primarily due to ultrafine particles causing substrate compaction, hindering root growth, and leading to soil water saturation and oxygen deficiency. The 10% AMF treatment emerged as the most effective in mitigating these adverse effects and increasing nutrient content. Further research is crucial to optimizing treatments for sustainable agricultural practices in the context of rising phosphate solid sludge levels.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/agronomy14020370/s1, Table S1: pH (water) and pH (KCl) of the mixtures, Table S2: Impact of solid phosphate sludge amended with bacteria or AMF on the absorption of mineral nutrients in sorghum shoots.

Author Contributions

Conceptualization, F.Z.A. and J.I.; Methodology and data analysis, F.Z.A., R.L. and E.A.B.; Writing—original draft, F.Z.A.; Review and Editing, R.L., L.N., E.A.B., J.I. and M.E.G.; Supervision, J.I. and L.N.; Project administration, E.A.B. and M.E.G. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Data Availability Statement

The data are contained within the article.

Acknowledgments

The Authors would like to acknowledge the support through the R&D Initiative—Call APPHOS—sponsored by OCP (OCP Foundation, R&D OCP, Mohammed VI Polytechnic University, National Center of Scientific and technical Research CNRST, Ministry of Higher Education, Scientific Research and Professional Training of Morocco MESRSFC) under the project entitled “Recycling solid phosphate sludge in fruit growing and forestry”, project ID-BIO-ELG 01/2017.

Conflicts of Interest

The authors declare no conflicts of interest.

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Agronomy 14 00370 g001
Figure 1. Experimental design showing a randomized complete block design with 5 replicates for each treatment; colors represent the different treatments.
Figure 1. Experimental design showing a randomized complete block design with 5 replicates for each treatment; colors represent the different treatments.
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Figure 2. Microscopic examination of the mycorrhization level in the root system. Roots were stained with Trypan blue. (A): Control; (B): Treatment 0%; (C): Treatment 10%; (D): Treatment 20%; (E): Treatment 40%; (F): Treatment 60%. Arrows indicate vesicles.
Figure 2. Microscopic examination of the mycorrhization level in the root system. Roots were stained with Trypan blue. (A): Control; (B): Treatment 0%; (C): Treatment 10%; (D): Treatment 20%; (E): Treatment 40%; (F): Treatment 60%. Arrows indicate vesicles.
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Agronomy 14 00370 g003
Figure 3. Heatmap presenting the correlation between all parameters studied in response to treatments (p < 0.05). Trt treatements; RDW Root dry wt; Chll.b chlorophyll b; PH Plant height; SDW Shoot dry wt; K potassium; N nitrogen; Ca Calcium; P phosphorus; Chll.a; Chlorophyll a.
Figure 3. Heatmap presenting the correlation between all parameters studied in response to treatments (p < 0.05). Trt treatements; RDW Root dry wt; Chll.b chlorophyll b; PH Plant height; SDW Shoot dry wt; K potassium; N nitrogen; Ca Calcium; P phosphorus; Chll.a; Chlorophyll a.
Agronomy 14 00370 g003
Table 1. Bacterial strains.
Table 1. Bacterial strains.
StrainIdentification
BM11Serratia rubidaea strain JCM1240
BM28Enterobacter bugandensis strain 247BMC
CB13Pantoea agglomerans strain ATCC 27155
BT125Pseudomonas brassicacearum subsp. Neoaurantiaca strain CIP109457
Table 2. Physico-chemical parameters of phosphate solid sludge and the mixtures.
Table 2. Physico-chemical parameters of phosphate solid sludge and the mixtures.
ParametersMeasured Values
Organic matter2.13%
Total Phosphate10.22%
Conductivity0.41 mmhos/cm
Ammonium (N-NH4)4.58 mg/kg
Nitrate (N-NO3)57.88 mg/kg
Chloride (Cl−)150 mg/kg
Sodium (Na2O)160.14 mg/kg
pH (Water 2/5)7.47
pH (KCl 2/5)7.21
Total limestone20.17%
Active limestone7.62%
Calcium (CaO)11200 mg/kg
Potassium (K2O)133.63 mg/kg
Magnesia (MgO)333.66 mg/kg
Copper (Cu)7.28 mg/kg
Manganese (Mn)3.83 mg/kg
Iron5.45 mg/kg
Zinc3.6 mg/kg
Sulfur25.84 mg/kg
Cation Exchange Capacity31.22 meq/100 g
Saturation rate136.61%
Table 3. Phosphate solid sludge effect on plant growth Chlorophyll a and b of Sorghum inoculated with PSB and AMF.
Table 3. Phosphate solid sludge effect on plant growth Chlorophyll a and b of Sorghum inoculated with PSB and AMF.
Proportions of Phosphate Sludge (%)StrainsPlant Height (cm)Shoot Dry wt/Plant (g)Root Dry wt/Plant (g)Chlorophyll a mg/gChlorophyll b mg/g
0Control63.8 ± 2.3 e8.7 ± 1.2 h22.5 ± 3.3 h23.4 ± 1.2 f6.7 ± 0.1 c
BM1176.5 ± 4.2 g10.2 ± 0.9 i31.7 ± 1.2 j39.4 ± 3.2 j11.9 ± 0.4 f
BM2889.0 ± 2.9 h10.4 ± 3.5 i26.9 ± 2.6 i27.8 ± 0.9 g19.3 ± 0.6 h
BT12581.5 ± 6.3 h10.8 ± 2.1 i36.9 ± 4.0 j34.5 ± 3.5 hi11.0 ± 0.8 f
CB1374.5 ± 2.3 g11.0 ± 0.8 i33.0 ± 2.8 j25.5 ± 2.8 fg7.8 ± 0.2 c
AMF120.8 ± 8.1 j28.3 ± 2.5 j34.9 ± 1.9 k39.5 ± 2.7 j12.3 ± 0.8 g
10Control55.5 ± 6.2 e2.6 ± 0.8 e13.1 ± 1.3 f22.6 ± 1.5 f6.3 ± 0.8 c
BM1168.3 ± 2.3 f5.5 ± 1.0 g29.5 ± 2.3 ij33.9 ± 3.7 h8.3 ± 0.0 e
BM2870.8 ± 8.0 g8.1 ± 0.6 h17.2 ± 0.9 g37.7 ± 0.8 i12.3 ± 1.7 g
BT12576.3 ± 5.6 g4.7 ± 1.1 f17.2 ± 1.5 g31.2 ± 2.9 h8.5 ± 0.2 e
CB1365.5 ± 7.3 f5.0 ± 0.9 f16.8 ± 2.3 g39.3 ± 0.6 j11.7 ± 0.5 fg
AMF126.8 ± 9.4 j26.2 ± 3.2 j25.7 ± 2.7 i51.7 ± 4.1 k18.1 ± 1.6 h
20Control38.5 ± 2.8 d1.3 ± 0.0 d10.4 ± 2.0 e19.0 ± 0.2 d3.37 ± 0.5 b
BM1141.6 ± 5.6 d0.6 ± 0.1 c14.3 ± 0.9 f24.9 ± 0.3 f9.5 ± 0.9 e
BM2843.0 ± 5.7 d1.6 ± 0.5 d12.3 ± 0.2 e21.8 ± 1.3 e6.8 ± 0.2 c
BT12556.3 ± 5.5 e2.3 ± 0.3 e14.0 ± 1.3 f28.4 ± 3.0 g8.2 ± 1.0 e
CB1351.0 ± 2.5 e1.6 ± 0.1 d14.3 ± 2.4 f26.5 ± 2.7 g7.2 ± 0.4 c
AMF103.3 ± 10.5 i10.7 ± 2.1 i18.8 ± 2.6 g36.8 ± 0.3 i11.1 ± 0.8 f
40Control19.4 ± 2.8 b0.2 ± 0.0 b0.4 ± 0.01 b13.2 ± 0.2 c5.9 ± 0.1 c
BM1122.6 ± 5.3 b0.3 ± 0.0 b0.3 ± 0.04 b20.8 ± 0.0 d4.8 ± 0.3 b
BM2820.8 ± 5.1 b0.6 ± 0.0 c0.2 ± 0.01 b18.9 ± 0.5 d6.3 ± 1.0 c
BT12527.0 ± 3.4 c0.2 ± 0.0 b0.7 ± 0.01 c18.5 ± 0.7 d6.4 ± 0.7 c
CB1322.5 ± 2.7 b0.3 ± 0.0 b0.8 ± 0.12 c21.6 ± 3.1 e4.7 ± 0.2 b
AMF78.3 ± 8.2 g5.8 ± 0.2 g15.8 ± 4.5 e38.1 ± 3.8 j16.6 ± 0.8 h
60Control14.7 ± 0.9 a0.1 ± 0.0 a0.8 ± 0.02 c6.2 ± 0.5 a2.0 ± 0.2 a
BM1119.8 ± 4.8 b0.2 ± 0.0 b0.3 ± 0.04 b10.0 ± 0.8 c3.1 ± 0.2 a
BM2823.4 ± 4.0 b0.2 ± 0.0 b0.1 ± 0.05 a10.4 ± 0.3 c4.5 ± 0.6 b
BT12516.3 ± 2.4 a0.1 ± 0.0 a0.2 ± 0.02 b8.7 ± 0.1 b2.8 ± 0.1 a
CB1320.8 ± 4.0 b0.1 ± 0.0 a0.6 ± 0.03 c19.0 ± 0.2 d5.7 ± 0.4 c
AMF36.0 ± 3.9 d1.0 ± 0.1 d1.2 ± 0.4 d27.6 ± 2.7 g8.4 ± 0.9 e
Values represent the means of five replicates ± SD. Different letters among treatments group indicate statistically significant differences (Duncan’s test), (p < 0.05).
Table 4. Effect of AMF and phosphates solid sludge on percentage of root colonization.
Table 4. Effect of AMF and phosphates solid sludge on percentage of root colonization.
Treatments (%)Root Colonization (%)
050 a
1069 c
2079 d
4072 e
6060 b
Values are means of three replicates. Different letters among treatments group indicate statistically significant differences (Duncan’s test), (p < 0.05).
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Aliyat, F.Z.; El Guilli, M.; Nassiri, L.; Lahlali, R.; Barka, E.A.; Ibijbijen, J. Elevating Sorghum Prosperity: Unveiling Growth Trends through Phosphate-Solubilizing Bacteria and Arbuscular Mycorrhizal Fungi Inoculation in Phosphate-Enriched Substrates. Agronomy 2024, 14, 370. https://doi.org/10.3390/agronomy14020370

AMA Style

Aliyat FZ, El Guilli M, Nassiri L, Lahlali R, Barka EA, Ibijbijen J. Elevating Sorghum Prosperity: Unveiling Growth Trends through Phosphate-Solubilizing Bacteria and Arbuscular Mycorrhizal Fungi Inoculation in Phosphate-Enriched Substrates. Agronomy. 2024; 14(2):370. https://doi.org/10.3390/agronomy14020370

Chicago/Turabian Style

Aliyat, Fatima Zahra, Mohammed El Guilli, Laila Nassiri, Rachid Lahlali, Essaid Ait Barka, and Jamal Ibijbijen. 2024. "Elevating Sorghum Prosperity: Unveiling Growth Trends through Phosphate-Solubilizing Bacteria and Arbuscular Mycorrhizal Fungi Inoculation in Phosphate-Enriched Substrates" Agronomy 14, no. 2: 370. https://doi.org/10.3390/agronomy14020370

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