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Article

Influence of Organomineral Fertiliser from Sewage Sludge on Soil Microbiome and Physiological Parameters of Maize (Zea mays L.)

by
Małgorzata Hawrot-Paw
1,*,
Małgorzata Mikiciuk
2,
Adam Koniuszy
1 and
Edward Meller
3
1
Department of Renewable Energy Engineering, West Pomeranian University of Technology, Pawla VI 1, 71-459 Szczecin, Poland
2
Department of Bioengineering, West Pomeranian University of Technology, Slowackiego 17, 71-434 Szczecin, Poland
3
Department of Environmental Management, Faculty of Environmental Management and Agriculture, West Pomeranian University of Technology, Slowackiego 17, 71-434 Szczecin, Poland
*
Author to whom correspondence should be addressed.
Agronomy 2022, 12(5), 1114; https://doi.org/10.3390/agronomy12051114
Submission received: 31 March 2022 / Revised: 28 April 2022 / Accepted: 1 May 2022 / Published: 4 May 2022
(This article belongs to the Special Issue A Circular Economy: Chemical, Microbiological and Environmental Implications of Mineral and Organic Fertilizers Use in Soils)
Browse Figures
Versions Notes

Abstract

:
The use of a soil fertiliser results in high, good quality yields. The most widely used fertilisers are mineral or organic, but there is increasing attention on organomineral fertilisers produced from sewage sludge. These contain beneficial components which may improve soil fertility and thus plant productivity, but there are some concerns associated with their application due to their composition. Using a short-term pot experiment the effect of such a soil conditioner called FS, produced from sewage sludge after stabilisation with lime, on the qualitative−quantitative composition and activity of soil microorganisms and selected physiological parameters of the maize was analysed. The study was carried out in a completely randomised design, including a control (soil + lime + NPK). The application of the FS had a positive effect on the soil pH, equivalent to the application of lime. Organomineral fertiliser, as a source of organic carbon and macroelements, had a positive effect on the number of soil microorganisms and their activity, and this influence was stable during maize vegetation. FS did not influence the gas exchange activity of maize, the content of assimilation pigments in leaves or and the efficiency of the photosynthetic apparatus determined by chlorophyll “a” fluorescence analysis, but it increased the light absorption efficiency of the PSII photosystem. Differences in biomass yield from organomineral and mineral fertilisation were statistically insignificant.

1. Introduction

Soil fertility, or the ability to supply plant nutrients, depends on the availability of nutrients, soil organic matter, soil pH and moisture [1]. It can be improved by appropriate fertilisation, mineral [2] or organic [3]. Due to the high cost of mineral fertilisers, there is a growing interest in alternative solutions. Positive effects, including increase in soil organic matter and major plant nutrients, can be obtained by using sewage sludge (SS) as fertiliser [4,5]. However, there are some concerns about its use in agriculture, mainly in relation to the possible heavy metal content [6,7], pathogens [8] and antibiotic residues [9].
Sewage sludge and the fertilisers produced from it contain organic and inorganic compounds valuable to plants [10], and their use can promote both sustainable crop production and also contribute to nutrient recycling [11]. For sanitary reasons, sewage sludge requires stabilisation. Different treatments are used in this process, including biological methods such as anaerobic digestion [12] and composting [13], thermal methods [14] and chemical methods with alkaline stabilisation [15]. When sewage sludge is stabilised with calcium oxide (CaO), its pH is significantly increased and it can then be used to fertilise acidic soils.
Soil pH is important not only for plant growth, but also for soil microorganisms. In addition, it determines the availability of carbon and nutrients and the solubility of metals, which directly affects the structure of the soil microbiome [16]. Microorganisms are an integral part of the soil and their activity affects its proper functioning [17] and provides potential for high yields and appropriate crop quality [18]. Changes in the qualitative and quantitative composition of microbiocenoses determine biodiversity and the direction of many biological processes [19]. Soil microorganisms play a significant role in the decomposition of organic matter and in the cycling of elements. Microorganisms are responsible for the production of polymeric substances that retain soil structure [20]. The activity of some groups of microorganisms promotes atmospheric nitrogen fixation [21], and there are soil microorganisms capable of sequestering carbon dioxide [22]. They are very sensitive indicators of any adverse changes in soil and are used in ecotoxicological analysis of the soil environment [23], so they also can be an indicator of biological imbalance associated with sludge application into the soil.
A significant factor for soil fertility is also plants [24]. Their physiological states, influenced by the conditions of their growth, such as soil properties including soil fertility, are well described by gas exchange parameters. They include, for example, the intensity of CO2 assimilation and transpiration. The productivity and efficiency of the photosynthetic apparatus are also important. These are parameters that determine the productivity and the yield of crops. Some of the most insightful methods for evaluating light phases of photosynthesis are those based on measuring the fluorescence of chlorophyll ‘a’. They are highly sensitive, non-invasive and rapid. According to many authors, analysis of fluorescence allows the determination of both functioning and certain structural attributes of the photosynthetic apparatus of plants [25,26].
Available studies on sewage sludge as a fertiliser mainly report plant yields and physical and chemical soil properties, including heavy metal content. Much less is known about the relationship between SS application and soil microbiota. Most studies analyse the amount of pathogens introduced into the soil with sewage sludge or the proliferation of antibiotic resistance among soil microorganisms. The aim of this study was to evaluate the influence of the application of organomineral fertiliser on the structure of soil microorganisms of the main taxonomic and functional groups and on their activity, as well as evaluation of selected physiological parameters of maize cultivated with this fertiliser. It was hypothesised that FS added to soil could affect its biological properties by modifying the qualitative−quantitative composition of the microbiome and its activity, as well as the physiological characteristics of plants that determine their productivity.

2. Materials and Methods

2.1. Characteristics of Soil Conditioner

Organomineral fertiliser is produced from stabilised municipal sewage sludge and lime in an agglomeration and hygienisation system. Selected parameters of the sewage sludge are presented in Table 1. In Poland, FS has been registered as a soil conditioner. FS contains significant amounts of phosphorus, nitrogen and magnesium so it can improve soil fertility.

2.2. Soil Characteristic

Soil was collected from the A horizon (0–15 cm) at the Agricultural Experimental Station of the West Pomeranian University of Technology in Szczecin, Lipnik, near Stargard, Poland (53°20′ N, 14°58′ E). This was an acid soil with a pH of 4.23 (in KCl). The C and N contents of the soil were 10 g·kg−1 and 1.1 g·kg−1 of soil dry mass (DM), respectively. The soil on which the experiment was set up was classified as clay sand (79.7% sand, 18.9% silt and 1.4% clay). The samples were air-dried and sieved through a 2 mm mesh sieve. The actual soil moisture was determined by gravimetric method using a moisture analyser (AXIS ATS60, Gdansk, Poland) and adjusted to 50% of water-holding capacity (WHC).

2.3. Experimental Set-Up

The studies were conducted in 15 litre PVC pots, which were filled with 8 kg of soil. Two treatments were applied to the soil: C (control) and FS (soil with organomineral fertiliser). FS was introduced to the soil in a dose of 75 g + 2.6 g N. The control object (C) was soil treated with a liming process using CaO at a dose equivalent to that declared by the FS producer with the addition of 2.6 g N as ammonium nitrate, 0.2 g P2O5 as triple superphosphate, 0.5 g K2O as potassium sulphate, and 0.5 g MgO as magnesium sulphate. Additional fertilisation during the growing season was applied—1.5 g N in both treatments in divided doses of 0.5 g. In the control (C) the total dose of applied elements was 0.51 g N·kg−1, phosphorus 0.011 g P·kg−1 and potassium 0.052 g K·kg−1. Fertilisers were distributed over the surface and mixed homogeneously into the soil. The study was carried out in a completely randomised design in four replications for each treatment. The test plant was maize (Zea mays L.) var. Polan. Five maize seeds were sown into each pot and after germination the number was reduced to three plants per pot. Soil moisture contents were measured and maintained to constant weight by adding an appropriate amount of distilled water.
During the study, the qualitative−quantitative composition of the microbiota, microbial activity and selected physiological parameters of the plant were analysed. The material for microbiological analyses was collected with a stainless steel soil probe sampler. Samples were taken from the rhizosphere zone of the maize in triplicate from each pot. After thorough mixing, collective samples were made. At the end of the study, the dry mass yield was determined by gravimetric method. Moreover, the content of N, P and K was determined in soil and aerial parts of the plant.

2.4. Microbial Analysis

As part of microbiological analyses, the number of selected groups of soil microorganisms was evaluated. These analyses of number were carried out after plating the soil dilutions on the appropriate culture medium: bacteria on the soil extract medium according to Bunt and Rovira [28] at 25 °C after 3 days of incubation, actinobacteria on the medium according to Cyganov and Žukov [29] at 25 °C after 7 days, fungi on the agar medium according to Martin [30] at 25 °C after 5 days, proteolytic microorganisms on milk medium by Kędzia and Konar [31] at 25 °C after 3 days, amylolytic microorganisms on starch medium by Cooney and Emerson [32] at 25 °C after 3 days, lipolytic microorganisms on tributyrin medium by Burbianka and Pliszka [33] at 25 °C after 3 days, cellulolytic microorganisms on Maliszewska medium [34] at 25 °C after 7 days, Azotobacter on Fenglerowa medium [35] at 25 °C after 7 days, Rhizobium on mannitol medium at 25 °C after 7 days, Bacillus on LB medium at 37 °C after 3 days, copiotrophs on NB (nutrient broth) after 7 days of incubation at 28 °C [36], oligotrophs on DNB (dilution nutrient broth) after 14 days of incubation at 28 °C [36] and Pseudomonas fluorescens on King B medium at 26 °C after 3 days of incubation. All determinations were carried out in triplicate. The results were calculated per 1 g of soil dry matter and presented as colony-forming units (CFU). Additionally, by equating the number of bacteria and actinobacteria to the number of fungi, the so-called SR fertility index was calculated [37].
The activity of soil microorganisms was determined according to the PN-EN ISO 16,072:2011 standard [38]. The measurements were carried out in fresh soil. Soil samples were placed in test tubes, which were introduced into conical flasks containing 0.05 mol·L−1 NaOH solution which absorbed the CO2 produced by the soil microorganisms. After 24 h of incubation, 0.5 mol·L−1 BaCl2 solution was added to the NaOH solution and the mixture was titrated with 0.1 mol·L−1 HCl solution using phenolphthalein as an indicator. The rate of CO2 production was converted per unit of dry mass soil (mg CO2·g−1·h−1). The results of microbial activity are presented as a percentage in relation to the control.
Microbiological analyses were carried out before sowing maize (1st measurement date), then at flowering stage (2nd measurement date) and finally at cob formation stage (3rd measurement date).

2.5. Plant Analysis

2.5.1. Gas-Exchange Parameters of Plants

The parameters of gas exchange of plants (CO2 assimilation intensity—A, transpiration—E, stomatal conductance for water—gs, and CO2 concentration in chlorenchyma intercellular spaces—c) were measured during the flowering stage of maize, on the third pair of leaves from the bottom of the plant, with a TPS-2 (PP Systems) portable gas analyser (with standard settings) equipped with a PLC4 measuring chamber operating in an open system. The measurements were performed on healthy, fully grown leaves. On the basis of the results of CO2 assimilation intensity and transpiration, the photosynthetic water-use efficiency (ωW) was calculated by the ratio of assimilation intensity to transpiration [39].

2.5.2. Concentrations of Assimilation Pigments in Leaves

The amounts of chlorophylls “a” and “b” and total chlorophyll in leaves were determined by the method of Arnon et al. [40] modified by Lichtenthaler and Wellburn [41], while the concentrations of carotenoids in leaves by the method of Hager and Mayer-Berthenrath [42]. The concentration of chlorophyll and carotenoids was determined on the same leaves on which gas exchange measurements were made. Extracts of the pigments were obtained by grinding samples of fresh leaf mass, about 0.05 g, in a mortar with 10 cm3 of 80% acetone. The homogenates were then centrifuged at 1500 rpm for 10 min. The absorbance of extracts was determined using a Shimadzu UV-1280 spectrophotometer at wavelengths 440, 645 and 663 nm.

2.5.3. Chlorophyll Fluorescence Parameters

Chlorophyll fluorescence parameters were recorded using a Handy PEA (Handy Plant Efficiency Analyzer) spectrofluorometer (Hansatech Instruments Ltd., King’s Lynn, Norfolk, GB) based on the standard apparatus procedure (3 × 650 nm LEDs, maximum actinic light intensity 3500 μmol·m−2·s−1). The measurements were made on the same test date and the same leaves on which the other physiological characteristics were determined. Leaves were shaded 20 min before measurement with factory clips (illuminated area with a diameter of 4 mm). Values of fluorescence were registered between 10 μs and 1 s after the activation of the excitation light pulse. The following parameters of chlorophyll fluorescence induction were measured and calculated using the spectrofluorometer: F0—initial fluorescence (zero), excitation energy loss index in power antennas [43]; FM—maximum fluorescence, after reduction of acceptors in PS II and after dark adaptation; FV = FM − F0—variable fluorescence, determined after dark adaptation, a parameter dependent on the maximum quantum yield of PS II [44]; FV/FM—the maximum potential photochemical reaction efficiency in PS II determined after dark adaptation and after reduction of acceptors in PS II [45], PI—PS II vitality index for the overall viability of this system, area—surface area above the chlorophyll fluorescence curve and between F0 and FM points proportional to the size of the reduced plastoquinone acceptors in PS II, TFM—time of chlorophyll fluorescence growth from the beginning of measurement to the maximal value.

2.6. Chemical Analysis

The total nitrogen (N) content of the soil and plant material was determined using an elemental analyser (Costech Elementary Analyzer ECS 4010, Italy) and the total potassium (K) and phosphorus (P) contents after previous mineralization of the materials in a mixture of concentrated acids HNO3 and HClO4 at a ratio of 1:1 [46]. Potassium content was determined using flame atomic emission spectrometry (ICE 3000 series spectrometer) and phosphorus content by molybdenum blue spectrophotometry (Marcel MEDIA™ spectrophotometer).

2.7. Statistical Analysis

Results were analysed using the analysis of variance followed by post-hoc tests by Tukey at a significance level of p < 0.05. All the statistical analyses were carried out using a statistical software package for Windows (Dell Statistica (data analysis software system) version 13.3 (2016); Dell Inc., Tulsa, OK, USA). The standard deviation (SD) was also determined.

3. Results

3.1. Soil Microbiome

Fertilisation influences the soil microbiome, as confirmed by the presented studies, and the effect depends on the sensitivity of specific microbial groups and the type of cultivated crop [47].
Introduction of organomineral fertiliser into the soil increased the number of all major taxonomic groups of soil microorganisms (Figure 1a–c). The increase of aerobic microorganisms after application of sewage sludge after biological stabilisation from 4.48 million CFU in control soil to 8.25 million CFU per gram in SS-fertilised soil was also reported by Farsang et al. [48]. Significant differences were mostly observed at the flowering stage of the plants and at the cob production stage. A significantly high increase (4.77 × 107 CFU g−1 DM soil), almost 800 percent in relation to the control, was observed on the second measurement date for bacteria. These microorganisms secrete extracellular polymeric substances (EPS) that increase their water-holding potential [49,50] and therefore their presence is important for this environment. Ondreičková et al. [51] carried out an analysis of bacterial communities in the rhizosphere of Arundo donax and reported that total microbial biomass was statistically higher in the soil with additives derived from sewage sludge and agricultural by-products than in control samples. Bacteria and other microorganisms involved in the decomposition of organic matter provide an elemental cycle [52]. A reduction in the numbers of actinobacteria would result in a reduction in the rate of mineralisation of difficult-to-decompose compounds such as lignin. Amounts of actinobacteria during maize vegetation after application of organomineral fertilisation were significantly higher compared to the control object, 5.32 × 104 CFU and 8.40 × 104 CFU g−1 DM soil in the soil of the FS object (flowering phase), respectively, and 3.29 × 104 CFU and 5.69 × 104 CFU g−1 DM soil in the soil with mineral fertilisation (cob formation phase). Different results were observed by Francioli et al. [53], in which numbers of actinobacteria were significantly higher in NPK-fertilised soil than in organically fertilised soils. Some studies indicate that actinobacteria are more active in soils with higher pH [54], so the positive effect of FS application into the soil could be due to the increase in soil pH. Different results in regard to correlation between soil pH and actinobacteria community were obtained by Khafipour et al. [55]. A reduction in the number of actinobacteria, due to their high degradation activity [56], could have a negative impact on the rate and level of organic matter mineralization. During the study, regardless of the fertiliser type, the number of fungi changed significantly, from 1.99 × 104 CFU to 4.15 × 104 CFU g−1 DM soil in the C soil and from 2.15 × 104 CFU to 1.10 × 105 CFU g−1 DM soil in the FS object at the second measurement date. At the end of the study, differences in numbers were not significant. This is confirmed by the study carried out by Marschner et al. [57], in which even long-term application of sewage sludge had a low effect on eucaryotic organisms.
According to Myśkow et al. [58] the use of mineral fertilisation results in strong acidification of soils, increases growth of fungi and affects the fertility index value SR. Soils with higher values of this coefficient have more beneficial microbiological properties [59]. The application of FS increased the soil pH to 7.51. At the end of the experiment, the pH value in the FS treatment decreased to 7.03. This could be one of the more important factors increasing the SR value in the soil with organomineral fertilisation (Figure 1d).
The effect of fertilisation on the numbers of major metabolic groups of soil microflora is shown in Figure 2a–d. Only at the first measurement date was the number of lipolytic microorganisms in the FS object lower compared to the C object. At the maize flowering stage, the number of these microorganisms increased to 1.30 × 106 CFU g−1 DM soil and was higher compared to the number in the control soil. Significant differences for organomineral fertilisation were also observed at the next measurement date. In the presented study, the number of amylolytic organisms was significantly increased—up to 6.96 × 105 CFU g−1 DM soil at the end of the study experiment. After introduction of FS into the soil, the number of proteolytic microorganisms also increased. This is a positive change, because a reduction in the quantity of these microorganisms could have a negative effect on the mineralisation of organic nitrogen compounds in the soil. The beneficial effect of sewage sludge on the number and activity of proteolytic microorganisms was also confirmed by Wolna-Maruwka et al. [60]. Enzymes secreted by cellulolytic microorganisms are involved in the breakdown of cellulose, which is the main component of plant biomass. Their presence is important for the carbon cycle [61] and although the number of these microorganisms changed during the experiment, it was always higher compared to the control object.
The atmospheric nitrogen-fixing microorganisms present in the soil are represented mainly by the genera Azotobacter and Rhizobium, i.e., free-living bacteria living in symbiosis with plants. Azotobacter are generally not very numerous in the soil, which is also confirmed by the results presented in this study (Figure 3a), whereas their number increased under FS application. However, the differences between the control soil and the soil with organomineral fertilisation were not significant. Similar results were obtained for Rhizobium (Figure 3b). These bacteria are sensitive to environmental stress caused, among others, by soil pH, nutrient deprivation and the presence of heavy metals [62], but in the presence of FS such negative reactions were not observed. Rhizobia belong to plant-growth-promoting bacteria (PGPB), and their positive effects on maize have been confirmed by studies carried out by Pérez-Pérez et al. [63] and Cavalcanti et al. [64].
The availability of organic carbon in the soil affects the copiotrophic and oligotrophic microorganism population [65], and sewage sludge has a high organic matter content [66]. This was also confirmed by the obtained results (Figure 4a). Significant differences in copiotrophic number in relation to the control were observed during maize flowering (max 1.71 × 107 CFU g−1 DM soil), and for oligotrophic microorganisms also during the cob production phase. The decrease in the number of copiotrophic microorganisms at the end of maize vegetation could be related to the utilization of compounds introduced with organomineral fertiliser. The soil was then dominated by oligotrophic organisms, which provide a stable level of organic matter in the soil. Similar results after fertilisation with sewage sludge were reported by Wolna-Maruwka et al. [67].
Pseudomonas fluorescens produces a volatile organic compound that inhibits the growth and development of fungal plant pathogens [68,69], therefore its presence in the soil is very important. In the soil after application of organomineral fertiliser, the number of these bacteria slightly increased at the flowering stage and decreased at the last measurement date, but at both measurement dates these changes were not significantly different from the results obtained in the control soil (Figure 5).
Bacteria belonging to the Bacillus genus, such as Pseudomonas, which exists in the rhizosphere, are a biological control agent important in the growth inhibition of many fungal plant pathogens [70,71]. In the present study, it was found that the numbers of Bacillus were higher in the objects fertilised with FS compared to the control object (Figure 5b). Bacteria of this genus are not only important for plant health, but also play an important role in stimulating plant growth, which, among others, for maize was confirmed by a study carried out by Akinrinlola et al. [72].
Organomineral fertilisation had a positive effect on the microbial respiration activity (Figure 6). Higher activity was observed at all measurement dates, and significant differences were noted at the maize flowering phase and after cob formation. Increases in microbial activity and biomass after sewage sludge application were also reported by other authors [73,74]. In a study carried out by Fernandes et al. [75] the respiratory activity of microorganisms was positively correlated with the doses of sewage sludge introduced into the soil.

3.2. Plants

Many authors [76,77] reported that the application of sewage sludge has a positive effect on plant biomass, including maize [78]. In the present study, the yield of aboveground parts of maize was a total of 173.1 g, averaging 43.28 ± 3.64 g per pot after organomineral fertilisation and 157.93 g in the control treatment, averaging 39.48 ± 3.29 g per pot. Similar results after application of maize fertiliser with sewage sludge in a three-year experiment were reported by Gondek [79]. In the presented study, the yield was almost 9% lower after FS application, while Zalewska et al. [80] recorded a five-fold increase in maize biomass after application of sewage sludge. In a study carried out by Najera et al. [81], soil pH had a significant effect on maize yield. In the presented study, the pH of the control soil (7.19) was only slightly higher compared to the soil fertilised with FS (7.03).
No differences were found between the content of nitrogen and potassium in the soil with FS and in the control soil. For plants, significant differences were noted for N and P (Table 2). The slightly lower content of nitrogen, phosphorus and potassium in the fertilised soil (FS) compared to the control (C) may have been due to the different amounts of these nutrients introduced with FS and NPK fertilisation in the control treatment.
The effects of soil fertilisation on the physiological parameters of maize are presented in Table 3 and Table 4. The intensity of gas exchange in plants is one of the most important physiological properties determining their productivity. Maintaining high photosynthetic activity of leaves, especially under stress conditions, is a fundamental factor in plant yield. One of the factors influencing the intensity of plant gas exchange is the availability of nutrients, which is largely influenced by soil pH. The plants growing in soil fertilised with FS and the control plants had similar values of all determined gas exchange parameters. For the intensity of CO2 assimilation, transpiration, CO2 concentration in chlorenchyma inter-cellular spaces and stomatal conductance for water, slightly higher values were observed in plants fertilised with FS, however, differences were not statistically significant. Moreover, no differences were found between plants in photosynthetic water-use efficiency, as indicated by the values of the ωW index. Fertilisation did not affect the content of chlorophylls “a” or “b”, total chlorophyll or carotenoids in maize leaves. There were also no differences between the treatments for the ratio of chlorophyll “a”/chlorophyll “b” (Table 2). No effect of soil application of sewage sludge at different doses on chlorophyll content was also reported by Zielonka et al. [82] for Cannabis sativa L. and by Zabotto et al. [83] for Eucalyptus urograndis. However, after application of sewage sludge, Zabotto et al. observed an increase in carotenoid content in leaves.
There were no significant differences in most parameters characterizing photosynthetic activity and assimilation pigments between organomineral-fertilised and control plants despite significant differences in nitrogen and phosphorus content, in plants (Table 3). These elements, as well as potassium, are important for photosynthesis. Much of the cellular nitrogen is involved in the photosynthetic apparatus: major integral protein complexes, including the PSI and PSII systems and cytochrome, and smaller surface proteins e.g., ferredoxine and plastocyanine [84]. Phosphorus is responsible for photosynthetic phosphorylation and ATP production. Its availability in plants also affects the intensity of photosynthesis through changes in chlorophyll content and chloroplast structure [85]. Potassium, although it does not form organic compounds in plants, has a beneficial effect on photoreduction and photophosphorylation reactions. Increased content of potassium ions is correlated with more intensive CO2 assimilation [86].
The efficiency of the photosynthetic apparatus in maize was evaluated by measuring the fluorescence of chlorophyll “a”, since research methods using this phenomenon are among the most sensitive, allowing for the analysis of plant responses to external factors [87,88]. No differences were found between plants growing in soil fertilised with FS and control treatment with regard to the values of parameters such as F0, FM, area, TFM and PI (Table 4). According to these results, it can be concluded that the application of FS did not induce stress in the plants and no significant changes in their photosynthetic apparatus were observed. The F0 index shows similar efficiency of excitation energy transfer between chlorophyll molecules in plants growing in soil with FS addition as in control [89]. The values of TFM, i.e., time of fluorescence increase from the beginning of the measurement to the maximum of FM, for plants growing in soil fertilised with FS as well as in the control, according to Lichtenthaler et. al. [90], were in the range of the most frequently reported values (500–800 ms). The value of the area parameter is proportional to the size of the PS II electron acceptor pool and in case of blocking their transport from reaction centres to plastoquinons (e.g., during stress) it may decrease [91]. This index also informs about the number of available acceptors in PSII [44]. In maize leaves growing in soil with organomineral fertiliser, an increase in light absorption efficiency of photosystem PSII was observed, as showed by higher FV/FM values (Table 4). This index for plants growing in soil with FS as well as in the control treatment was lower than those for plants under non-stressed conditions (0.83) [92]. However, according to Bjorkman and Demmig [93] the FV/FM values were characteristic for plants under physiological conditions. These authors reported that the FV/FM ratio ranges from 0.78 to 0.84.

4. Conclusions

Changes in soil microbiome structure affect soil quality and productivity. Microorganisms are an important indicator of changes in the soil environment and are much more sensitive than chemical analytical methods. Using microbiological analysis to determine the biological effects related to organomineral fertiliser application into the soil provides an opportunity to assess possible negative reactions due to the composition of such fertilisers made from sewage sludge. It was found that the application of FS fertiliser as a source of organic carbon and elements, had a positive effect on soil microorganisms, and this effect was maintained during the maize vegetation period. The activity of microorganisms in soil fertilised with the organomineral product was higher than the control, in the range from 8 to 43%. Introduction of organomineral fertiliser had the beneficial effect of increasing the efficiency of light absorption by the maize photosystem PSII and did not affect other physiological parameters. The yield of maize aerial biomass after organomineral fertilisation was lower by less than 9% compared to mineral fertilisation, but the difference was statistically insignificant. The fertiliser produced in the chemical stabilization process with lime can be applied to acidic soils for pH increase.

Author Contributions

Conceptualization, M.H.-P.; methodology, M.H.-P., M.M. and E.M.; validation, M.H.-P. and M.M.; formal analysis, M.H.-P., M.M. and E.M.; investigation, M.H.-P., M.M., A.K. and E.M.; data curation, M.H.-P. and M.M.; writing—original draft preparation, M.H.-P. and M.M.; writing—review and editing, M.H.-P. and M.M.; visualization, M.H.-P. and M.M. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

The data presented in this study are available on request from the corresponding author.

Conflicts of Interest

The authors declare no conflict of interest.

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Agronomy 12 01114 g001 550
Figure 1. The number of basic taxonomic groups of soil microorganisms and the soil fertility coefficient: (a) bacteria, (b) actinobacteria, (c) fungi and (d) fertility coefficient. Different letters above the error bars (i.e., ± SD) indicate significant differences (p < 0.05) between means (Tukey post-hoc test).
Figure 1. The number of basic taxonomic groups of soil microorganisms and the soil fertility coefficient: (a) bacteria, (b) actinobacteria, (c) fungi and (d) fertility coefficient. Different letters above the error bars (i.e., ± SD) indicate significant differences (p < 0.05) between means (Tukey post-hoc test).
Agronomy 12 01114 g001
Agronomy 12 01114 g002 550
Figure 2. The number of selected metabolic groups of soil microorganisms: (a) lipolytic, (b) amylolytic, (c) proteolytic and (d) cellulolytic microorganisms. Different letters above the error bars (i.e., ± SD) indicate significant differences (p < 0.05) between means (Tukey post-hoc test).
Figure 2. The number of selected metabolic groups of soil microorganisms: (a) lipolytic, (b) amylolytic, (c) proteolytic and (d) cellulolytic microorganisms. Different letters above the error bars (i.e., ± SD) indicate significant differences (p < 0.05) between means (Tukey post-hoc test).
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Agronomy 12 01114 g003 550
Figure 3. The number of (a) Azotobacter and (b) Rhizobium in soil after fertilisation. Different letters above the error bars (i.e., ± SD) indicate significant differences (p < 0.05) between means (Tukey post-hoc test).
Figure 3. The number of (a) Azotobacter and (b) Rhizobium in soil after fertilisation. Different letters above the error bars (i.e., ± SD) indicate significant differences (p < 0.05) between means (Tukey post-hoc test).
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Figure 4. The number of (a) copiotrophic and (b) oligotrophic microorganisms in soil after fertilisation. Different letters above the error bars (i.e., ± SD) indicate significant differences (p < 0.05) between means (Tukey post-hoc test).
Figure 4. The number of (a) copiotrophic and (b) oligotrophic microorganisms in soil after fertilisation. Different letters above the error bars (i.e., ± SD) indicate significant differences (p < 0.05) between means (Tukey post-hoc test).
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Figure 5. The number of (a) Pseudomonas fluorescens and (b) Bacillus in soil after fertilisation. Different letters above the error bars (i.e., ± SD) indicate significant differences (p < 0.05) between means (Tukey post-hoc test).
Figure 5. The number of (a) Pseudomonas fluorescens and (b) Bacillus in soil after fertilisation. Different letters above the error bars (i.e., ± SD) indicate significant differences (p < 0.05) between means (Tukey post-hoc test).
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Figure 6. Microbial respiration in soil after fertilisation. Different letters above the error bars (i.e., ± SD) indicate significant differences (p < 0.05) between means (Tukey post-hoc test).
Figure 6. Microbial respiration in soil after fertilisation. Different letters above the error bars (i.e., ± SD) indicate significant differences (p < 0.05) between means (Tukey post-hoc test).
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Table
Table 1. The parameters of sewage sludge [27].
Table 1. The parameters of sewage sludge [27].
ParameterUnitSewage Sludge after Hygienisation
and Agglomeration
pH-12.5
Organic matter%high
Total N%2.43
Ca%41.90
Mg%0.49
Total P%0.30
Pbmg/kg30
Crmg/kg20
Cumg/kg32
Nimg/kg33
Cdmg/kg2.70
Znmg/kg108.00
Hgmg/kg0.08
Pathogenic bacteria Salmonellapresence of bacteria/100 gnot isolated
Viable parasite eggsamount/kgnot found
Table
Table 2. Elements in soil and plants.
Table 2. Elements in soil and plants.
TreatmentsContent of Elements
N (%)P (g·kg−1)K (g·kg−1)
SoilC0.07 ± 0.01a *1.06 ± 0.05a5.70 ± 0.08a
FS0.06 ± 0.00a0.93 ± 0.01b5.64 ± 0.05a
PlantsC2.43 ± 0.07a4.94 ± 0.17a19.68 ± 0.68a
FS2.17 ± 0.03b3.92 ± 0.16b20.45 ± 0.58a
* Means marked with the same letters in each column do not differ significantly at p < 0.05, according to Tukey’s test. Data are presented as mean ± SD.
Table
Table 3. Effect of fertilisation on the intensity of CO2 assimilation (A) and transpiration (E), photosynthetic water use efficiency (ωW), stomatal conductance for water (gS), CO2 concentration in chlorenchyma intercellular spaces (ci), and concentration of assimilation pigments in leaves of maize.
Table 3. Effect of fertilisation on the intensity of CO2 assimilation (A) and transpiration (E), photosynthetic water use efficiency (ωW), stomatal conductance for water (gS), CO2 concentration in chlorenchyma intercellular spaces (ci), and concentration of assimilation pigments in leaves of maize.
TreatmentsGas Exchange Parameters
A
(μmol·m−2·s−1)		E
(mmol·m−2·s−1)		ωW
(mmol·mol−1)		gS
(mol·m−2·s−1)		ci
(μmol·mol−1)
C6.16 ± 1.55a *0.26 ± 0.05a24.79 ± 8.07a0.05 ± 0.01a235.22 ± 61.44a
FS6.92 ± 0.92a0.33 ± 0.07a22.16 ± 6.56a0.05 ± 0.02a273.47 ± 24.36a
TreatmentsConcentration of assimilation pigments
Chlorophyll “a” (mg·g−1 FW)Chlorophyll “b” (mg·g−1 FW)Ratio chl “a”/chl. “b”Total ChlorophyllCarotenoids (mg·g−1 FW)
C1.24 ± 0.12a0.35 ± 0.02a3.53 ± 0.1a1.59 ± 0.15a0.59 ± 0.05a
FS1.38 ± 0.12a0.38 ± 0.03a3.60 ± 0.09a1.76 ± 0.14a0.65 ± 0.05a
* Means marked with the same letters in each column do not differ significantly at p < 0.05, according to Tukey’s test. Data are presented as mean ± SD.
Table
Table 4. Effect of fertilisation on the fluorescence parameters of chlorophyll “a” in leaves of maize.
Table 4. Effect of fertilisation on the fluorescence parameters of chlorophyll “a” in leaves of maize.
TreatmentsF0FMFV/FMPIArea (bms)TFM (ms)
C219.34 ± 11.09a *1057.66 ± 65.49a0.78 ± 0.01a1.66 ± 0.38a35,009.62 ± 7474.56a740.62 ± 58.96a
FS228.43 ± 7.71a1114.39 ± 148.57a0.79 ± 0.01b1.82 ± 0.1a38,372.53 ± 2454.88a765.62 ± 15.72a
F0, initial fluorescence (zero); FM, maximum fluorescence; FV/FM, maximum potential photochemical reaction efficiency in PS II; P I, PS II vitality index; area, surface area above the chlorophyll fluorescence curve and between F0 and FM points proportional to the size of the reduced plastoquinone acceptors in PS II; TFM, time of chlorophyll fluorescence growth from the beginning of measurement to the maximal value. * Means marked with the same letters in each column do not differ significantly at p < 0.05, according to Tukey’s test. Data are presented as mean ± SD.
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Hawrot-Paw, M.; Mikiciuk, M.; Koniuszy, A.; Meller, E. Influence of Organomineral Fertiliser from Sewage Sludge on Soil Microbiome and Physiological Parameters of Maize (Zea mays L.). Agronomy 2022, 12, 1114. https://doi.org/10.3390/agronomy12051114

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Hawrot-Paw M, Mikiciuk M, Koniuszy A, Meller E. Influence of Organomineral Fertiliser from Sewage Sludge on Soil Microbiome and Physiological Parameters of Maize (Zea mays L.). Agronomy. 2022; 12(5):1114. https://doi.org/10.3390/agronomy12051114

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Hawrot-Paw, Małgorzata, Małgorzata Mikiciuk, Adam Koniuszy, and Edward Meller. 2022. "Influence of Organomineral Fertiliser from Sewage Sludge on Soil Microbiome and Physiological Parameters of Maize (Zea mays L.)" Agronomy 12, no. 5: 1114. https://doi.org/10.3390/agronomy12051114

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