Fertilization and Soil Microbial Community: History
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Subjects: Area Studies
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Lucian Dinca

Crop production is currently expanding globally due to an increased demand for food, animal feed and biofuels; the latter has been stimulated by the increase in oil prices making bioenergy crops more competitive and profitable compared to fossil fuels. Chemical fertilizers (also termed mineral, inorganic or synthetic fertilizers) contain a high concentration of a primary nutrient (nitrogen, N; potassium, K; phosphorous, P) as inorganic salts. Secondary elements (calcium, magnesium and sulfur) can also be added to soil by chemical fertilizers. Micronutrients (boron, manganese, iron, zinc, copper, molybdenum, cobalt and chlorine) are in general absent in NPK chemical fertilizers and can be supplied by specific synthetic and expensive plant nutrients with soil or foliar applications. Soil microbes have different responses to fertilization based on differences in the total carbon (C), nitrogen (N) and phosphorus (P) contents in the soil, along with soil moisture and the presence of plant species.

  • microorganisms
  • microbial activity
  • fungi
  • farming practices

1. Introduction

Currently, 47.9 million km2 are devoted to agriculture, which is about 50% of habitable land [1].
Higher yields and better harvest quality can be achieved through the optimized use of fertilizers and the implementation of strategic production practices. Chemical fertilizers (also termed mineral, inorganic or synthetic fertilizers) contain a high concentration of a primary nutrient (nitrogen, N; potassium, K; phosphorous, P) as inorganic salts. Secondary elements (calcium, magnesium and sulfur) can also be added to soil by chemical fertilizers. Micronutrients (boron, manganese, iron, zinc, copper, molybdenum, cobalt and chlorine) [2] are in general absent in NPK chemical fertilizers and can be supplied by specific synthetic and expensive plant nutrients with soil or foliar applications [3].
The nutrient content in chemical fertilizers is indicated as the N:P:K rate, representing the percentages of nitrogen, total phosphorus (in the form of phosphorus pentoxide, P2O5) or total K (in the form of potassium oxide, K2O). If they also contain secondary elements, numbers in brackets specify calcium oxide (CaO), magnesium oxide (MgO), sodium oxide (Na2O) or sulfur trioxide (SO3) content.
The majority of the inorganic fertilizers (with the exception of N) is extracted from rocks using physical or chemical processes. N fertilizers (mainly as ammonium—NH4+—and nitrate—NO3−: urea, urea ammonium nitrate, ammonium nitrate and calcium ammonium nitrate) are produced by combining atmospheric N2 with hydrogen (mainly from hydrocarbons such as natural gas—CH4) to obtain anhydrous ammonia (NH3), which can be used directly as a plant nutrient or converted into other different N fertilizers [4][5]. Phosphate fertilizers (principally single superphosphate, triple superphosphate, mono-ammonium phosphate, di-ammonium phosphate and ammonium polyphosphate liquid) are extracted from natural phosphate rock deposits [6]. K fertilizers (potash muriate, KCl; potassium sulfate, K2SO4; potassium nitrate, KNO3; sulfate potash magnesia, K2SO4·MgSO4; kainite, KCl + NaCl + MgSO4) are produced by different chemical processes [7].
Differently, organic fertilizers (Table 1) are derived from plant- or animal-based materials or other organic constituents that are either a by- or end-product of naturally occurring processes, containing both the essential nutrients and micronutrients for plant growth. They also comprise biofertilizers (bacteria, algae, fungi or biological compounds), including plant-growth promoting bacteria [8][9][10].
Table 1. Organic fertilizers.
Type Production Process and Materials Pros and Cons Refs.
Biochar and biochar-based fertilizers Pyrolysis (thermal decomposition of organic matter with absence of or very limited access to oxygen), hydrothermal liquefaction and gasification of different type of biomass (agricultural residues, sewage sediment, forest waste, energy crops and residues from agro-food processing) They improve physical, chemical and biological properties of soil, together with nutrient absorption and cation exchange capacity. They reduce the uptake of metals, pesticides, PAHs, engineered nanomaterials, and pharmaceuticals by plants. The type of biomass used influences the biochar properties. If used together with other fertilizers, they can reduce their beneficial effects. [11][12][13]
Biofertilizers or microbial fertilizers (bacteria, algae, fungi or biological compounds), including-plant-growth-promoting bacteria Isolation of microbes, screening, scale-up Increase soil fertility by various macro- and micronutrients; improve soil biodiversity and plant growth by increasing the accessibility to or uptake of nutrients from a limited soil nutrient pool. Power of biofertilizers depends on the type of microorganism used and their metabolic activity during and after field applications. [8][9][10][14][15]
Biosolids Stabilization of organic solids from sewage treatment processes (mainly from biological treatment of wastewater). The stabilization reduces the pathogen presence They contain macro and micronutrients in variable quantities; K concentrations are commonly low, so that an additional K fertilization may be necessary. They can contain pathogens, traces of metals, pharmaceuticals, personal care products and other organic contaminants (e.g., phthalates, pesticides, phenols, PCBs, dioxins). [16][17]
Bio-surfactants Surface-active biomolecules produced by microorganisms (bacteria, yeasts and fungi); they have both hydrophilic and hydrophobic regions They increase the surface area of hydrophobic substrates (e.g., hydrocarbon pollutants, heavy metals or nutrients) increasing their bioavailability (solubilisation/desorption). They also regulate the attachment and removal of microorganisms from surfaces. Used for hydrocarbon biodegradation in contaminated soil, for plant pathogen elimination thanks to their antifungal, antiviral, insecticidal and antimycoplasma activities and for increasing the nutrient bioavailability for beneficial plant-associated microbes. [18][19][20]
Compost Composting (biological decomposition under controlled moisture, self-heating and aerobic conditions) of animal manure, sewage sludge, municipal solid waste and green wastes Simplicity of technologies and possibility of implementation on every farm; quality protocols are provided in several countries for reducing pathogen, heavy metal and organic pollutant presence. [21][22]
Green waste or biowaste Different origins: crop residues, food and kitchen waste. It does not include forestry or agricultural residues, manure, sewage sludge or other biodegradable waste such as natural textiles, paper or processed wood. Improve soil structure; low nutrient content; could contain plant pathogens. [23]
Digestate Anaerobic fermentation of different organic wastes (food waste, manure and energy crops). Microorganisms, under anaerobic conditions, convert organic matter into biogas and digestate Production of biogas; digestate could contains residual concentrations of contaminants (e.g., plastics, pharmaceuticals, including antibiotics, etc.) depending on the type of biowaste used; a duff layer could be formed on soil surface that hinders seed germination. [21][24][25][26]
Manure Mainly from beef, pig or poultry livestock Improve soil structure (depending on its origin). Increase in potentially mineralizable N. Potentially pathogenic; could contain heavy metals used for animal feed, manily Zn and Cu; could contain pharmaceutical residues and antibiotic resistance genes; water pollution by nitrates or by P in intensive livestock productions by spreading manure rich in N and P out of the soil capacity. [27][28][29][30]
Vermicompost Vermicomposting, a bio-oxidative process involving several organic materials (e.g., sewage sludge, crop residues, manure, digestate) using mainly epigeic earthworm species and different microorganisms. It is rich in microorganisms, nutrients, vitamins, and growth hormones; used also as biocontrol agents against diseases and pests. The nutrient-rich compost could also be used for biogas production. [31][32][33][34]
Inorganic and organic fertilizers have an important role in increasing agricultural production, but the use of mineral fertilizers is constantly growing, with an estimated total 186.67 million tons in 2016 [35]. There is increasing concern regarding the negative environmental effects of chemical fertilizers. In fact, they can cause serious greenhouse gas (GHG) emissions and pollution of soil and water ecosystems. For example, synthetic nitrogen fertilizers have been recognized to be the most important factor contributing to direct N2O emissions into the atmosphere as a consequence of their biodegradation by soil microorganisms [36]. In addition, only 50–60% of synthetic nitrogen fertilizers added to soil is usually taken up by crops [7], and the rest runs off into water bodies (surface or groundwater [37]) due to their high dissolution properties. A possible alternative is the use of controlled-release fertilizers (coated and uncoated fertilizers with a low solubility) [38], but they are expensive and, therefore, used mainly for high-value crops (e.g., vegetables, fruits, flowers, ornamentals) [7]. Inhibitors of nitrification and urease processes can also be used for maintaining N in its soil-stable form by slowing its conversion to nitrate or delaying the first step of degradation of urea [39]. For these compounds (such as dicyandiamide, thiosulfates, 3,4-dimethylpyrazole phosphate), there is a lack of correlation between laboratory testing data and the actual field data [40]; there is also some concern about the potential for some of them to enter the food chain [41].
Phosphorus availability to plants after chemical fertilization can vary depending on the type of fertilizer used and, even under the best conditions, only about 25% of applied P is taken up by plants during the first cropping season [42]. Depending on the pH and moisture of soil, P can than precipitate (at high pH due to the presence of calcium and magnesium and at low pH due to an iron and aluminum presence) [43] or can be immobilized in soil [44]. The use of P fertilizers also leads to eutrophication (when P runs off to surface waters) [45]. Potassium has several beneficial roles in plant physiological and metabolic processes, including resistance to biotic and abiotic stresses and absorption and utilization of N and P by crops [46]. On the other hand, fertilization with KCl does not increase crop yields and has detrimental effects on the quality of major food, feed and fiber crops, with serious repercussions for soil ecosystem and human health [47].
Conversely, organic farming using organic fertilizers that are environmentally friendly amendments (e.g., microbial fertilizers [48][49], manure, compost) can be a good alternative and can reduce the consequences of environmental pollution from synthetic fertilization. In fact, organic fertilizers for example gradually release primary and micronutrients into the soil, maintaining a nutrient balance for a healthy growth of crop plants. They can also be an effective source of soil microbes, while also improving soil structure [50]. Table 1 shows a list of the main organic fertilizers.
Fertilizers and amending materials are regulated in the EU by the Regulation 2019/1009. In the US, they are differently regulated at the state level rather than by the federal government.
Fertilizers in China are controlled by several regulations and standards. Importing, producing, selling or utilizing un-registered fertilizers is not allowed. Moreover, fertilizers sold in China also have to meet important product standards and requirements for their marking, with the compulsory national standard GB 18382-2021, which was issued in 2021 and comes into force on 1 May 2022. The “Mandatory national standard GB 38400-2019 Limit requirements for toxic and harmful substances in fertilizers” that comes into force on 1 July 2020, defines the hazardous substance limits in fertilizers (i.e., heavy metals).
In Brazil, the main regulatory agencies for fertilizers are MAPA (the Brazilian Ministry of Agriculture, Livestock and Food Supply), ANVISA (Brazilian Health Regulatory Agency), MMA (Brazilian Ministry of Environment) and INMETRO (Brazilian National Institute of Metrology, Quality and Technology). Law 6894/80, also called the “Fertilizer Act”, contains the general rules regarding the registration and classification of such products. It is devoted to the inspection of the production and trade of fertilizers (including also correctives, inoculants, stimulants, bio-fertilizers, remineralizers and substrates for plants). All these fertilizers have to be registered at the Ministry of Agriculture. The Fertilizer Act is regulated by the Decrees n. 4954/2004 and n. 8384/2014.
In India, the Ministry of Chemicals and Fertilizers (https://fert.nic.in (accessed on 18 January 2022)) is devoted to the regulation of fertilizers. The Fertilizer Control Order provides for registration of fertilizer manufacturers, importers and dealers; it is specifically for all fertilizers manufactured/imported and sold in the country, regulating also fertilizer mixtures, and the packing and brand description on the fertilizer bags etc. Chemical fertilizer consumption has been generally increasing in India during the last 4 years, with a maximum of 59.88 million tons of fertilizer products used (mainly urea, di-ammonium phosphate, murate of potash, complexes and single super phosphate), as recently reported by the Indian Ministry of Agriculture and Farmers’ Welfare (https://pib.gov.in/PressReleseDetail.aspx?PRID=1696465 (accessed on 18 January 2022)).
Soil biota encompasses a huge diversity of organisms, including microorganisms (i.e., bacteria, fungi and archaea), which are the largest group of soil organisms in terms of number and biomass [51]. Soil microbial communities play important roles in ecosystem functions and regulate key processes, such as the carbon and nitrogen cycles [52]; for example, microorganisms carry out the ecological functioning of N2-fixation, ammonia-oxidation, denitrification and ammonification. Microbial communities are also key players in the degradation of various compounds, including organic pollutants such as pesticides [53], and they promote plant growth and disease control [54]. The diversity and biomass of soil microbial communities are the major regulators of fundamental ecosystem processes [54], supporting crop production [51]. In fact, a good soil quality, which means a diverse and abundant microbial community and activity, is a pre-requisite for plant growth and, consequently, for crop production [55]. In particular, soil microbial biomass, activity and diversity are an indicator of soil fertility and ecosystem productivity [56][57]. For this reason, they are used as indicators of soil quality and health [51][58]. Soil quality is defined as the capacity of a specific kind of soil to function, within natural or managed ecosystem boundaries, to sustain plant and animal productivity, maintaining or enhancing water and air quality, and supporting human health and habitation [59]. Microbial populations vary depending on different abiotic factors such as soil type, presence/absence of plants and climate; their responses to similar fertilization treatments can thus be different depending on the above-mentioned abiotic factors. During the long-term process of evolution, soil, plants and microbes co-evolved to form relatively stable relationships within a given ecosystem. In fact, the soil microbial community has recently been termed the soil microbiome [52][60][61]. Changes in soil microbial communities induced by environmental changes could influence the relationships between microorganisms and plants and may negatively influence soil fertility and crop productivity. Consequently, studying the effects of chemical/organic fertilizers on the natural microbial community is of crucial importance. For example, understanding how NPK chemical fertilizers influence the microbial biomass, which is an indicator of soil fertility and quality, is a basic prerequisite for understanding microbiological processes [62], in order to preserve the ecosystem functions of soil.
These research themes are an important part of soil ecology, as pointed out by several international authorities (e.g., EU commission, FAO [63][64]). The use of inappropriate farming practices (e.g., excessive use of chemical fertilizers and pesticides) and frequent changes in land use may cause variability in soil microbial communities, which can have significant effects on soil fertility and productivity [65].

2. Effects of Chemical Fertilizers on Biomass, Activity and Diversity of Soil Microorganisms

It has been generally shown that both chemical and organic fertilizers can directly stimulate the growth of specific microbial populations by supplying nutrients [66], leading to an increase in total microbial numbers [67][68][69][70], improving microbial activity [71] and determining a switch in microbial diversity. A high soil microbial diversity is crucial for the productivity and stability of the agroecosystems [72]. In several studies, mineral fertilization has been found to reduce microbial diversity, including the plant-beneficial microbial taxa [72]. Meta-analysis of microbial communities, based on 107 datasets from 64 long-term trials from around the world, concluded that mineral fertilizer application (in particular N fertilizer treatment) leads to a 15.1% increase in microbial biomass compared to unfertilized control plots; moreover, N application (urea and ammonia fertilizers) can have a temporary or stable effect in increasing pH [73][74][75]. However, the use of a chemical fertilizer alone does not lead to a remarkable increase in soil microbial abundance. This was observed in a rice–wheat cropping system [76], in a drip-irrigated cotton systems [70] and in paddy field soils [77]. Long-term mineral fertilization, and in particular N addition, increases microbial biomass beca.use soil microorganisms may be carbon- or N-limited. The increase is significant if soil pH is >5; in other cases, fertilization reduce microbial biomass [73].
Soil-available P and total N are the most important factors influencing the abundance of microbial communities involved in the nitrogen cycle [78]. However, chemical fertilization, in particular N addition, was found to decrease bacterial alpha-diversity [79], although a recent study found that soil fertility and plant yield was mainly due to bacterial and archaeal abundance and community structure rather than bacterial, archaeal or fungal alpha-diversities [80]. In fact, the increase in microbial biomass has been attributed to better plant growth, which results in higher rhizodeposition [81]. The latter was found to be more active in determining a shift in the fungal community [82]. That is, soil bacteria were more sensitive than fungi to fertilization practices [83][84]. In addition, the plant composition and carbon substrate utilization patterns of rhizobacterial communities were more diversified in unfertilized plots than in chemical fertilized plots in grasslands [85]. Long-term NPK applications have been found to result in a loss in soil organic matter (SOM), especially in arid and semi-arid areas or where a monoculture is performed (e.g., corn) [86][87][88]. An increase in SOM by mineral fertilizers has been found only when they are applied in combination with organic amendments [89][90]. SOM quality greatly influences soil microbial community composition [91]. Soil quality and crop yield also depend on SOM content [3]. The latter affects the availability of micronutrients, with higher micronutrient amounts in higher SOM content [3]. Moreover, SOM quality (e.g., organic acid, protein, humic acid and lignin content) and its biodegradability essentially influence microbial characteristics (e.g., specific population size, microbial activity and composition) [90][92]. Consequently, any SOM depletion has negative consequences for microbial community richness together with lower plant health, growth and productivity.
In general, organic fertilizers improve soil structure (in terms of particle-size fraction [93]), and they are responsible for a more balanced and stable nutrient supply, which can sustain a more diverse microbial community if compared to mineral fertilizers [94]. Moreover, organic fertilization is reported to increase microbial activity and SOM content and improve the chemical and physical properties of soil better than inorganic fertilization [95][96][97], preventing the decrease in soil pH due to mineral fertilizer application [86]. In any case, long-term inorganic or organic fertilization significantly decreased soil pH if compared to a non-fertilized control [82], although soil pH changes due to organic amendments depend on the amendment used [98]. For example, some biochar was found to increase soil pH [98], whereas manure could in general decrease soil pH [99].
Dehydrogenases are respiratory enzymes that oxidase organic compounds allocating two hydrogen atoms from these compounds to electron acceptors, producing energy [57]. These enzymes are present in all soil microorganisms and are not present as a free form, representing only the activity of live microbial cells. Consequently, dehydrogenase activity has been considered as an indicator of soil microbiological activity [57][100][101][102].
Dehydrogenase activity (DHA) was found to be lower in soils that had received high (160 N, 120 P2O5, 160 K2O) amounts of NPK fertilization [94], suggesting that these enzymes are highly sensitive to the inhibitory effects associated with high mineral fertilization. In addition, long-term P-deficiency fertilization can significantly decrease DHA together with soil microbial biomass and bacterial diversity [86]. Although an NPK balanced fertilization can increase DHA, the higher increase is always found with organic fertilization [67]. Applying phosphorus-based fertilizers has been shown to lead to seasonal variations in microbial activity, as well as in the abundance of specific bacterial and fungal phospholipid fatty acid (PLFA) indicators of soil microbial biomass [103][104][105].
In their experimental study, Enebe and Babalola [106] examined the response of maize bacterial, fungi and archaeal communities to compost and inorganic fertilizations. The results showed that both fertilizers influenced the maize rhizosphere microbial community but the organic amendments provided the most stable microbial community; these results were also found by Zhang et al. [107], in which higher levels of NPK treatments (60 kg of NPK fertilizer as N/ha) negatively affected the microbial community structure and abundance in an agricultural soil.
On the other hand, long-term fertilization with organic amendments can both mitigate the negative effects and exploit the positive effects of climate change on crop production, enhancing soil quality and improving crop productivity, as was observed by several authors (e.g., Song et al. [108] in northeast China).
In an overall view, although it is not possible to summarize all the beneficial effects of organic fertilizers because they are very different in type of production, content in essential nutrients (NPK), pH, structure, etc., they always improve soil structure and organic matter content of soil, together with an increase in microbial communities. Moreover, thanks to the soil quality improvement, they also favor microbial community abundance and activity. On the other hand, although mineral fertilizers, apart from their environmental side effects (GHG emission, soil and water pollution), provide essential nutrients, long-term application contributes to soil depletion. In fact, soil treated only with chemical fertilizers relies solely on the root residues and exudates of the crops to increase carbon input [89].

3. Types of Fertilizers Used and Their Influence on Soil Microbial Community

The sustainable development of agroecosystems is based on a better understanding of the complex responses of microbial communities to the various organic and inorganic fertilization regimes, as highlighted by Pan et al. [109], demonstrating that a better understanding of the complex responses of microbial communities to various organic and inorganic fertilizations is critical for a sustainable development of agroecosystems. They found that using chemical fertilizer together with manure clearly increased soil fertility and were recommended for further optimization of fertilization patterns. In addition, the results of their research suggested that organic and inorganic fertilizers dominated in shaping bacterial and fungal community distributions in fluvo-aquic soils.
Nakhro and Dkhar [77] compared the use of organic fertilizers with inorganic ones, observing that organically treated soils had the largest number of microorganisms (fungi and bacteria) and microbial biomass carbon. Chemical fertilizers, on the other hand, have been shown to have a smaller effect than other soil treatments on bacterial composition and diversity [110].
Comparing the effects of chemical fertilizers with manures (farmyard manure, slurry and green manure), Edmeades [111] concluded that there is no significant difference in the long-term effects on crop production between these two types of fertilization. However, manured soils had higher organic matter contents and higher numbers of microfauna than soils added with chemical fertilizers. The manured soils were also more enriched in P, K, Ca and Mg in the topsoil and nitrate, N, Ca and Mg in the subsoil.
When an organic fertilizer is applied to soil, its decomposition is due to bacteria and fungi, which in turn support the soil fauna chain. The ratio of fungal to bacterial biomass can be considered an indicator of the activity of two pathways of the soil food web, formed by fungivores or bacterivores and their predators, respectively [112]. In general, bacteria are prevalent under conventional tillage, whereas fungi dominate under no-tillage. The use of nitrogen fertilizers by applying organic amendments decreases the fungi/bacteria ratio and can decrease the soil pH [112].

This entry is adapted from the peer-reviewed paper 10.3390/app12031198

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