Long-Term Fertilization in the Crop Rhizosphere: History
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Subjects: Soil Science
Contributor:
Vyacheslav M. Semenov

Fungi represent a highly diverse group of organisms that play an essential role in maintaining soil health and ecosystem functioning. Fungi interact with plants at various niches, including the rhizosphere—a narrow zone of soil adjacent to the roots of living plants that is directly influenced by root exudates.

  • fungi
  • organic fertilizers
  • NPK

1. Introduction

Fungi represent a highly diverse group of organisms that play an essential role in maintaining soil health and ecosystem functioning [1]. Fungi are important decomposers and recyclers of recalcitrant or labile organic materials [2]. Although they are often involved in symbiosis with plant roots [3], they can also be soil-borne plant pathogens [4]. Many fungal groups combine these opposite lifestyles—saprophytic, pathogenic, or symbiotic—and they can switch between different strategies depending on the environmental conditions [5]. Despite their high biomass and importance for ecosystem sustainability, the fungal diversity in soil is significantly less studied than the bacterial diversity [4].
Fungi interact with plants at various niches, including the rhizosphere—a narrow zone of soil adjacent to the roots of living plants that is directly influenced by root exudates. Nutrient-rich rhizosphere niches harbor specific fungal communities, including the rhizosphere mycobiome [6]. The rhizosphere mycobiome includes many potential plant pathogens and their antagonists, and can therefore influence plant health and soil disease suppressiveness [7][8]. In the rhizosphere, plant pathogens interact intensively with the rest of the microbial community, which partly determines whether a plant becomes infected [9]. Hence, understanding the factors that shape the composition and intermicrobial relationships of the rhizosphere mycobiome is an important step to control plant health and productivity [10][11].
At a regional level, climate, soil chemistry, and location are usually considered as the major predictors of fungal richness and community composition [12]. Thus, the structure and diversity of soil and rhizosphere mycobiomes are driven by edaphic physicochemical characteristics, such as organic C [13][14], pH [15], and moisture [4]. Soil fungal diversity often is decoupled from plant diversity, although relationships between plant and fungal diversity can be strong locally [4][16][17][18]. The reason for this coupling is that each plant species selects fungal communities in the rhizosphere through the composition of its root exudates [19]. In addition to plant species, the plant developmental stage determines the composition and quantity of rhizodeposits and the associated microbiome [20].
At the farm level, land use and management, such as tillage and fertilization, lead to changes in many soil properties affecting fungal communities [21][22]. Long-term application of mineral fertilizers or fresh farmyard manure supplies large amounts of nutrients to the bulk soil, which is regarded as an oligotrophic environment without these extra nutrients [23]. Introduced nutrients reduce the dependence of the rhizosphere communities on plant-derived C and activate many dormant fungal species. Inorganic N additions may result in increased exudation and soil acidification, changing the soil fungal community [24]. Increased inorganic nutrient availability for plants decreases their dependence on fungal symbioses [25]. Ultimately, inorganic fertilization decreases fungal diversity and biomass [25][26]. In the end, plant-microbe networks in soil often are weakened by the long-term use of inorganic fertilizers [27]. Contrary to inorganic fertilization, the application of organic fertilizer shifts the composition and abundance of fungal communities, and may increase fungal diversity [26][28]. The increase in fungal diversity often leads to root disease suppression [29][30]. Thus, long-term fertilization is a crucial factor determining both rhizosphere nutrient status and fungal communities in agroecosystems. The contribution of long-term fertilization into plant species effects into rhizosphere fungal communities in agroecosystems is not yet fully understood.

2. Long-Term Organic Fertilization Shapes Rhizosphere and Bulk Soil Mycobiome and Reduces Its Diversity

The conducted study shows that fertilization can be a crucial factor determining the structure, diversity, and abundance of fungal communities in bulk soil and plant rhizosphere. The researcher identified two groups of fungal communities: (1) bulk soil and rhizosphere under NPK or without fertilization, and (2) bulk soil and rhizosphere under manure. Despite the sharp decline in soil pH due to the long-term application of physiologically acidic mineral fertilizers, fungal communities under NPK treatment did not differ significantly from those in unfertilized soils. In turn, the application of organic fertilizers hardly changed the soil pH but significantly increased the microbial biomass and fungal abundance. In addition, the application of organic fertilizers decreased the fungal diversity and prevented the detection of many fungal taxa from the bulk soil and rhizosphere. Thus, our study confirms previous findings that soil fungal community composition is primarily driven by total organic carbon content rather than soil pH [13][14].
Nevertheless, the effect of fertilizer systems on the soil fungal communities is not yet fully understood. Organic fertilization commonly increases fungal abundance in soils with manure [14][28], but NPK application could increase [31] or decrease it [28]. Similarly, fungal diversity may decrease [26][31] or remain unchanged [24][28][32][33] under long-term mineral fertilization. Some authors have explained this variation by the difference in pH across soils. Long-term mineral fertilization decreases fungal diversity in neutral soils (pH > 6, such as Phaeozems in our study) rather than in acidic soils (pH < 6) [28][33]. Trends in fungal diversity under organic fertilizers are even more variable. The application of manure may increase fungal diversity [26][28] or decrease it [32], or it may remain unchanged [33].
Among the most abundant fungal genera, Mortierella was the only taxon that increased its abundance under both mineral and organic fertilizer systems. Species of Mortierella live as saprotrophs in soil and are usually non-pathogenic for plants. Mortierella could also promote plant growth and are dominant in suppressive soils [34]. The application of mineral fertilizers increased the abundance of many phytopathogenic taxa, particularly Fusarium. Under organic fertilization, Cephaliophora, Cercophora, Phialophora, and Preussia became the most represented genera in bulk soil and rhizosphere mycobiomes. Cephaliophora consists of rotifer-capturing species, while Cercophora are typical coprophilous species [35]. The genus Phialophora was also detected by plating on solid media in our previous study, and was identified as Phialophora fastigiata—a saprophyte commonly found in soil or on decaying wood [36]. Several Preussia species produce bioactive secondary metabolites, particularly the preussomerins, which perform an antimicrobial activity [37].
Plate counting on Czapec and PDA media gave the opposite results for cultivated fungal diversity in the same treatments as studied here: Applications of NPK led to a decrease in cultivated fungal diversity, while organic fertilization increased it [36]. Altogether, 39 fungal species belonging to 19 genera were cultivated. This is less than 5% of the total fungal diversity (444 genera) obtained by DNA metabarcoding in this study. However, some fungal genera detected by plating are not always found by DNA metabarcoding, e.g., Epicoccum and Sarocladium. Penicillium was the dominant genus in cultivated communities [36]. However, it was a minority taxon in our current experiment. In contrast to our current results, the abundance of cultivated Trichoderma was higher in manure plots than in soils treated with NPK [36]. Thus, the results based on culture-dependent and -independent techniques using the same soil samples may be completely different and may sometimes arrive at opposite conclusions. The differences may be due to the increased detection of sporulating fungi by cultivation on solid media and the decreased detection of these fungi by direct DNA or RNA extraction and metabarcoding as it is more difficult to extract nucleic acids from spores than from mycelium.

3. Long-Term Fertilization Overrides Plant Species Effects on Rhizosphere Mycobiomes

The effect of fertilizers on fungal communities was detected not only in the bulk soil but also in the rhizosphere of the studied crop species. Moreover, the influence of plant-related factors on rhizosphere mycobiomes was much less compared to long-term fertilization. The plant-related rhizosphere effect was indicated by an increase in fungal abundance and biomass, as well as in the dominance of some fungal indicator taxa. However, this effect was governed by what type of fertilizer was applied—mineral or organic.
Plants and fungi often have strong interspecies relationships. Therefore, rhizosphere mycobiomes are commonly considered to differ from those in bulk soil and between plant species [38]. Fungi are heterotrophic organisms that depend on exogenous C for growth, and plant root exudates contain C substrates for their growth and development. The researcher revealed that fertilization, regardless of the type, led to the convergence of the rhizosphere and bulk soil fungal community structures. This is in accordance with our previous culture-dependent analysis [36]. Long-term input of mineral or organic fertilizers may decrease a preference of the rhizosphere microbiome for root-derived substrates [39], since soil labile organic carbon introduced with organic fertilization is more than enough to level out the contribution of root exudates [40]. The long-term application of mineral fertilizers without additional C source also alters the rhizosphere mycobiome [24] and weakens plant-microbe networks [27].
On the other hand, the effect of fertilizers on the fungal community of the soil versus the rhizosphere was much lower than on bacteria [41][42]. First, fungi are less sensitive to changes in pH caused by the application of mineral fertilizers. Second, the plant-related effect was much higher for the rhizosphere mycobiome in the NPK plots: The interaction between the plant species and its stage of development had a strong impact on the fungal abundance. Unlike bacteria, many indicative fungal taxa were associated with a particular plant species.

4. Plant Pathogens in Rhizosphere and Soil Suppressiveness Management

Long-term application of manure drastically reduced the soil and rhizosphere fungal diversity in our study. Microbial diversity is considered as one of the factors responsible for the sustainable functioning of soil systems [43][44]. Rhizosphere microbiomes influence the productivity of plant communities, promote plant growth, and protect plants from pathogens [7]. The latter is closely related to soil suppressive activity against plant pathogens [8][45]. Higher microbial diversity in the rhizosphere of plants has been shown to increase soil suppressiveness [34].
Indeed, organic fertilization significantly reduced the relative abundances of most pathogenic genera detected in our study. A similar effect of organic fertilizers was found in previous studies, e.g., for Alternaria, Fusarium, and Gibberella [15][28][32]. Long-term application of manure also increased the relative abundance of Cladorrhinum, a potential biological control agent for the reduction of Rhizoctonia solani [46]. Organic amendments have been proposed as a strategy for the management of plant diseases caused by soil-borne pathogens [29][45], and they have been effective in the suppression of Fusarium [47], Verticillium [30], Pyrenochaeta [48], and many other fungal genera [29]. The suppressive effect is likely related to an increase of pathogen-antagonistic fungi (e.g., Mortierella, Pseudaleuria, and Hypocreales [28][34]) or biocontrol bacteria, such as Collimonas and Lysobacter [39], since the organic fertilizers may act as an alternative C source for the antagonists. Banerjee et al. also showed that the network connectivity and abundance of keystone microbial taxa were higher under organic farming than conventional farming, which could be related to higher soil suppressiveness [49].
Contrary to the suppressive effects of organic fertilization, the long-term application of mineral fertilizers led to an increase in the relative abundances of several potential phytopathogenic genera, such as Alternaria, Gibellulopsis, Fusarium, Gibberella, Eocronartium, and Plenodomus. In some samples, the sum of potential plant pathogenic genera reached more than 40% of the total mycobiome. Increases in phytopathogens [15][24][26] and root diseases were shown to be associated with mineral fertilizer applications in previous studies [44][50].
The abundances of Trichoderma and Humicola also increased with mineral fertilizers in our experiment. Trichoderma species are opportunistic, avirulent plant symbionts, which can be parasites and antagonists of many phytopathogenic fungi, thus protecting plants from disease [51]. Humicola species from soil are considered as potential antagonists for the biological control of plant diseases [52]. However, the high abundances of Trichoderma and Humicola were associated with large numbers of phytopathogenic fungi. Therefore, antagonistic activity related to phytopathogens depends on specific ecological conditions and may not necessarily occur. Moreover, the antagonistic effect may not occur at the same time, but at a lag that can be observed only by sampling frequently over time.
The large differences between the effects of organic and mineral fertilization on fungal communities are likely partially due to the differences in the soil food web. Fertilization by manure likely strengthens the microbe-eukaryote associations, such as survival, predation, and cooperation, more than NPK application [53]. Fungal mycelium is an efficient nutrient source for soil nematodes, collembola, oribatid mites, and enchytraeids due to the low C/N ratios of fungal cords and hyphae compared to plant-derived organic matter [54]. Since soil fauna can suppress the abundance of many plant pathogenic fungi (e.g., Fusarium spp.) in agricultural ecosystems [55], organic amendments might therefore be used to control the soil-borne phytopathogens by manipulating the structure of detrital food webs.

This entry is adapted from the peer-reviewed paper 10.3390/jof8030251

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