Shifts and recovery of soil microbial communities in a 40-year field trial under mineral fertilization
Introduction
The application of fertilizers into soil is primarily used to increase nutrient availability to growing plants and therefore to raise the yield of the subsequent harvest; nevertheless, it can also affect soil microorganisms (Marschner et al., 2003). Soil microorganisms have long been recognized for their indispensable role in decomposition of organic residues, cycling of nutrients and production of crops (Shen et al., 2010).
Among the most ecologically relevant microbial parameters sensitive to changes in soil management (including fertilization) are microbial enzymatic activities, mainly due to their narrow relationship with the biological status of soil and relatively easy assessment (Moscatelli et al., 2018). Microbial enzymatic activities have been successfully used for assessment of the impact of both mineral and organic fertilizers on the microbial status of different soil types in various climatic regions (Debosz et al., 1999; Marinari et al., 2000; Pajares et al., 2009; Reardon and Wuest, 2016; Tamilselvi et al., 2015).
Inorganic fertilizers have been reported to have effects on both microbial activities and soil microbial community structure (Böhme et al., 2005; Chen et al., 2014b; Ding et al., 2016; Marschner et al., 2003; Pan et al., 2014). In a literature review by Allison and Martiny (2008), 84% of 38 studies reported that microbial community composition is sensitive to N/P/K fertilization. However, the results are often contradictory, and both stimulating and suppressing effects of fertilizers on activity and composition of microbial communities can be observed. In general, microbial communities are dynamic systems, able to change rapidly in response to a disturbance such as an addition of fertilizer.
Despite the sensitivity of microbial parameters to soil management, they are naturally highly variable with regard to different soil types and various physico-chemical soil properties. Field experiments that are managed for a relatively long time (decades) are then a very effective tool for drawing plausible conclusions about the manipulated parameter, because the other variables remain unchanged. Moreover, long-term field trials, if appropriately arranged, might represent a great opportunity to survey the recovery of microbial communities, whether in terms of their structure or activity, if the manipulation (fertilization) is terminated. As proposed by Stevens (2016), recovery from an environmental perturbation can sometimes be difficult to define, because reversion to a pre-existing state often fails to consider natural developments within the system (e.g. succession). This means that in a permanently changing environment it is not always realistic to expect an individual site to return to a previous state. However, in replicated long-term trials with experimental controls, recovery can be advantageously considered as convergence with control plots (Stevens, 2016). Although, much of work has been done in the field of spontaneous recovery of plant diversity after cessation of fertilization in grasslands (e.g. Královec et al., 2009; Pallett et al., 2016), there are only a very limited number of studies involving terminated inorganic fertilization that are focused on microbial recovery (Chen et al., 2014a; Griffiths et al., 2012; Malý et al., 2009). In general, research on microbial communities after cessation of environmental disturbance is needed to provide a missing insight into their ecological resilience and recovery rate.
The present investigation was undertaken (1) to assess the impact of long-term inorganic fertilization of grassland field on soil microbial enzymatic activities and on the composition of soil bacterial and fungal communities, and (2) to analyze possible relationships between microbial community composition and activity. The investigation was carried out in soils of field trial in the Czech Republic, fertilized since 1969. In a previous study situated in the same long-term field fertilization trial (Malý et al., 2009), it was shown that permanent application of mineral fertilizers increased the proportion of r-strategists in soil. However, it was not clear whether the changes in the r/K strategy were linked to changes in the composition of microbial communities or caused by transition between the r/K physiological states. Here we hypothesize that long-term application of mineral fertilizers leads to changes in the functioning of microbial communities, assessed as the activity of extracellular enzymes, and that these changes are coupled with shifts in soil bacterial and fungal community composition. Furthermore, although it is likely in general that repeated additions of fertilizers impact the microbial communities to some degree, it is unknown whether the fertilization produces lasting effects, particularly after the plots return to a non-fertilization regime, and whether the microbial communities are ecologically resilient. Fortunately, the long-term field trial includes a treatment where application of fertilization was stopped after 20 y of fertilization, with the subsequent two decades under a non-fertilization regime. With this treatment, we have a rare opportunity to raise and test the hypothesis that the changes in microbial parameters caused by permanent inorganic fertilizer inputs persist beyond the cessation of the fertilization and can be apparent even 20 y afterward.
Section snippets
Experimental field
Soils for the study were sampled from a long-term experiment focused on surveying the effects of fertilization on the production and quality of fodder, as well as on soil quality. The experimental site is located at Závišín near Mariánské Lázně, Czech Republic (49°58′39′′N, 12°45′14′′E, altitude 750 m above sea level) and was established in 1969. The soil is a sandy loam classified as Haplic Cambisol (Dystric) (IUSS Working Group WRB, 2006). Soil characteristics, annual temperature,
Soil chemical properties and plant aboveground biomass
Long-term fertilization of grassland soil led to changes in plant aboveground biomass and almost all assessed soil chemical properties, which is shown in Table 1. Soil reaction (pHKCl) and the content of Ca were significantly higher in plots fertilized with N (80N and 160N). The increased values of pHKCl and Ca content reflect the fact that ammonium sulphate used as fertilizer in 80N and 160N plots also contained some limestone. In the case of NF plots, terminated fertilization led to the
Conclusion
We demonstrated that 40-y mineral fertilization of grassland soil had a significant effect on soil microbial communities in terms of both function and community composition. Fertilization altered the activity of selected extracellular enzymes; however, PK inputs alone, without N, did not represent a sufficient impact. Moreover, the shifts in enzyme activities were accompanied by changes in the composition of whole bacterial and fungal communities, implying a linkage between microbial community
Funding
The research was funded by the Ministry of Agriculture of the Czech Republic.
Declaration of competing interest
None.
Acknowledgements
The current owner of the study land is a private farmer Mr. Ivan Kožíšek. Thanks to his rare understanding, it is possible to maintain the field trial and to continue with monitoring of long-term fertilization.
References (58)
- et al.
Responses of extracellular enzyme activities and microbial community in both the rhizosphere and bulk soil to long-term fertilization practices in a fluvo-aquic soil
Geoderma
(2012) - et al.
Microbial biomass, enzyme activities and microbial community structure in two European long-term field experiments
Agric. Ecosyst. Environ.
(2005) - et al.
Soil enzymes in a changing environment: Current knowledge and future directions
Soil Biol. Biochem.
(2013) - et al.
Microbial and microfaunal communities in phosphorus limited, grazed grassland change composition but maintain homeostatic nutrient stoichiometry
Soil Biol. Biochem.
(2014) - et al.
Temporal variations in microbial biomass C and cellulolytic enzyme activity in arable soils: effects of organic matter input
Appl. Soil Ecol.
(1999) - et al.
Effect of 35 years inorganic fertilizer and manure amendment on structure of bacterial and archaeal communities in black soil of northeast China
Appl. Soil Ecol.
(2016) - et al.
Long-term effects of mineral fertilizers on soil microorganisms – A review
Soil Biol. Biochem.
(2014) - et al.
Soil extracellular enzyme activities, soil carbon and nitrogen storage under nitrogen fertilization: A meta-analysis
Soil Biol. Biochem.
(2016) - et al.
Influence of organic and mineral fertilisers on soil biological and physical properties
Bioresour. Technol.
(2000) - et al.
Structure and function of the soil microbial community in a long-term fertilizer experiment
Soil Biol. Biochem.
(2003)
Assessment of soil microbial functional diversity: land use and soil properties affect CLPP-MicroResp and enzymes responses
Pedobiologia
Biochemical indicators of carbon dynamic in an Acrisol cultivated under different management practices in the central Mexican highlands
Soil Tillage Res.
Changes in plant species richness and productivity in response to decreased nitrogen inputs in grassland in southern England
Ecol. Indic.
Soil amendments yield persisting effects on the microbial communities—a 7-year study
Appl. Soil Ecol.
Impact of long-term fertilization practices on the abundance and composition of soil bacterial communities in Northeast China
Appl. Soil Ecol.
How long do ecosystems take to recover from atmospheric nitrogen deposition? Biol
Conserv.
Effect of long-term nutrient managements on biological and biochemical properties of semi-arid tropical alfisol during maize crop development stages
Ecol. Indic.
Sample storage for soil enzyme activity and bacterial community profiles
J. Microbiol. Methods
Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics
Thirty four years of nitrogen fertilization decreases fungal diversity and alters fungal community composition in black soil in northeast China
Soil Biol. Biochem.
Resistance, resilience, and redundancy in microbial communities
Proc. Natl. Acad. Sci. U. S. A.
The Nature and Properties of Soils
Microbial community and functional diversity associated with different aggregate fractions of a paddy soil fertilized with organic manure and/or NPK fertilizer for 20 years
J. Soils Sediments
Controls on soil microbial community stability under climate change
Front. Microbiol.
Soil microbial responses to elevated phosphorus and pH in acidic temperate deciduous forests
Biogeochemistry
Isolation and direct complete nucleotide determination of entire genes. Characterization of a gene coding for 16S ribosomal RNA
Nucleic Acids Res.
Sulfate ester formation and hydrolysis: a potentially important yet often ignored aspect of the sulfur cycle of aerobic soils
Bacteriol. Rev.
ITS primers with enhanced specificity for basidiomycetes: application to the identification of mycorrhizae and rusts
Mol. Ecol.
Enzymes of importance to rhizosphere processes
J. Soil Sci. Plant Nutr.
Cited by (11)
Detection, production, modification, and application of arylsulfatases
2023, Biotechnology AdvancesEffect of reduced subsequent N supply and organic amendment on soil bacterial community in a wheat-maize rotation system with over-fertilization
2023, Applied Soil EcologyCitation Excerpt :First, we evaluated the response of soil physicochemical and biochemical properties to RCN and RCN + OF; then, we assessed the changes in alpha and beta diversities of soil bacterial community after receiving RCN and RCN + OF and last, we explored the changes in interactions of taxa within bacterial community under RCN and OF via co-occurrence network analysis. This study focused on bacterial microbiome since soil bacteria have been revealed to be more resilient to chemical fertilization disturbances than fungi (Čuhel et al., 2019). We hypothesized that: (1) RCN could improve diversity and structure of bacterial microbiome in over-fertilized soil because it has been indicated that negative changes in soil microbiota over elevated N input are involved in decreased soil pH and soil N enrichment (Lu et al., 2021; Ren et al., 2020; Yang et al., 2021; Zeng et al., 2016); and (2) incorporating OF could further affect bacterial microbiome while a stronger influence on bacterial microbiome was from RCN rather than OF, since the influence of organic amendment on soil physicochemical properties is usually a slow process and therefore, probably releases a more modest impact on soil microbes relative to chemical fertilization (Chen et al., 2017; M.L. Zhang et al., 2021).
Changes in litter input exert divergent effects on the soil microbial community and function in stands of different densities
2022, Science of the Total EnvironmentCitation Excerpt :Although, as described above, research on the effects of a single factor or a few two-factor treatments on the soil microbial community is relatively adequate, it remains largely unknown whether litter removal or different amounts of litter input have the same degree of effect on soil microbial communities at different densities of the forest. Changes in microbial communities are often accompanied by changes in their functions, such as soil enzyme activity and respiration (Čuhel et al., 2019). Extracellular enzymes are crucial in regulating decomposition and nutrient cycling (Sinsabaugh, 1994; Song et al., 2014).
Nitrogen enrichment affects soil enzymatic stoichiometry via soil acidification in arid and hot land
2020, PedobiologiaCitation Excerpt :Secondly, we found that soil microbial community structures partly mediated the effects of soil pH on enzymatic stoichiometries. Soil microbial community structures are sensitive to soil pH variations (Chen et al., 2013, 2016; Rousk et al., 2010) and play important roles in regulating enzyme activities (Čuhel et al., 2019; Luo et al., 2018; Tischer et al., 2015; Trivedi et al., 2016), therefore mediate the effects of soil acidification on enzymatic stoichiometries. Ln(AP):ln(NAG), ln(LAP):ln(NAG) and ln(BG):ln(NAG) were positively related to fungi:bacterial ratios and GN:GP ratios, indicating that NAG activities (compared to other enzyme activities) decreased with the increases in fungi:bacterial ratios and GN:GP ratios.
No-tillage participatory quality index reflects the condition of soil management
2023, Revista Ciencia AgronomicaSoil Microbiome Study Based on DNA Extraction: A Review
2022, Water (Switzerland)