Effects of long-term nitrogen addition on soil fungal communities in two temperate plantations with different mycorrhizal associations
Introduction
Nitrogen (N) deposition is expected to continuously increase in the future (Galloway et al., 2008), which may substantially influence both above- and below-ground processes in forest ecosystems (Frey et al., 2004; Weand et al., 2010). Exogenous N inputs are likely to eliminate the potential N limitation, but also result in soil acidification, which may contribute to the leaching of base cations and mobilization of Al3+ (Meng et al., 2019; Treseder, 2008). Soil N availability and pH are the important drivers of the diversity and structure of fungal communities (Zhang et al., 2016; Ren et al., 2017). Increase in N availability and soil acidification consequently are thought to be major paths of N addition effects on fungal communities (Meng et al., 2019; Treseder, 2008). Ecosystems from different locations and climate conditions suffer from different levels of N limitation (Du et al., 2020), and thus have different buffer capacities in response to N-induced soil acidification (Meng et al., 2019). However, few long-term experiments focused on the effects of N addition on soil fungal diversity in forest ecosystems (Wang et al., 2018).
Almost all terrestrial plants form symbiotic associations with mycorrhizal fungi, of which the major mycorrhizal types are arbuscular mycorrhiza (AM) and ectomycorrhiza (EcM) (van der Heijden et al., 2015; Xiao et al., 2019). AM-associated plants often dominate in tropical and subtropical regions, while EcM-associated plants commonly dominate in temperate and boreal forests (van der Heijden et al., 2015; Lin et al., 2017). AM-dominated forests are suggested to have higher leaf litter quality, faster litter decomposition rate, higher nitrification rates, and faster nutrients cycling rates than EcM-dominated forests (Read and Perez-Moreno, 2003; Lin et al., 2017). Mycorrhizal fungi have exclusive access to recently fixed plant carbon (C) and can shift the structure of fungal communities through the competition for nutrients with other saprotrophic fungi, i.e., the “Gadgil effect” (Fernandez and Kennedy, 2016). Therefore, forest ecosystems with different mycorrhizal types may have different responses to N addition (Thomas et al., 2010; Boggs et al., 2005; Phillips et al., 2013; Lin et al., 2017). However, we know little about the responses of soil fungal communities to N addition in forests with contrasting mycorrhizal associations especially on the long term.
Soil fungi are important decomposer in terrestrial ecosystems, and typically dominate the decomposition of recalcitrant C like lignin (Zechmeister-Boltenstern et al., 2015; Li et al., 2017). Fungal communities, especially most basidiomycetes and many ascomycetes, widely produce phenol oxidase and peroxidase in soils (Kellner et al., 2009; Sinsabaugh, 2010). Phenol oxidase oxidizes phenols using oxygen, while peroxidase oxidizes aromatic and aliphatic hydrocarbons using peroxide (Sinsabaugh et al., 2008). Therefore, these enzymes mediate key ecosystem functions of lignin degradation, humification, and C mineralization (Sinsabaugh, 2010). Mycorrhizal associations also influence the activities of phenol oxidase and peroxidase. For example, Lauber et al. (2009) found that about 55% of the soil laccase, the largest class of phenol oxidases in soils, was associated with EcM fungi. However, it is unclear how N addition affects the activities of phenol oxidase and peroxidase through the adjustment of the fungal communities in forests with contrasting mycorrhizal associations.
Dahurian larch (Larix gmelinii) and Manchurian ash (Fraxinus mandshurica) are major tree species in the natural forests and the key commercial plantations in Northeast China, which have contrasting eco-physiological characteristics (e.g., coniferous vs. broadleaved, and EcM vs. AM). A study at the same site based on a common garden experiment (Wang and Wang, 2018) reported that larch stand has lower litter quality, soil respiration rate, root and microbial biomass, and greater C stock in the forest floor than ash stand does; but we do not know how soil microbial communities in these stands respond to N deposition. In this study, we used a 16-year N-addition experiment in the monoculture plantations of Dahurian larch and Manchurian ash to investigate the responses of soil fungal diversity, community composition, and functions to long-term N addition. We will address the following questions: (1) Do the soil fungal communities in the larch and ash plantations with different mycorrhizal associations have different sensitivities in response to N addition? (2) How does N addition affect the fungal communities, through increasing N availability vs. soil acidification? (3) Does the N-induced shift in fungal communities affect the decomposition of lignin?
Section snippets
Description of site and N-addition experiment
This study was conducted at the Maoershan Forest Ecosystem Research Station, Heilongjiang Province, Northeast China (45°20′ N, 127°30′ E). The climate is continental monsoon climate with a windy and dry spring, a warm and humid summer, and a dry and cold winter. The mean annual temperature is 2 °C, and the mean January (the coldest month) and July (the warmest month) temperatures are −20.7 °C and 20.5 °C, respectively. The mean annual precipitation is 702 mm, and 81% of the rainfall falls
Results
The two-way ANOVA showed that tree species and N-addition treatment significantly (P < 0.05) influenced soil inorganic N concentrations (Table 1). In specific, NH4+-N and NO3−-N in ash stand were 56% and 67% greater than those in larch stand, and those in N-addition treatment were 91% and 80% greater than those in control, respectively. N addition significantly reduced soil pH (P < 0.001), and the activities of phenol oxidase (P = 0.003) and peroxidase (P = 0.021). Tree species and treatment
Long-term N addition has little effect on fungal diversity
We found that the 16-year N addition had no significant effect on the fungal alpha diversity in both larch and ash plantations (Fig. 1), which is in agreement with a recent study of two tropical montane rainforests in Hainan Island, China (Li et al., 2019). However, some previous studies reported a negative response of microbial alpha diversity to N addition and attributed it to soil acidification (Zhang et al., 2011; He et al., 2016; Zhou et al., 2016). A global meta-analysis (Wang et al., 2018
Declaration of competing interest
The current manuscript represents an original work that has not been published previously, and the authors declared that there is no conflict of interest.
Acknowledgments
We thank Professor Zhengquan Wang for the setting of the long-term N addition experiments. This work was financially supported by the National Natural Science Foundation of China (31901278), the National Key Research and Development Program of China (2016YFD0600201), and the Young Elite Scientists Sponsorship Program by China Association for Science and Technology (2018QNRC001). The Heilongjiang Maoershan Forest Ecosystem National Observation and Research Station provided field logistic support
References (57)
- et al.
Labile, recalcitrant, and microbial carbon and nitrogen pools of a tallgrass prairie soil in the US Great Plains subjected to experimental warming and clipping
Soil Biol. Biochem.
(2009) - et al.
Consistent responses of surface- and subsurface soil fungal diversity to N enrichment are mediated differently by acidification and plant community in a semi-arid grassland
Soil Biol. Biochem.
(2018) - et al.
Nitrogen addition alters ectomycorrhizal fungal communities and soil enzyme activities in a tropical montane forest
Fung. Ecol.
(2017) - et al.
Chronic nitrogen enrichment affects the structure and function of the soil microbial community in temperate hardwood and pine forests
For. Ecol. Manag.
(2004) - et al.
Responses of rhizosphere soil properties, enzyme activities and microbial diversity to intercropping patterns on the Loess Plateau of China
Soil Tillage Res.
(2019) - et al.
Soil extracellular enzyme activities, soil carbon and nitrogen storage under nitrogen fertilization: a meta-analysis
Soil Biol. Biochem.
(2016) - et al.
Contrasting responses of hydraulic traits between leaf and branch to 16-year nitrogen addition in a larch plantation
For. Ecol. Manag.
(2020) - et al.
Temporal changes in diversity and expression patterns of fungal laccase genes within the organic horizon of a brown forest soil
Soil Biol. Biochem.
(2009) - et al.
Linking soil fungal community structure and function to soil organic carbon chemical composition in intensively managed subtropical bamboo forests
Soil Biol. Biochem.
(2017) - et al.
Chronic nitrogen additions fundamentally restructure the soil fungal community in a temperate forest
Fungal Ecol.
(2016)
FUNGuild: an open annotation tool for parsing fungal community datasets by ecological guild
Fungal Ecol.
Tree species influence on microbial communities in litter and soil: current knowledge and research needs
For. Ecol. Manag.
Phenol oxidase, peroxidase and organic matter dynamics of soil
Soil Biol. Biochem.
Composition of fungal and bacterial communities in forest litter and soil is largely determined by dominant trees
Soil Biol. Biochem.
Biomass allometric equations for 10 co-occurring tree species in Chinese temperate forests
For. Ecol. Manag.
Mycorrhizal associations differentiate soil respiration in five temperate monocultures in Northeast China
For. Ecol. Manag.
Decreasing soil microbial diversity is associated with decreasing microbial biomass under nitrogen addition
Soil Biol. Biochem.
Effects of tree species and N additions on forest floor microbial communities and extracellular enzyme activities
Soil Biol. Biochem.
Effects of re-vegetation type and arbuscular mycorrhizal fungal inoculation on soil enzyme activities and microbial biomass in coal mining subsidence areas of Northern China
Catena
Thirty four years of nitrogen fertilization decreases fungal diversity and alters fungal community composition in black soil in northeast China
Soil Biol. Biochem.
Patterns and mechanisms of responses by soil microbial communities to nitrogen addition
Soil Biol. Biochem.
Effects of thinning on soil saprotrophic and ectomycorrhizal fungi in a Korean larch plantation
For. Ecol. Manag.
The UNITE database for molecular identification of fungi–recent updates and future perspectives
New Phytol.
Differential sensitivity of total and active soil microbial communities to drought and forest management
Glob. Chang. Biol.
Tree growth, foliar chemistry, and nitrogen cycling across a nitrogen deposition gradient in southern Appalachian deciduous forests
Can. J. For. Res.
Integrating plant litter quality, soil organic matter stabilization, and the carbon saturation concept
Glob. Chang. Biol.
The Microbial Efficiency-Matrix Stabilization (MEMS) framework integrates plant litter decomposition with soil organic matter stabilization: do labile plant inputs form stable soil organic matter?
Glob. Chang. Biol.
It is elemental: soil nutrient stoichiometry drives bacterial diversity
Environ. Microbiol.
Cited by (4)
Globally nitrogen addition alters soil microbial community structure, but has minor effects on soil microbial diversity and richness
2023, Soil Biology and BiochemistryEffects of Achnatherum inebrians ecotypes and endophyte status on plant growth, plant nutrient, soil fertility and soil microbial community
2022, Soil Science Society of America Journal