Elsevier

Applied Soil Ecology

Volume 168, December 2021, 104111
Applied Soil Ecology

Effects of long-term nitrogen addition on soil fungal communities in two temperate plantations with different mycorrhizal associations

https://doi.org/10.1016/j.apsoil.2021.104111Get rights and content

Highlights

  • N addition changes fungal structure at OTU level, but not at phylum level.

  • Fungal structure of ash soil was more sensitive to N input than that of larch soil.

  • N availability explains more variances of fungal structure than pH.

  • N addition reduces ligninolytic capability by adjusting fungal structure.

Abstract

Forests are profoundly influenced by the rapid increase in nitrogen (N) deposition. Fungal communities dominate the decomposition of recalcitrant carbon (C) in soils, but it is still unclear how fungal communities respond to N addition in forests with different mycorrhizal associations. Here, we used the high-throughput sequencing methods to examine the effects of 16-year N addition on fungal diversity and community structure in two plantations, i.e., Dahurian larch (Larix gmelinii) associated with ectomycorrhiza and Manchurian ash (Fraxinus mandshurica) associated with arbuscular mycorrhiza, in Northeast China. We found that fungal alpha diversity was comparable between the two plantations and responded insignificantly to N addition. The permutational multivariate analysis of variance demonstrated that the fungal community structure was significantly affected by tree species, while N addition altered the fungal community structure in ash stand but had little effect on it in larch stand. The distance-based redundancy analysis further revealed that N addition regulated the fungal community structure dominantly by increasing N availability, while tree species influenced it mainly by altering soil labile C fractions. In addition, the fungal community structure was correlated with the activity of phenol oxidase. Overall, the effects of N addition on soil fungal communities in the forest ecosystems are tree species-specific, and N addition may decrease the ligninolytic capability through adjusting the fungal community structure.

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

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