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Significant Alterations in Soil Fungal Communities Along a Chronosequence of Spartina Alterniflora Invasion in a Chinese Yellow

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Significant Alterations in Soil Fungal Communities Along a Chronosequence of Spartina Alterniflora Invasion in a Chinese Yellow Science of the Total Environment 693 (2019) 133548 Contents lists available at ScienceDirect Science of the Total Environment journal homepage: www.elsevier.com/locate/scitotenv Significant alterations in soil fungal communities along a chronosequence of Spartina alterniflora invasion in a Chinese Yellow Sea coastal wetland Wen Yang a,⁎,DiZhanga,XinwenCaia,LuXiab,YiqiLuoc,XiaoliChengd,⁎⁎, Shuqing An b a College of Life Sciences, Shaanxi Normal University, Xi'an 710119, PR China b School of Life Science and Institute of Wetland Ecology, Nanjing University, Nanjing 210023, PR China c Center for Ecosystem Science and Society (Ecoss), Department of Biological Sciences, Northern Arizona University, Flagstaff, AZ 86011, USA d Key Laboratory of Aquatic Botany and Watershed Ecology, Wuhan Botanical Garden, Chinese Academy of Sciences, Wuhan 430074, PR China HIGHLIGHTS GRAPHICAL ABSTRACT • S. alterniflora invasion altered soil fungal abundance, diversity and composition. • The fungal abundance and diversity were highest in 9-year-old S. alterniflora soil. • Basidiomycota was gradually replaced by Ascomycetes along S. alterniflora in- vasion. • S. alterniflora invasion greatly shifted fungal trophic modes and functional groups. • Soil fungal communities were driven by plant and soil properties, nutrient substrate. article info abstract Article history: Plant invasion typically alters the microbial communities of soils, which affects ecosystem carbon (C) and nitro- Received 3 May 2019 gen (N) cycles. The responses of the soil fungal communities to plant invasion along its chronosequence remain Received in revised form 22 July 2019 poorly understood. For this study, we investigated variations in soil fungal communities through Illumina MiSeq Accepted 22 July 2019 sequencing analyses of the fungal internal transcribed spacer (ITS) region, and quantitative polymerase chain re- Available online 23 July 2019 action (qPCR), along a chronosequence (i.e., 9-, 13-, 20- and 23-year-old) of invasive Spartina alterniflora.We fl Editor: Sergi Sabater compared these variations with those of bare at in a Chinese Yellow Sea coastal wetland. Our results highlighted that the abundance of soil fungi, the number of operational taxonomic units (OTUs), species richness, and Shan- Keywords: non diversity indices for soil fungal communities were highest in 9-year-old S. alterniflora soil, which gradually Carbon sequestration declined along the invasion chronosequence. The relative abundance of copiotrophic Basidiomycota revealed sig- Coastal salt marshes nificant decreasing trend, while the relative abundance of oligotrophic Ascomycota gradually increased along the Exotic plants S. alterniflora invasion chronosequence. The relative abundance of soil saprotrophic fungi (e.g., undefined Fungal functional guilds saprotrophs) was gradually reduced while symbiotic fungi (e.g., ectomycorrhizal fungi) and pathotrophic fungi Fungal trophic modes (e.g., plant and animal pathogens) progressively increased along the S. alterniflora invasion chronosequence. Soil fungal community composition Abbreviations: ACE, Abundance-based coverage estimator; AMF, Arbuscular mycorrhizal fungi; ANOVA, Analysis of variance; C, Carbon; C:N ratio, Carbon: Nitrogen ratio; Chao1, Chao's species richness estimator; ECM, Ectomycorrhizal; ITS, Internal transcribed spacer; N, Nitrogen; NMDS, Non-metric multidimensional scaling; OTUs, Operational taxonomic units; PCoA, Principal coordinates analysis; QIIME, Quantitative insights into microbial ecology; qPCR, Quantitative polymerase chain reaction; RDA, Redundancy analysis; RDP, Ribosomal database project; Shannon, Shannon's diversity index; SOC, Soil organic carbon; SOM, Soil organic matter; SON, Soil organic nitrogen; WSOC, Water-soluble organic carbon. ⁎ Correspondence to: W. Yang, College of Life Sciences, Shaanxi Normal University, No. 620 West Chang'an St., Chang'an Dist., Xi'an 710119, Shaanxi, PRChina. ⁎⁎ Correspondence to: X. Cheng, Key Laboratory of Aquatic Botany and Watershed Ecology, Wuhan Botanical Garden, The Chinese Academy of Sciences, Wuhan 430074, PR China. E-mail addresses: [email protected] (W. Yang), [email protected] (X. Cheng). https://doi.org/10.1016/j.scitotenv.2019.07.354 0048-9697/© 2019 Elsevier B.V. All rights reserved. 2 W. Yang et al. / Science of the Total Environment 693 (2019) 133548 Our results suggested that S. alterniflora invasion significantly altered soil fungal abundance and diversity, com- munity composition, trophic modes, and functional groups along a chronosequence, via substantially reduced soil litter inputs, and gradually decreased soil pH, moisture, and soil nutrient substrates along the invasion chronosequence, from 9 to 23 years. These changes in soil fungal communities, particularly their trophic modes and functional groups along the S. alterniflora invasion chronosequence could well impact the decompo- sition and accumulation of soil C and N, while potentially altering ecosystem C and N sinks in a Chinese Yellow Sea coastal wetland. © 2019 Elsevier B.V. All rights reserved. 1. Introduction is added to the soil (Bachelot et al., 2016). The physicochemical proper- ties of soils (e.g., soil pH, and moisture) have been implicated as one of Plant invasion is an emerging driver of global change (Craig et al., the essential driving factors in soil fungal communities (Leff et al., 2015), which threatens natural habitats (Bazzichetto et al., 2018), alters 2015). For instance, soil pH is considered to be one of the most vital in- species compositions (Carboni et al., 2018), ecosystem processes, and fluential predictors of soil fungal communities (Geml et al., 2014; Hu their functions (Craig et al., 2015; Stefanowicz et al., 2016; Carboni et al., 2017). Maestre et al. (2015) observed that the abundance and di- et al., 2018). These shifts in plant communities, induced by plant inva- versity of soil fungi decrease with a decreasing soil pH. Further, the qual- sion, may considerably alter net primary production (Stefanowicz ity and quantity of soil nutrient substrates have been reported to modify et al., 2016), soil nutrient inputs (e.g., invasive plant litter and exudates) soil fungal communities (Lauber et al., 2008; Peay et al., 2013), as most and decomposition (Liao et al., 2007), as well as soil characteristics soil fungi are saprophytes (Zimudzi et al., 2018). Geml et al. (2014) re- (Stefanowicz et al., 2016). These changes further modify nutrient fluxes vealed that the soil fungal communities were closely associated with and biogeochemical cycles (Turpin-Jelfs et al., 2019), particularly eco- soil organic carbon (SOC), N content, and C:N ratio. Previous studies re- system carbon (C) and nitrogen (N) cycles (Craig et al., 2015; Lee vealed that invasive plant species greatly modified the characteristics of et al., 2018). Meanwhile, soil microbes play a critical role in the regula- plant litter (Liao et al., 2007), soil physicochemical properties (Yang tion of ecosystem C and N cycles through the decomposition of various et al., 2016, 2019), and soil organic C and N sequestration (Wolkovich organic detritus, while controlling soil organic matter (SOM) turnover et al., 2010; Lee et al., 2018). The identification of biotic and abiotic fac- and formation (Morris and Blackwood, 2015; Yang et al., 2016). Al- tors that drive variations in soil fungal communities will help better un- though the impacts of plant invasion on ecosystem C and N cycles derstand the influential mechanisms of invasive plants on the have been extensively reported (Liao et al., 2008; Wolkovich et al., abundance of soil fungi, as well as their diversity, community composi- 2010; Lee et al., 2018), the elucidation of soil microbial communities re- tion, trophic modes, and functional groups. sponses to plant invasion remains limited (Lazzaro et al., 2018). Spartina alterniflora (a perennial grass), which is native to North Plant invasion has been demonstrated to alter the abundance and di- America, was introduced to China in 1979 to accelerate sedimentation versity of plant and animal communities (Stefanowicz et al., 2019), as and the stabilization of tidal flat lands. Subsequently, S. alterniflora rap- well as soil nutrient substrates (Yang et al., 2016). Further, it eventually idly expanded across the eastern coast of China, from Tianjin (in the modifies the biomass, composition, and structures of soil microbial north) to Beihai (in the south), by invading bare flat and/or by replacing communities (Stefanowicz et al., 2019). Recently, the responses of soil native plants (e.g., Suaeda salsa, Phragmites australis,andScirpus bacterial communities to plant invasion have been extensively docu- mariqueter)(Liao et al., 2007; Yang et al., 2016). It has since become mented (Piper et al., 2015; Rodríguez-Caballero et al., 2017; Xiang one of the dominant plants in China's coastal wetlands (Yang et al., et al., 2018). In contrast, the impacts of plant invasion on soil fungal 2017). The Jiangsu coast has the greatest S. alterniflora distribution communities have not been well addressed (Li et al., 2017; Phillips area in China (Yang et al., 2015). S. alterniflora has been demonstrated et al., 2019). Soil fungi are among the most abundant and diverse taxo- to have unique ecophysiological properties relative to native plants, nomic groups on the earth (Egidi et al., 2019), and comprise diverse such as higher growth rate, greater net primary production, and higher groups of eukaryotic microorganisms that form essential component salt tolerance (Liao et al., 2007). Moreover,
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