Soil fungal communities vary with invasion by the exotic Spartina alternifolia Loisel. in coastal salt marshes of eastern China
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Soil fungal communities play a critical role in ecosystem carbon (C) and nitrogen (N) cycling. Although the effect of plant invasions on ecosystem C and N cycling is well established, its impact on soil fungal communities is not fully understood. The objective of this study was therefore to understand the variations in soil fungal communities as affected by plant invasion, and the mechanisms that drive these changes.
We examined the impacts of invasive Spartina alternifolia Loisel. (SA) on soil fungal abundance, diversity, community composition, trophic modes and functional groups in comparison with bare flat (BF) and native Suaeda salsa (Linn.) Pall. (SS), Scirpus mariqueter Tang et Wang (SM), and Phragmites australis (Cav.) Trin. ex Steud. (PA) communities in coastal salt marshes of eastern China, based on analyses of the quantitative polymerase chain reaction (qPCR) and Illumina MiSeq DNA sequences of fungal internal transcribed spacer (ITS) region.
SA invasion increased the soil fungal abundance and diversity compared to BF, SS, SM, and PA soils. The increased soil fungal abundance and diversity were highly related to soil organic carbon (C) and nitrogen (N), water-soluble organic carbon (WSOC), litter C:N ratio, and root C:N ratio. Soil fungal community composition was shifted following SA invasion. Specifically, SA invasion significantly enhanced the relative abundance of Basidiomycota, and reduced the relative abundance of Ascomycota compared with BF, SS, SM, and PA soils. Additionally, SA invasion changed soil fungal trophic modes and functional groups. The relative abundance of saprotrophic fungi significantly increased, while the relative abundances of symbiotic and pathotrophic fungi decreased following SA invasion.
Our data revealed that SA invasion altered soil fungal abundance, diversity, community composition, trophic modes and functional groups, which were primarily driven by the quality and quantity of plant residues, soil nutrition substrates, as well as soil physicochemical properties. The changes in soil fungal communities, especially their trophic modes and functional groups following SA invasion would greatly affect soil C and N decomposition and accumulation with potential feedback on climate change.
KeywordsCoastal wetland Fungal functional groups Illumina MiSeq DNA sequencing Plant invasions Soil carbon and nitrogen sequestration Soil fungal community composition
Abundance-based coverage estimator
Arbuscular mycorrhizal fungi
Analysis of variance
Chao’s species richness estimator
- C:N ratio
Carbon: Nitrogen ratio
Internal transcribed spacer
Operational taxonomic units
Phragmites australis (Cav.) Trin. ex Steud.
Principal coordinates analysis
Quantitative insights into microbial ecology
Quantitative polymerase chain reaction
Ribosomal database project
Spartina alternifolia Loisel.
Shannon’s diversity index
Scirpus mariqueter Tang et Wang
Soil organic carbon
Soil organic matter
Soil organic nitrogen
Suaeda salsa (Linn.) Pall.
Water-soluble organic carbon
This study was supported by the National Natural Science Foundation of China (grant no. 31600427), Fundamental Research Funds for the Central Universities (grant no. GK201803042), China Scholarship Council (grant no. 201806875004), Research Startup fund of Shaanxi Normal University (grant no.1000951110010899), and the China Postdoctoral Science Foundation (grant no. 2016 M590440). We thank the whole staff of the Jiangsu Yancheng Wetland National Nature Reserve for Rare Birds for supporting and helping in this research. We also appreciate two anonymous reviewers and editor for their insightful comments and valuable suggestions on this paper.
- Abarenkov K, Henrik Nilsson R, Larsson K-H, Alexander IJ, Eberhardt U, Erland S, Høiland K, Kjøller R, Larsson E, Pennanen T, Sen R, Taylor AFS, Tedersoo L, Ursing BM, Vrålstad T, Liimatainen K, Peintner U, Kõljalg U (2010) The UNITE database for molecular identification of fungi—recent updates and future perspectives. New Phytol 186:281–285CrossRefPubMedGoogle Scholar
- Chao A (1984) Non-parametric estimation of the number of classes in a population. Scand J Stat 11:265–270Google Scholar
- Chen J, Xu H, He D, Li YD, Luo TS, Yang HG, Lin MX (2019) Historical logging alters soil fungal community composition and network in a tropical rainforest. Forest Ecol Manag 433:228–239Google Scholar
- Chen YL, Xu TL, Veresoglou SD, Hu HW, Hao ZP, Hu YJ, Liu L, Deng Y, Rillig MC, Chen BD (2017) Plant diversity represents the prevalent determinant of soil fungal community structure across temperate grasslands in northern China. Soil Biol Biochem 110:12–21Google Scholar
- Guo JJ, Liu WB, Zhu C, Luo GW, Kong YL, Ling N, Wang M, Dai JY, Shen QR, Guo SW (2018) Bacterial rather than fungal community composition is associated with microbial activities and nutrient-use efficiencies in a paddy soil with short-term organic amendments. Plant Soil 424:335–349CrossRefGoogle Scholar
- Krogius-Kurikka L, Lyra A, Malinen E, Aarnikunnas J, Tuimala J, Paulin L, Mäkivuokko H, Kajander K, Palva A (2009) Microbial community analysis reveals high level phylogenetic alterations in the overall gastrointestinal microbiota of diarrhoea-predominant irritable bowel syndrome sufferers. BMC Gastroenterol 9:95CrossRefPubMedPubMedCentralGoogle Scholar
- Lee MR, Bernhardt ES, van Bodegom PM, Cornelissen JHC, Kattge J, Laughlin DC, Niinemets Ü, Peñuelas J, Reich PB, Yguel B, Wright JP (2017) Invasive species’ leaf traits and dissimilarity from natives shape their impact on nitrogen cycling: a meta-analysis. New Phytol 213:128–139CrossRefPubMedGoogle Scholar
- Rodríguez-Caballero G, Caravaca F, Alguacil MM, Fernández-López M, Fernández-González AJ, Roldán A (2017) Striking alterations in the soil bacterial community structure and functioning of the biological N cycle induced by Pennisetum setaceum invasion in a semiarid environment. Soil Biol Biochem 109:176–187CrossRefGoogle Scholar
- Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sahl JW, Stres B, Thallinger GG, van Horn DJ, Weber CF (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541CrossRefPubMedPubMedCentralGoogle Scholar
- Sun RB, Dsouza M, Gilbert JA, Guo XS, Wang DZ, Guo ZB, Ni YY, Chu HY (2016) Fungal community composition in soils subjected to long-term chemical fertilization is most influenced by the type of organic matter. Environ Microbiol 18:5137–5150Google Scholar
- Sun RB, Zhang XX, Guo XS, Wang DZ, Chu HY (2015) Bacterial diversity in soils subjected to long-term chemical fertilization can be more stably maintained with the addition of livestock manure than wheat straw. Soil Biol Biochem 88:9–18Google Scholar
- ter Braak CJF, Smilauer P (2002) CANOCO reference manual and CanoDraw for windows user’s guide: software for canonical ordination (version 4.5). Microcomputer Power, IthacaGoogle Scholar
- Walker GM, White NA (2011) Introduction to fungal physiology. In: Kavanagh K (ed) Fungi: biology and applications, 2nd edn. Wiley, Chichester, pp 1–35Google Scholar
- Wang M, Shi S, Lin F, Jiang P (2014) Response of the soil fungal community to multi-factor environmental changes in a temperate forest. Appl Soil Ecol 81:45–56Google Scholar
- Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73:5261–5267Google Scholar
- White TJ, Bruns T, Lee SB, Taylor JW (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR protocols: a guide to methods and applications. Academic Press, San Diego, pp 315–322Google Scholar
- Yang W, An SQ, Zhao H, Fang SB, Xia L, Qiao YJ, Cheng XL (2015) Labile and recalcitrant soil carbon and nitrogen pools in tidal salt marshes of the eastern Chinese coast as affected by short-term C4 plant Spartina alterniflora invasion. Clean–Soil, Air, Water 43:872–880Google Scholar
- Yang W, Jeelani N, Zhu ZH, Luo YQ, Cheng XL, An SQ (2019) Alterations in soil bacterial community in relation to Spartina alterniflora Loisel. invasion chronosequence in the eastern Chinese coastal wetlands. Appl Soil Ecol 135:38–43Google Scholar
- Yang W, Zhao H, Chen XL, Yin SL, Cheng XL, An XQ (2013) Consequences of short-term C4 plant Spartina alterniflora invasions for soil organic carbon dynamics in a coastal wetland of eastern China. Ecol Eng 61:50–57Google Scholar
- Zak DR, Pellitier PT, Argiroff WA et al (2019) Exploring the role of ectomycorrhizal fungi in soil carbon dynamics. New Phytol. https://doi.org/10.1111/nph.15679