Spartina alterniflora invasions reduce soil fungal diversity and simplify co-occurrence networks in a salt marsh ecosystem

https://doi.org/10.1016/j.scitotenv.2020.143667Get rights and content

Highlights

  • Spartina alterniflora invasion significantly decreased soil fungal richness.

  • The fungal community became more homogenized with the invasion.

  • Soil pH and salinity were the shaping factors in the fungal community structure.

  • The fungal co-occurrence network was simplified with the invasion.

  • Saprotrophic fungi were increased but pathotroph were suppressed with invasion.

Abstract

Soil fungal communities drive diverse ecological processes and are critical in maintaining ecosystems' stability, but the effects of plant invasion on soil fungal diversity, community composition, and functional groups are not well understood. Here, we investigated soil fungal communities in a salt marsh ecosystem with both native (Suaeda salsa) and exotic (Spartina alterniflora) species in the Yellow River Delta. We characterized fungal diversity based on the PCR-amplified Internal Transcribed Spacer 2 (ITS2) DNA sequences from soil extracted total DNA. The plant invasion evidently decreased fungal richness and phylogenetic diversity and significantly altered the taxonomic community composition (indicated by the permutation test, P < 0.001). Co-occurrence networks between fungal species showed fewer network links but were more assembled because of the high modularity after the invasion. As indicated by the fungal Bray-Curtis and weighted UniFrac distances, the fungal community became homogenized with the invasion. FUNGuild database analyses revealed that the invaded sites had a higher proportion of saprophytic fungi, suggesting higher organic matter decomposition potential with the invasion. The plant invasion dramatically inhibited the growth of pathogenic fungi, which may facilitate the expansion of invasive plants in the intertidal habitats. Soil pH and salinity were identified as the most important edaphic factors in shaping the fungal community structures in the context of Spartina alterniflora invasion. Overall, this study elucidates the linkage between plant invasion and soil fungal communities and poses potential consequences for fungal contribution to ecosystem function, including the decomposition of soil organic substrates.

Introduction

Plant invasions are among the most important emerging drivers of ecosystem successions across the world because of globalization and other human-induced environmental changes (Sardans et al., 2017). As a consequence, profound effects on belowground soil microbial communities and the ecosystem processes in which they participate have already been indicated in different ecosystems (Broz et al., 2007; Bradford et al., 2014; Fahey et al., 2020). For instance, soil nitrification rate was altered by the changed soil nitrifying community with the exotic grass invasion (Hawkes et al., 2005). In addition, different fractions of soil microbial communities exhibited distinct responses to plant invasion (Elgersma and Ehrenfeld, 2011). Therefore, to predict the consequences of exotic plant invasions on ecosystems functioning, a better understanding of the interactions between invasive plants and the resident soil microbial community is needed (Graham et al., 2016).

In soil, fungal communities are a quantitatively important microbial group, which maintains the ecosystem balance by contributing to the decomposing soil organic matter and promoting plant growth by facilitating their access to nutrients (Miransari, 2010; Banerjee et al., 2016). They may also act as plant pathogens or, on the contrary, protect the plant against them (Egidi et al., 2019). Due to their close relationship with plants, there is increasing interests in evaluating the response of soil fungal community to exotic plant invasions (Broz et al., 2007; Lekberg et al., 2013) and feedbacks from intrinsic soil fungal communities for plant invasion success (Xiao et al., 2014; Dawson and Schrama, 2016). Invasive grasses (Bromus diandrus and Avena fatua) may lower fungal richness and change the abundance of specific fungal species (such as arbuscular mycorrhizal fungi, AM fungi), which may increase their access to soil nutrients more efficiently than the native plants (Phillips et al., 2019). In contrast, studies with temperate forests revealed an increase in soil fungal community diversity under the invasion with Impatiens glandulifera (Gaggini et al., 2018). Altered fungal communities can even become beneficial to the successful invasions of an exotic plant (Bunn et al., 2015), as shown with Centaurea maculosa acquiring more soil phosphorus in response to changed AM fungi than native grasses (Callaway et al., 2004).

The driving forces of soil fungal diversity and community composition with plant invasion can be a complex result of various active environmental filters and previous land-use history (Zhang et al., 2017a). The importance of environmental filters as drivers may vary with the studied ecosystem types, invasive plant species, and spatiotemporal scales. At the regional scale, environmental filtering was found to being more important than dispersal limitation in structuring soil fungal communities (Kivlin et al., 2014; Zeng et al., 2019). Generally, it is worthy to consider and distinguish the potential activity of soil fungi in order to understand their ecological pattern. All soil fungi are heterotrophic organisms, but they can be divided into three functional groups based on their trophic strategy: (i) pathotroph, (ii) symbiotroph, and (iii) saprotroph (Tedersoo et al., 2014; Nguyen et al., 2016). Pathotrophic fungi may be enriched after plant invasion, thus causing diseases to the native plant, and thereby enhancing the exotic plant invasiveness (Inderjit and van der Putten, 2010). In addition, plant invasion can contribute to releasing fungal pathogens in soils and promoting the establishment of invasive plants (Reinhart et al., 2010). Symbiotrophic fungi (e.g., AM fungi) can provide invasive host-plants with nutrients in exchange for carbon source for their growth (Phillips et al., 2019). Saprotrophic fungi mainly act as organic matter decomposers in soils and regulate carbon and nitrogen flow, which can retain and re-allocate nutrients within their mycelium, and are thereby able to overcome the local nutrient limitation in soils (Boberg et al., 2014; Kyaschenko et al., 2017). Overall, it can be expected that changes in plant-derived carbon sources, as it would occur with an invasive plant can result in the alternation of any of these three soil fungal functional groups.

Fungi may also exhibit quite different preferences for specific edaphic conditions, as determined by soil texture, pH, salinity, and nutrient levels. Previous studies documented that soil nutrient status was the best predictor in determining soil fungal community along a small-scale elevational gradient of alpine tundra (Ni et al., 2018), and a similar result was found in a study across different land-use types (Lauber et al., 2008). Under other environmental conditions and ecosystem properties, soil pH was found as a key underlying driver of soil fungal community composition, e.g. in an Arctic tundra soil (Zhang et al., 2016), in boreal forests after wildfire disturbance (Day et al., 2019), in Andean Yungas forests along an altitudinal gradient (Geml et al., 2014), or even across biomes at a global scale (Tedersoo et al., 2014). Considering conditions as they exist in coastal ecosystems, e.g., mangroves salinity could be an essential environmental filter in shaping rhizosphere fungal community composition (Vanegas et al., 2019).

Coastal ecosystems provide multiple ecological services including mitigation of climate change, biodiversity conservation, sediment and nutrient retention, and water purification (Danovaro and Pusceddu, 2007; Barbier et al., 2011). Plant invasion has been well recognized to pose a serious threat to the sustainability of these ecosystems (Ramus et al., 2017). Smooth cordgrass (Spartina alterniflora Loisel., abbreviated as S. alterniflora), native to the United States, was initially introduced into China in 1979 for coastal protection and eco-engineering purposes (Liu et al., 2016). Since then, it has widely established in coastal mudflats and salt marshes in China along the coastline from Liaoning Province to Hainan Province (Zhang et al., 2017b). In fact, S. alterniflora has become a model plant species for studying invasion ecology in coastal ecosystems. Previous studies have already indicated that S. alterniflora invasion can drastically increase soil organic matter (Cheng et al., 2006; Zhang et al., 2010; He et al., 2019), influence edaphic variables (e.g., pH and salinity) (Zhang et al., 2019), and alter soil nutrients availability (Liao et al., 2007; Xie et al., 2019). Compared with native plant species (Pragmites australis and Scirpus mariqueter), higher nutrient input from S. alterniflora could enhance the resource availability for soil microorganisms (Zhang et al., 2020b), eventually, favor the growth of opportunistic saprotrophic species (Kyaschenko et al., 2017). In recent years, S. alterniflora expanded rapidly in the tidal areas of the Yellow River Delta (YRD), displacing native species and thereby threatening the local aboveground biodiversity (Ren et al., 2019). Yet little is known about the responses of soil fungal diversity and community composition to the S. alterniflora invasion in coastal wetlands.

In this study, we assessed the changes in soil fungal diversity and community after the S. alterniflora invasion in a developing invaded saltmarsh ecosystem. We hypothesize that: (i) soil fungal richness will increase with the S. alterniflora invasion due to increased resource availability triggering a higher abundance of fungal saprotrophs; (ii) the associations among fungal species will become more complex in invaded sites due to the elevated nutrient input with invasion, thus triggering more negative connections as a consequence of species competition for growth.

Section snippets

Study area and soil sampling

This study was conducted in the Yellow-River-Delta National Nature Reserve (37°40′–38°10′N, 118°40′–119°20′E; Fig. 1), located in the Dongying city, Shandong province, China. This area has a warm-temperate continental monsoon climate with four seasons, including a rainy summer. The average annual precipitation is 530–630 mm (Fan et al., 2012) and the annual mean temperature ranges from 11.5 to 12.4 °C (Kong et al., 2015). The exotic S. alterniflora was introduced in the YRD in 1989 to prevent

Edaphic parameters

Soils from the S. alterniflora invaded site had a significantly lower pH and salinity (P < 0.01) (Table 1). In contrast, soil moisture was significantly higher (F1,18 = 15.53, P = 0.001). Soil nutrients content was elevated as a consequence of invasion, as indicated by SOC, DOC, and TN, respectively (P < 0.01). However, there was no statistically significant difference in soil C/N ratios between native and invaded sites (F1,18 = 0, P > 0.05).

Fungal alpha diversity

After quality filtering, a total of 1139 OTUs with a

Effects of plant invasion on soil fungal diversity and community composition

Compared to the native sites, the sites invaded with S. alterniflora showed a remarkably different soil fungal diversity and community composition. High levels of shoot input and litter production from invasive species relative to the native species (Liao et al., 2008; Zhang et al., 2020a) may have promoted the growth of a more diverse fungal community, resulting in a higher number of niches where nutrients would be available (Kubartová et al., 2009; Piper et al., 2015). However, the fungal

Conclusions

Changes in soil fungal diversity, community composition, and functional guilds were investigated in a newly-invaded salt marsh ecosystem in Northern China. Exotic S. alterniflora invasion dramatically decreased fungal richness and phylogenetic diversity compared with native sites with Suaeda salsa. Shifts of the structural and functional fungal community compositions due to S. alterniflora invasion were tightly associated with changes in edaphic parameters, especially soil pH and salinity.

Declaration of competing interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgements

This study was funded by the National Key Research and Development Program of China (Grant No. 2017YFC0505906), the Fundamental Research Funds for the Central Universities (No. 310430001), and the Interdisciplinary Research Funds of Beijing Normal University. We acknowledge the China Scholarship Council (CSC) for the financial support for Guangliang Zhang to study in Thünen Institute, Germany.

References (96)

  • C.L. Lauber et al.

    The influence of soil properties on the structure of bacterial and fungal communities across land-use types

    Soil Biol. Biochem.

    (2008)
  • Y.C. Li 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)
  • X. Liang et al.

    Effect of exotic Spartina alterniflora on fungal symbiosis with native plants Phragmites australis and Scirpus mariqueter, and model plants Lolium perenne L. and Trifolium repens

    Aquat. Bot.

    (2016)
  • N.H. Nguyen et al.

    FUNGuild: An open annotation tool for parsing fungal community datasets by ecological guild

    Fungal Ecol.

    (2016)
  • M.L. Phillips et al.

    Fungal community assembly in soils and roots under plant invasion and nitrogen deposition

    Fungal Ecol.

    (2019)
  • K.M. Rath et al.

    The microbial community size, structure, and process rates along natural gradients of soil salinity

    Soil Biol. Biochem.

    (2019)
  • J. Vanegas et al.

    Effect of salinity on fungal diversity in the rhizosphere of the halophyte Avicennia germinans from a semi-arid mangrove

    Fungal Ecol.

    (2019)
  • R.R. Xie et al.

    Changes in sediment nutrients following Spartina alterniflora invasion in a subtropical estuarine wetland, China

    Catena

    (2019)
  • Q.C. Zeng et al.

    The local environment regulates biogeographic patterns of soil fungal communities on the Loess Plateau

    Catena

    (2019)
  • Y.H. Zhang et al.

    Changes in soil organic carbon dynamics in an Eastern Chinese coastal wetland following invasion by a C4 plant Spartina alterniflora

    Soil Biol. Biochem.

    (2010)
  • G.L. Zhang et al.

    Shifts of soil microbial community composition along a short-term invasion chronosequence of Spartina alterniflora in a Chinese estuary

    Sci. Total Environ.

    (2019)
  • A.K. Alzarhani et al.

    Are drivers of root-associated fungal community structure context specific?

    ISME J

    (2019)
  • M.A. Anthony et al.

    Fungal community homogenization, shift in dominant trophic guild, and appearance of novel taxa with biotic invasion

    Ecosphere

    (2017)
  • M.A. Anthony et al.

    Fungal communities do not recover after removing invasive Alliaria petiolata (garlic mustard)

    Biol. Invasions

    (2019)
  • S. Banerjee et al.

    Keystone taxa as drivers of microbiome structure and functioning

    Nat. Rev. Microbiol.

    (2018)
  • E.B. Barbier et al.

    The value of estuarine and coastal ecosystem services

    Ecol. Monogr.

    (2011)
  • M. Bastian et al.

    Gephi: an open source software for exploring and manipulating networks

  • Y. Benjamini et al.

    Controlling the false discovery rate: a practical and powerful approach to multiple testing

    J. R. Stat. Soc. Ser. B Methodol.

    (1995)
  • J.B. Boberg et al.

    Nitrogen and carbon reallocation in fungal mycelia during decomposition of boreal forest litter

    PLoS One

    (2014)
  • M.A. Bradford et al.

    Discontinuity in the responses of ecosystem processes and multifunctionality to altered soil community composition

    Proc. Natl. Acad. Sci. U. S. A.

    (2014)
  • J.R. Bray et al.

    An ordination of upland forest communities of southern Wisconsin

    Ecol. Monogr.

    (1957)
  • A.K. Broz et al.

    Soil fungal abundance and diversity: another victim of the invasive plant Centaurea maculosa

    ISME J

    (2007)
  • R.A. Bunn et al.

    Do native and invasive plants differ in their interactions with arbuscular mycorrhizal fungi? A meta-analysis

    J. Ecol.

    (2015)
  • R.M. Callaway et al.

    Soil fungi alter interactions between the invader Centaurea maculosa and north American natives

    Ecology

    (2004)
  • J.G. Caporaso et al.

    QIIME allows analysis of high-throughput community sequencing data

    Nat. Methods

    (2010)
  • C.C. Cleveland et al.

    C:N:P stoichiometry in soil: is there a “Redfield ratio” for the microbial biomass?

    Biogeochemistry

    (2007)
  • W. Dawson et al.

    Identifying the role of soil microbes in plant invasions

    J. Ecol.

    (2016)
  • N.J. Day et al.

    Wildfire severity reduces richness and alters composition of soil fungal communities in boreal forests of western Canada

    Glob. Change Biol.

    (2019)
  • F.T. de Vries et al.

    Soil bacterial networks are less stable under drought than fungal networks

    Nat. Commun.

    (2018)
  • Y. Deng et al.

    Molecular ecological network analyses

    BMC Bioinform

    (2012)
  • T.W. d’Entremont et al.

    Examining arbuscular mycorrhizal fungi in saltmarsh hay (Spartina patens) and smooth cordgrass (Spartina alterniflora) in the Minas Basin, Nova Scotia

    Northeast. Nat.

    (2018)
  • R.C. Edgar

    UPARSE, highly accurate OTU sequences from microbial amplicon reads

    Nat. Methods

    (2013)
  • R.C. Edgar et al.

    UCHIME improves sensitivity and speed of chimera detection

    Bioinformatics

    (2011)
  • E. Egidi et al.

    A few Ascomycota taxa dominate soil fungal communities worldwide

    Nat. Commun.

    (2019)
  • K.J. Elgersma et al.

    Linear and non-linear impacts of a non-native plant invasion on soil microbial community structure and function

    Biol. Invasions

    (2011)
  • C. Fahey et al.

    Plant communities mediate the interactive effects of invasion and drought on soil microbial communities

    ISME J

    (2020)
  • X. Fan et al.

    Soil salinity development in the Yellow River Delta in relation to groundwater dynamics

    Land Degrad. Dev.

    (2012)
  • J. Geml et al.

    Large-scale fungal diversity assessment in the Andean Yungas forests reveals strong community turnover among forest types along an altitudinal gradient

    Mol. Ecol.

    (2014)
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