Rhizosphere fungal assemblages and soil enzymatic activities in a 110-years alpine chronosequence

https://doi.org/10.1016/j.soilbio.2014.02.014Get rights and content

Highlights

  • Plant species affected AMF and ECM fungal communities in a young alpine ecosystem.

  • Soil developmental stage determined the community composition of saprophytic fungi.

  • Rhizosphere from Salix helvetica had high chitinase and α-glucosidase activities.

  • Rhizosphere from Rhododendron ferrugineum had high α-glucosidase and sulfatase activities.

  • Rhizosphere from Agrostis gigantea had high phosphatase and β-glucosidase activities.

Abstract

The abundance, distribution and functions of soil fungi in alpine ecosystems remain poorly understood. We aimed at linking the fungal community structure with soil enzymatic activities in the rhizospheres of several plants associating with mycorrhizal fungi (arbuscular, ecto- and ericoid) and growing along a soil developmental gradient on the forefield of an alpine glacier. Fungal communities in roots and in rhizosphere soils were assessed using a site-tailored set of quantitative PCR assays with fluorescent hydrolysis probes. Enzymatic activities of mycorrhizal roots and rhizosphere soils were assessed using fluorogenic substrates. In this study we addressed: i) whether and how the structure of fungal communities and enzymatic activities in rhizosphere soils change along the soil developmental gradient, ii) whether the type of mycorrhiza shows a clear relationship to the pattern of enzymatic activities in the rhizosphere, and iii) how the structure of fungal communities and enzymatic activities in rhizosphere soils is related to plant species abundances along the soil chronosequence. The results suggest that plant identity affected the structure of both ecto- and arbuscular mycorrhizal fungal communities in rhizosphere soil and roots, whereas the community of non-mycorrhizal fungi was rather dictated by the soil developmental stage. Both plant identity and associated mycorrhizal fungi affected the enzymatic activity in the rhizosphere soil. Species-specific elevations of rhizosphere enzyme activities were detected for Salix helvetica (chitinase and α-glucosidase), Rhododendron ferrugineum (α-glucosidase and sulfatase), and Agrostis gigantea (phosphatase and xylosidase). These results indicate different functional roles played by different types of mycorrhizal symbiosis in a young alpine ecosystem.

Introduction

Land gradually emerging from underneath retreating glaciers provides a natural laboratory for studying ecosystem development (Huggett, 1998, Walker et al., 2010). Living organisms – especially plants – contribute substantially to ecosystem development in general and to soil formation in particular (Chapin et al., 1994). Acting as islands of available nutrients and carbon, their rhizospheres harbor a great diversity of highly active microorganisms (Hawkes et al., 2007), including mycorrhizal fungi.

Read (1993) proposed that occurrence and distribution of mycorrhizal fungal communities in primary succession ecosystems presented a predictable pattern: early successional stages were mainly colonized by non-mycorrhizal plants which were subsequently replaced by plants hosting arbuscular mycorrhizal fungi (AMF), followed by ectomycorrhizal (ECM) and eventually by the ericoid mycorrhizal (ER) plants. However, reviewing the most recent research on fungal communities during long-term soil development, Dickie et al. (2013) postulated that the distribution pattern of mycorrhizal fungi in newly developing ecosystems cannot be infallibly predicted. Firstly, the distribution pattern of mycorrhizal fungi in a given environment is affected by local edaphic conditions and plant community composition. Secondly, driven by ecosystem disturbances, the distribution pattern of mycorrhizal fungi comprises both progressive and retrogressive stages. This means that a given mycorrhizal type can occur at any developmental stage which provides persistent local conditions for its establishment and further development. For example, AMF commonly associated with early succession plants can still occur at later stages of ecosystem development. This can be either due to colonization of spaces opened by disturbance or due to persistence of AMF in the ecosystem as it develops (Lambers et al., 2008, Oehl et al., 2011). Reversely, the presence of ECM and ER fungi not only at the mature but also at the pioneering stages of ecosystem development has been repeatedly reported in the literature (Jumpponen, 2003, Cázares et al., 2005).

Different plant species are colonized by specific mycorrhizal type/s and preferentially associate with selected mycorrhizal fungal taxa (Smith and Read, 2008). Thus, the composition of mycorrhizal fungal communities is not random. The specificity of mycorrhizal fungi towards the host as well as the uneven distribution of a plant species in the landscape are likely to underlie observed fluctuations in the density and composition of mycorrhizal fungal communities in a given environment. Following this concept, Becklin et al. (2012) reported that richness and diversity of the AMF communities vary for different herbaceous plants (i.e., Taraxacum ceratophorum, Taraxacum officinale, and Polemonium viscosum) colonizing alpine meadows or shrublands. Similarly, Sykorová et al. (2007) noted qualitative differences in AMF communities associated with three plant taxa (i.e., Gentiana verna, Gentiana acaulis, and Trifolium spp.) in a Swiss alpine meadow. Like for AMF, plants often tend to share ECM symbionts rather than to harbor distinctive ECM communities (Ryberg et al., 2011), although cases of strict association between some fungal and plant partners are known (e.g. Lactarius sp. and Larix sp.). However, more investigations are needed to test how widespread is the sharing of symbionts between plant species or which factors decide about distinctiveness of the fungal communities associated with them.

The distribution, density and structure of mycorrhizal fungal communities in the environment are directly related to their functioning. Mycorrhizal fungi support the host plant in nutrient/water acquisition and alleviate various environmental stresses, and thus their functioning can directly influence development, establishment and fitness of the plant communities (Smith and Read, 2008). Among the mycorrhizal functions, enzymatic activity as a strategy for nutrient acquisition has received substantial attention. A variety of hydrolytic exoenzymes are produced by ECM and ER fungi (Read and Perez-Moreno, 2003). Upon hydrolysis of complex biomolecules immobilized in soil organic matter (SOM), essential nutrients are released to the soil. These are then taken up by mycorrhizal hyphae and further transferred to the mycorrhizal host plant (Smith and Read, 2008). Unlike for ECM and ER, production of large amounts of hydrolytic exoenzymes by AMF has not been consistently shown (Hodge and Fitter, 2010). Although bacteria, fungi and plants all contribute to the pool of enzymes in the soil, and a given enzyme cannot be traced back to a specific organism (Tabatabai and Dick, 2002), there is evidence that large amounts of numerous exoenzymes are actively produced and released to the hyphosphere of specific ECM and ER fungi (Courty et al., 2005, Mitchell and Gibson, 2006). This suggests that enzymatic activities in the rhizosphere soil of different plant species are to a great extent determined by their associated mycorrhizal partners.

Using a soil development sequence in a glacier forefield as a model, the aims of this work were to determine i) the contribution of plant identity and soil properties on the structure (composition and abundance) of mycorrhizal fungal communities and ii) the enzymatic activities in the rhizosphere soils of four different plant species (Salix helvetica, Agrostis gigantea, Leucanthemopsis alpina and Rhododendron ferrugineum) hosting different mycorrhizal types. We hypothesized that i) the structure of fungal communities associated with different plant species would change along a soil developmental gradient; ii) enzymatic activities in the rhizosphere soil of different plant species would change along the same gradient; iii) exoenzyme activities would be greater in the rhizospheres of plants associated with ecto- and ericoid mycorrhizal fungi (S. helvetica and R. ferrugineum, respectively) than of plants harboring arbuscular mycorrhizal fungi (A. gigantea and L. alpina).

Section snippets

Sampling sites

Sampling was performed at the forefield of the Damma glacier situated in the Central Swiss Alps (Canton of Uri, N46°38.117′, E8°27.677′). The same study site was used intensively for the multidisciplinary project “BigLink” and has been described in detail elsewhere (Bernasconi et al., 2011, Welc et al., 2012). In July 2009, eight experimental sites were selected for further investigations (see Fig. S1 in electronic supplement). The approximate ages of soils on these sites ranged from 7 to 110

Impact of plant species

Ectomycorrhizal fungi associated only with S. helvetica (Fig. 1A, B). The abundance of ECM as assessed by qPCR was lowest at the young sites (7–12 years after deglaciation), then peaked at the site deglaciated 65 years ago, and declined towards the older sites (i.e., deglaciated >65 years ago). Russula emetica and Laccaria pumila were the dominant ECM species associated with S. helvetica roots. In addition, Inocybe lacera commonly occurred in the rhizosphere soil of S. helvetica.

Arbuscular

Discussion

Three hypotheses were tested in this study, which will be discussed below.

Firstly, we hypothesized that the structure of fungal communities associated with different plant species would change along a soil developmental gradient. While the results generally supported this hypothesis, they revealed that it is crucial for the discussion whether the ‘soil developmental gradient’ is defined as a shift in soil properties with soil age or as a change of vegetation cover on differently aged soils. We

Conclusions

In this study, we combined quantitative PCR and enzymatic activity assays to investigate the relationships between fungal abundance and enzymatic activities in the rhizospheres of mountain plants that varied in mycorrhizal status. We demonstrated that the structure of mycorrhizal fungal (ECM and AMF) communities was strongly affected by plant species identity, whereas soil developmental stage influenced the community of other soil fungi (i.e., UTS). We also revealed that the fungal community

Acknowledgments

The authors thank Fabio Grasso for excellent technical support with the laboratory analyses and assistance during the sampling in the field. Thomas Flura is acknowledged for conducting the ICP and CNS measurements and Renaud Maire for excellent help with measurement of enzymatic activity of ECM root tips. We gratefully acknowledge funding from the BigLink project (Competence Center Environment and Sustainability, CCES) and Swiss National Science Foundation (project 31003A-125491). Jan Jansa was

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