Elsevier

Applied Soil Ecology

Volume 166, October 2021, 104079
Applied Soil Ecology

Abiotic factors affecting the bacterial and fungal diversity of permafrost in a rock glacier in the Stelvio Pass (Italian Central Alps)

https://doi.org/10.1016/j.apsoil.2021.104079Get rights and content

Highlights

  • The structure of bacterial communities is affected by depth, % of water, pH and LOI.

  • The structure of fungal communities is affected by depth.

  • Bacterial communities are dominated by Actinobacteria and Proteobacteria.

  • Meyerozyma is the prevalent fungal genera found in Alpine permafrost.

  • The prevalence of positive co-occurrences between bacteria and fungi was found.

Abstract

The impact of climate change in the European Alps has been roughly twice the global average, dramatically reducing permafrost extent and thickening of its active layer. Therefore, the study of the abiotic factors (i.e. chemical/physical parameters) affecting the microbial diversity inhabiting Alpine permafrost appears to be of dramatic relevance. Within the European Alps, the Stelvio area exhibits these effects in a particularly evident way, with important consequences on microbial ecosystems. Therefore, microbial communities inhabiting a permafrost core collected in the Scorluzzo active rock glacier (Stelvio Pass, Italian Central Alps) were investigated along a depth gradient (410 to 524 cm from the surface). The taxonomic structures of bacterial and fungal communities were investigated via a next-generation sequencing (NGS) approach (Illumina MiSeq), targeting the bacterial V3-V4 regions of 16S rDNA and the fungal ITS2 region. Abiotic soil factors (grain size, electrical conductivity, ice/water content, pH, Loss-on-Ignition - LOI, total and organic carbon, nitrogen and phosphorous) were analysed. Richness and Shannon-H diversity indices were correlated to abiotic factors. Bacterial diversity was significantly (p < 0.05) correlated with LOI, while fungal diversity was significantly (p < 0.05) correlated with the depth gradient. The Constrained Analysis of Principal (CAP) coordinates were used to study the correlation between abiotic parameters and the taxonomic structure of bacterial and fungal communities. Among all tested variables, the depth gradient, water content, pH and LOI affected the taxonomic structure of bacterial communities (in particular, the abundance of bacterial amplicon sequence variants - ASVs - assigned to Afipia sp., Chloroflexi, Gaiella sp., Oryzihumus sp. and Serratia, sp.), while fungal communities (ASVs assigned to Naganishia sp., Rhodotorula sp., Sordariomycetes and Taphrinales) were affected by the depth gradient. Co-occurrences (calculated by Pearson correlation coefficient) among microbial taxa (i.e. bacteria vs bacteria, bacteria vs fungi, fungi vs fungi) were investigated: the prevalence of significant (p < 0.05) positive co-occurrences was found, suggesting that the coexistence of different microbial taxa could play a crucial role in maintaining the ecological and taxonomic balance of both bacterial and fungal communities inhabiting the Alpine permafrost ecosystem. These findings suggest that the bacterial and fungal diversity of Alpine permafrost are affected in different ways by some abiotic factors.

Introduction

Almost 25% of the Northern Hemisphere and 17% of the Earth's exposed land surface is underlain by permafrost (Gruber, 2012) that is defined as a material (ground or rock) with a temperature remaining at or below 0 °C for at least two consecutive years (Shur et al., 2011). Although Alpine permafrost in Europe is quite widespread especially in barren ground, steep bedrock slopes, debris slopes, screes, or morainic deposits, it is above all concentrated within rock glaciers.

Recent atmospheric warming (over the last century) in the European Alps has been roughly twice the global average (Böhm et al., 2001; Auer et al., 2007) dramatically reducing the extent of permafrost and thickening its active layer (Etzelmüller et al., 2020). Within the European Alps, the Stelvio area exhibits these effects in a particularly evident way, with important consequences on microbial ecosystems (Ponti et al., 2021). Despite their frozen status, many microbial species inhabiting permafrost cores are considered metabolically active, and this activity can obviously increase in the case of permafrost thawing (even temporary) (Bakermans et al., 2003; Rivkina et al., 2004, Rivkina et al., 2018; Steven et al., 2006; Tuorto et al., 2014). Therefore, recent studies have included the monitoring of microbial parameters in order to gain a more complete picture of the interactions between biotic and abiotic factors occurring in these changing ecosystems (Wagner et al., 2007; Hollesen et al., 2011; Graham et al., 2012; Donhauser and Frey, 2018).

Research carried out during the last decade has focused on the detailed characterisations of the microbial communities occurring in permafrost ecosystems in Arctic and Antarctic regions, and the Tibetan plateau; the observed microbial diversity was often associated with a habitat-specific distribution (Yergeau et al., 2010; Zucconi et al., 2012; Goordial and Whyte, 2014; Hu et al., 2015; Chen et al., 2017; La Ferla et al., 2017; Borruso et al., 2018; Donhauser and Frey, 2018; Papale et al., 2019; Xue et al., 2019; Sannino et al., 2020a). On the other hand, there is little knowledge about the microbial communities inhabiting the European Alpine permafrost. Frey et al. (2016) studied both bacterial and fungal diversity, finding many unknown taxa in the active layer (1.60 m depths) of the permafrost (Muot-da-Barba-Peider, Eastern Switzerland), suggesting that these microorganisms may have developed peculiar structural and functional adaptation mechanisms to survive and even proliferate in such ecosystems.

The abiotic parameters affecting the microbial diversity inhabiting permafrost have previously been investigated (Zhang et al., 2013; Frank-Fahle et al., 2014; Gittel et al., 2014a; Borruso et al., 2018; Sannino et al., 2020a). Furthermore, recent studies have found that bacterial and fungal communities occurring in the Alpine active layer and permafrost were differently affected by an increase in temperatures (Donhauser and Frey, 2018; Luláková et al., 2019). However, despite the above studies, the knowledge about which abiotic factors may be able to affect the microbial diversity in Alpine permafrost remains largely incomplete. Considering the probability that Alpine glaciers may disappear in the coming decades, the importance of reducing these gaps in knowledge is becoming evident (Zemp et al., 2006). Hence, the study of microbial diversity inhabiting Alpine permafrost and the role of abiotic factors affecting the taxonomic structure of bacterial and fungal communities has a great strategic value.

In light of the above statements, the aims of the present study are: i) to evaluate the bacterial and fungal (including yeasts) diversity of a permafrost core drilled in a rock glacier of the Mount Scorluzzo, Stelvio Pass, Italy along a depth gradient; ii) to estimate what chemical-physical (abiotic) factors could putatively affect bacterial and fungal diversity inside this ecological niche, and ii) to investigate co-occurrences among bacterial and fungal taxa inhabiting the permafrost core.

Section snippets

Study site and sample collection

The Scorluzzo rock glacier is located close to the Stelvio Pass (46°31′ N, 10°25′ E) within the Stelvio National Park at an elevation of 2740 m above sea level in the Italian Central Alps (Fig. 1). The area around the rock glacier is characterised by bedrock outcrops (mainly paragneiss and mica schists), as well as some Holocene till and talus deposits (Ponti et al., 2021). The vegetation is very scarce and typical of the Alpine and nival belts mainly related to pioneer plant communities

Bacterial and fungal diversity

After bioinformatic analyses, a total of 702,630 reads grouped into 3292 ASVs for bacteria and 821,790 reads grouped into 860 ASVs for fungi were found in the six units (U1-U6, each one analysed in triplicate = a total of 18 samples) under study. Almost the entirety (99.99%) of bacterial reads were classified at the phylum level, 99.88% at the class level, 96.36% at the order level, 90.54% at the family level and 86.10% at the genus level. On the other hand, 97.665% of fungal reads were

Discussion

Permafrost is considered to be an important marker of global climate change (Harris et al., 2003). The observed LOI values ranging between 0.18 and 0.35% can be considered reasonable values even in harsh environments such as the rock glacier under study. Furthermore, the TC values (one order of magnitude higher) could probably due to the circulation of “hard water” linked to the occurrence of lenses of dolostones (as sources of carbonates) embedded in the metamorphic rock surrounding and

Conclusion

This study reports the taxonomic structure of bacterial and fungal communities in a permafrost core collected in an Alpine rock glacier. The abiotic factors affecting microbial diversity have also considered. The depth gradient, water content, pH and LOI affected the taxonomic structure of bacterial communities (in particular, the abundance of bacterial amplicon sequence variants - ASVs - assigned to Afipia sp., Chloroflexi, Gaiella sp., Oryzihumus sp., and Serratia sp.) while fungal

Funding

This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.

Declaration of competing interest

The authors declare that they have no conflicts of interest.

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