Seasonal dynamics of soil microbial diversity and functions along elevations across the treeline
Graphical abstract
Introduction
Understanding how microbes distribute along elevation and their driving factors is fundamental in biogeography (Lomolino, 2001; Hanson et al., 2012). A large body of studies have been focusing on microbial elevational diversity patterns, since the first study of microbial elevational distribution initiated by Bryant et al. (2008), with increasingly researchers continually observing significant trends with elevation in α-diversity for soil microbes, although the conclusions were inconsistent (Singh et al., 2012; Wang et al., 2015; Peay et al., 2017; Nottingham et al., 2018; Shen et al., 2019). For example, some studies observed the hump-shaped trends for microbial α-diversity and explained such elevational patterns with mid-domain effect (Singh et al., 2012; Miyamoto et al., 2014). Other studies found that the U-shaped or decreasing elevational patterns of microbial α-diversity were largely correlated with soil pH variation (Wang et al., 2015; Shen et al., 2019; Shen et al., 2020). Temperature and plant diversity are also important factors in explaining the decreasing elevational microbial α-diversity patterns (Nottingham et al., 2018; Shen et al., 2020). However, most of these conclusions were acquired from one-time (snapshot) survey, which overlooked microbial variation with time (Shade et al., 2013; Bardgett and van der Putten, 2014; Shade and Gilbert, 2015; Thompson et al., 2017). One may curious about whether the elevational diversity patterns showed by soil microbes were influenced by time (e.g. seasonality), as recent studies found strong seasonal effects on soil microbial diversity at horizontal regional or continental scales (Averill et al., 2019; Keet et al., 2019). Currently, the majority of studies have concluded that space is more important than season in shaping microbial communities (Lauber et al., 2013; Fournier et al., 2020; Zhang et al., 2020). Seasonality, always associated with shifts of climate and plant growth, may induce variations in soil properties and thus lead to the shift of elevational diversity patterns (Rasche et al., 2011; Lauber et al., 2013). To our knowledge, the relative importance of elevation and season in shaping microbial distribution is poorly understood (but see Shigyo et al., 2019; Zhu et al., 2020).
Soil microorganisms, including prokaryotic (i.e. bacteria and archaea) and eukaryotic (i.e. fungi, protist and metazoa) groups, are fundamental for driving biogeochemical cycling and maintaining ecosystem functions (Geisen et al., 2018; Rillig et al., 2019). There still exists a debate on whether these groups exhibited identical manner in elevational diversity patterns. For example, one recent study observed that soil bacterial and fungal α-diversity consistently decreased with elevation, which follows the plant species richness pattern driven by temperature, as predicted by Humboldt (Nottingham et al., 2018). Yet, our latest finding, together with a previous study by Peay et al. (2017), suggest that elevational α-diversity patterns between bacterial and fungal communities are contrasting (Shen et al., 2020). Recent studies have investigated the global-scale distributions of soil protists and nematodes, and revealed their ecological preferences and likely contributions to soil functioning (van den Hoogen et al., 2019; Oliverio et al., 2020). However, research on the elevational distributions of micro-eukaryotic groups is still rare (but see Shen et al., 2014; Dong et al., 2017; Sun et al., 2020). Limited studies reported that the elevational α-diversity trends for specific micro-eukaryotic groups (e.g. Onychiurinae and nematodes) are not significant or unimodal (Dong et al., 2017; Sun et al., 2020). Meanwhile, we know little about how microbial functional groups (e.g. diazotrophs) distribute along elevation, and whether their diversity patterns differ from those for taxonomic groups. Soil diazotrophic communities, receiving high attention recently in agricultural ecosystems (Tu et al., 2016; Feng et al., 2018; Gao et al., 2019), have been firstly investigated along an elevation gradient on Mount Gongga, and the authors found that their diversity patterns were basically same with that for bacteria (Wang et al., 2019).
Treeline, the boundary between forest and shrubland or grassland, has been identified as extremely sensitive to climate change (Dawes et al., 2017; Mayor et al., 2017). Previous studies suggest that the elevation of treeline tends to increase with elevated temperature or moisture (Körner and Paulsen, 2004; Liang et al., 2014). However, microbial studies in this area were scarce (but see Thébault et al., 2014; Ding et al., 2015; Shen et al., 2016; Mayor et al., 2017). Our previous studies indicate that treeline might be a potential factor hindering the significant elevational α-diversity patterns (Li et al., 2016; Shen et al., 2019). In this study, we collected soil samples along an elevation gradient above and below the treeline on Dongling Mountain. Soils sampling at the same sites was conducted in three seasons (spring, summer and autumn). We analyzed microbial species richness (α-diversity) and compositional dissimilarity of communities (β-diversity) through the sequencing of 16S, 18S rRNA genes and nifH gene. We also measured microbial functions as represented by basal and induced soil respiration. We asked: (1) whether there exist significant seasonal and elevational effects on soil microbial α-diversity, β-diversity and functions across the treeline; (2) which effects (season vs. elevation) are larger on microbial α-diversity, β-diversity and functions, and whether the elevational patterns affected by seasonality; (3) which environmental factors best explain the spatiotemporal variation of microbial α- and β-diversity and functions. Based on the recent findings at horizontal (Fournier et al., 2020; Zhang et al., 2020) and elevational (Shigyo et al., 2019; Zhu et al., 2020) scales, we hypothesized that (1) there would be significant seasonal and elevational effects on soil microbial α-diversity, β-diversity and functions; (2) the effects of elevation would be greater than seasonal effects on microbial α-diversity, β-diversity and functions, thus the elevational patterns would not be affected by seasonality.
Section snippets
Study site and soil sampling
Dongling Mountain (40°00′–40°03′N, 115°26′–115°30′E), located about 100 km northwest of Beijing (China), is a national nature reserve and the site of Beijing Forest Ecosystem Research Station. This region belongs to a warm temperate continental monsoon climate with average annual temperature between 5 °C–10 °C and average annual precipitation between 500 and 650 mm. The forest is characterized by a secondary forest around 80 years which is dominated by oak trees (Quercus liaotungensis) with a
Seasonal and elevational effects on microbial α-diversity
Seasonal and elevational effects on α-diversity were all significant for the six microbial groups, and the effects of elevation were larger than seasonal effects (Fig. 2). Among these groups, bacteria showed the highest seasonal variation in α-diversity, while diazotroph had the lowest level of seasonal variation (Fig. 2, Fig. S1). Along the whole elevation gradient across the treeline, elevational patterns for the α-diversity of three groups: bacteria, protist and metazoa were significantly
Discussion
There has been a number of studies focusing on microbial elevational distributions in the past decade (Fierer et al., 2011; Singh et al., 2012; Shen et al., 2013; Peay et al., 2017; Nottingham et al., 2018; Hu et al., 2020; Shen et al., 2020), while few of these elevational studies sampled at multiple times to simultaneously evaluate the spatial and temporal effects on microbial communities (but see Shigyo et al., 2019; Zhu et al., 2020). In this study, we investigated soil microbial diversity
CRediT authorship contribution statement
Congcong Shen: Conceptualization, Methodology, Formal analysis, Investigation, Data curation, Writing – original draft. Ji-Zheng He: Writing – review & editing. Yuan Ge: Conceptualization, Supervision, Writing – review & editing.
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
We thank Jichen Wang, Nenghu Qiao, Zhongwang Jing, Huaibo Sun, Jianlei Wang for assistance in soil sampling and Bojian Li in lab analysis. This work was supported by the National Natural Science Foundation of China (41701273, 41671254), the Second Tibetan Plateau Scientific Expedition and Research Program (2019QZKK0306, 2019QZKK0308), and the State Key Laboratory of Urban and Regional Ecology (SKLURE2017-1-7).
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