Soil protist diversity in the Swiss western Alps is better predicted by topo‐climatic than by edaphic variables

Abstract

Aim Trends in spatial patterns of diversity in macroscopic organisms can be well predicted from correlative models, using topo‐climatic variables for plants and animals allowing inference over large scales. By contrast, diversity in soil microorganisms is generally considered as mostly driven by edaphic variables and, therefore, difficult to extrapolate on a large spatial scale based on predictive models. Here, we compared the power of topo‐climatic versus edaphic variables for predicting the diversity of various soil protist groups at the regional scale. Location Swiss western Alps. Taxa Full protist community and nine clades belonging respectively to three functional groups: parasites (Apicomplexa, Peronosporomycetes and Phytomyxea), phagotrophs (Sarcomonadea, Tubulinea and Spirotrichea) and phototrophs (Chlorophyta, Trebouxiophyceae and Diatomeae). Methods We extracted soil DNA from 178 sites along a wide range of elevations with a random‐stratified sampling design. We defined protist Operational Taxonomic Units assemblages by metabarcoding of the V4 region of the rRNA small subunit gene. We assessed and modelled the diversity (Shannon index) patterns of all above‐mentioned taxonomic groups based on topo‐climatic (topography, slope southness, slope steepness and average summer temperature) and edaphic (soil temperature, relative humidity, pH, electroconductivity, phosphorus percentage, carbon/nitrogen, loss on ignition and shale percentage) variables in Generalized Additive Models (GAM). Results The respective significance of topo‐climatic and edaphic variables varied among taxonomic and—to a certain extent—functional groups: while many variables explained significantly the diversity of the three phototrophs this was less the case for the three parasites. Topo‐climatic variables had a better predictive power than edaphic variables, yet predictive power varied among taxonomic groups. Main conclusions Topo‐climatic variables (particularly slope steepness and summer temperature if we consider their significance in the GAMs) were, on average, better predictors of protist diversity at the landscape scale than edaphic variables. However, the predictive power of these variables on diversity differed considerably among taxonomic groups; such relationships may be due to direct and/or indirect (e.g. biotic) influences (like with parasitic taxa, where low predictive power is most likely explained by the absence of information on the hosts’ distribution). Future prospects include using such spatial models to predict hotspots of diversity and disease outbreaks.

Greater topoclimatic control of above‐ versus below‐ground communities

“…This suggests that soil microclimate, which better expresses the temperature and moisture conditions affecting below‐ground and ground‐dwelling organisms and which can be strongly decoupled from air temperature in space and time (see also Bramer et al., 2018; Graae et al., 2012; Scherrer & Körner, 2011; Suggitt et al., 2011), likely also better explains the distributions of soil microorganisms. Furthermore, other edaphic factors (particularly soil pH) and biotic interactions are known to be major drivers for the diversity and community structure of soil fungi and bacteria (Bahram et al., 2018; Bates et al., 2013; Fierer et al., 2009; Li et al., 2018; Malard, Anwar, Jacobsen, & Pearce, 2019; Yashiro et al., 2016), and also but to a lesser extent for the diversity of protists (Seppey et al., 2020). Thus, they can also be expected to strongly contribute to explain the distribution of individual soil microorganisms.…”

“…For instance, plants and some iconic groups of vertebrates and insects have been extensively studied with varying methodologies ranging from basic observational approaches to complex frameworks (Bateman, VanDerWal, Williams, & Johnson, 2012; Bradie & Leung, 2017; Illan et al., 2010; Lawrence et al., 2014; Miller et al., 2018; Mod & Luoto, 2016; Roberts, Nielsen, & Stenhouse, 2014; Seoane, Bustamante, & Diaz‐Delgado, 2004; Staniczenko, Sivasubramaniam, Suttle, & Pearson, 2017), but comparatively fewer attempts have been made to assess the drivers of distributions of soil microorganisms (Bradie & Leung, 2017; Lenoir et al, 2020; Lenoir & Svenning, 2015; Pacifici et al., 2015)—likely due to previous methodological limitations (Riesenfeld, Schloss, & Handelsman, 2004) and, for some groups (e.g. soil protists), to a lower sampling effort (Caron, Worden, Countway, Demir, & Heidelberg, 2008; Geisen et al., 2017, 2018; Seppey et al., 2020; Wilkinson, 1998). Existing studies have evidenced the importance of soil characteristics, such as pH, nutrient content and moisture availability, for explaining the diversity, biomass and community structure of microorganisms in soils (Bahram et al., 2018; Bates et al., 2013; Fierer & Jackson, 2006; Serna‐Chavez, Fierer, & van Bodegom, 2013; Tedersoo et al., 2014).…”

Investigation of an Elevational Gradient Reveals Strong Differences Between Bacterial and Eukaryotic Communities Coinhabiting Nepenthes Phytotelmata

“…Microbes have not been as extensively studied in the context of elevational gradients, but the past decade has seen an increasing number of studies examining elevational patterns of bacteria in soil [6,[8][9][10][11][12][20][21][22] and to a lesser extent, aquatic habitats [23][24][25][26]. Similar studies have also been conducted for fungi [27][28][29][30][31][32][33][34][35] and protists [18,[36][37][38][39]. Of these microbial elevational gradient studies, only a handful have compared diversity patterns of syntopic microbes and macrobes coinhabiting the same microhabitats.…”

Expanding forests in alpine regions: space-for-time indicates a corresponding shift in belowground fungal communities

“…In general, Cercozoa is commonly observed in various soil types, whereas Ciliophora and Apicomplexa have been shown to be relatively more abundant in humid soils (Bates et al, 2013). Due to the parasitic lifestyle of Apicomplexa, their distribution is likely largely dependent on the presence of host species (Arthropodes) (Mahe et al, 2017;Seppey et al, 2020). However, at kingdom and phylum level, none of the protists showed any clear distribution pattern across the ecotone.…”