Protist taxonomic and functional diversity in soil, freshwater and marine ecosystems

Protists dominate eukaryotic diversity and play key functional roles in all ecosystems, particularly by catalyzing carbon and nutrient cycling. To date, however, a comparative analysis of their taxonomic and functional diversity that compares the major ecosystems on Earth (soil, freshwater and marine systems) is missing. Here, we present a comparison of protist diversity based on standardized high throughput 18S rRNA gene sequencing of soil, freshwater and marine environmental DNA. Soil and freshwater protist communities were more similar to each other than to marine protist communities, with virtually no overlap of Operational Taxonomic Units (OTUs) between terrestrial and marine habitats. Soil protists showed higher γ diversity than aquatic samples. Differences in taxonomic composition of the communities led to changes in a functional diversity among ecosystems, as expressed in relative abundance of consumers, phototrophs and parasites. Phototrophs (eukaryotic algae) dominated freshwater systems (49% of the sequences) and consumers soil and marine ecosystems (59% and 48%, respectively). The individual functional groups were composed of ecosystem- specific taxonomic groups. Parasites were equally common in all ecosystems, yet, terrestrial systems hosted more OTUs assigned to parasites of macro-organisms while aquatic systems contained mostly microbial parasitoids. Together, we show biogeographic patterns of protist diversity across major ecosystems on Earth, preparing the way for more focused studies that will help understanding the multiple roles of protists in the biosphere

Niche Conservatism Drives the Elevational Diversity Gradient in Major Groups of Free-Living Soil Unicellular Eukaryotes

Ancestral adaptations to tropical-like climates drive most multicellular biogeography and macroecology. Observational studies suggest that this niche conservatism could also be shaping unicellular biogeography and macroecology, although evidence is limited to Acidobacteria and testate amoebae. We tracked the phylogenetic signal of this niche conservatism in far related and functionally contrasted groups of common soil protists (Bacillariophyta, Cercomonadida, Ciliophora, Euglyphida and Kinetoplastida) along a humid but increasingly cold elevational gradient in Switzerland. Protist diversity decreased, and the size of the geographic ranges of taxa increased with elevation and associated decreasing temperature (climate), which is consistent with a macroecological pattern known as the Rapoport effect. Bacillariophyta exhibited phylogenetically overdispersed communities assembled by competitive exclusion of closely related taxa with shared (conserved) niches. By contrast, Cercomonadida, Ciliophora, Euglyphida and Kinetoplastida exhibited phylogenetically clustered communities assembled by habitat filtering, revealing the coexistence of closely related taxa with shared (conserved) adaptations to cope with the humid but temperate to cold climate of the study site. Phylobetadiversity revealed that soil protists exhibit a strong phylogenetic turnover among elevational sites, suggesting that most taxa have evolutionary constraints that prevent them from colonizing the colder and higher sites of the elevation gradient. Our results suggest that evolutionary constraints determine how soil protists colonize climates departing from warm and humid conditions. We posit that these evolutionary constraints are linked to an ancestral adaptation to tropical-like climates, which limits their survival in exceedingly cold sites. This niche conservatism possibly drives their biogeography and macroecology along latitudinal and altitudinal climatic gradients

Higher spatial than seasonal variation in floodplain soil eukaryotic microbial communities

Beta diversity is a key component of biodiversity with implications ranging from species dynamics to ecosystem functioning. However, β-diversity and its drivers have received little attention, especially for micro-eukaryotes which play key roles in soil functioning. We studied the diversity of soil micro-eukaryotes in a Swiss lowland floodplain using high-throughput Illumina sequencing of soil DNA. We determined the temporal vs. spatial patterns of soil micro-eukaryotic α- and β-diversity in six contrasted habitats sampled over one year. We identified the drivers of these patterns among soil conditions and functions and identified indicator taxa of habitats in each season. We found higher spatial than temporal variability and a strong space-time interaction in soil micro-eukaryotic diversity patterns as well as in their edaphic drivers, which contrasts with previous observation of bacterial diversity patterns. Our results show that, although soil micro-eukaryotic diversity indeed varies seasonally, it is correlated most strongly with edaphic variables and vegetation but the strength of correlations with individual drivers varied seasonally. Microbial diversity patterns and their drivers can thus differ quite substantially among seasons and taxa. Despite the dominance of spatial patterns, the temporal component of microbial diversity should not be ignored to accurately estimate the diversity and the complexity of soil microbial community assembly processes. Given the importance of soil microbial diversity for ecosystem functioning such knowledge is relevant for land management

Landscape structure is a key driver of soil protist diversity in meadows in the Swiss Alps

Context: Human-induced changes in landscape structure are among the main causes of biodiversity loss. Despite their important contribution to biodiversity and ecosystem functioning, microbes - and particularly protists - remain spatially understudied. Soil microbiota are most often driven by local soil properties, but the influence of the surrounding landscape is rarely assessed. Objectives: We assessed the effect of landscape structure on soil protist alpha and beta diversity in meadows in the western Swiss Alps. Methods: We sampled 178 plots along an elevation gradient representing a broad range of environmental conditions and land-use. We measured landscape structure around each plot at 5 successive spatial scales (i.e. neighbourhood windows of increasing radius, ranging from 100 to 2000 m around a plot). We investigated the changes of protist alpha and beta diversity as a function of landscape structure, local environmental conditions and geographic distance. Results: Landscape structures played a key role for protist alpha and beta diversity. The percentage of meadows, forests, or open habitats had the highest influence among all landscape metrics. The importance of landscape structure was comparable to that of environmental conditions and spatial variables, and increased with the size of the neighbourhood window considered. Conclusions: Our results suggest that dispersal from neighbouring habitats is a key driver of protist alpha and beta diversity which highlight the importance of landscape-scale assembly mechanisms for microbial diversity. Landscape structure emerges as a key driver of microbial communities which has profound implications for our understanding of the consequences of land-use change on soil microbial communities and their associated functions

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

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

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

Aim: Trends in spatial patterns of macroscopic organisms diversity can be well predicted from correlative models, using topo-climatic variables for plants and animals allowing inference over large scales. By contrast, soil microorganisms diversity 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 vs. 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, Phytomyxea), phagotrophs (Sarcomonadea, Tubulinea, Spirotrichea) phototrophs (Chlorophyta, Trebouxiophyceae, 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 sub-unit 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

Assessing the degree to which climate explains the spatial distributions of different taxonomic and functional groups is essential for anticipating the effects of climate change on ecosystems. Most effort so far has focused on above¿ground organisms, which offer only a partial view on the response of biodiversity to environmental gradients. Here including both above¿ and below¿ground organisms, we quantified the degree of topoclimatic control on the occurrence patterns of >1,500 taxa and phylotypes along a c. 3,000 m elevation gradient, by fitting species distribution models. Higher model performances for animals and plants than for soil microbes (fungi, bacteria and protists) suggest that the direct influence of topoclimate is stronger on above¿ground species than on below¿ground microorganisms. Accordingly, direct climate change effects are predicted to be stronger for above¿ground than for below¿ground taxa, whereas factors expressing local soil microclimate and geochemistry are likely more important to explain and forecast the occurrence patterns of soil microbiota. Detailed mapping and future scenarios of soil microclimate and microhabitats, together with comparative studies of interacting and ecologically dependent above¿ and below¿ground biota, are thus needed to understand and realistically forecast the future distribution of ecosystems