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

Phylogenetic divergence within the Arcellinida (Amoebozoa) is congruent with test size and metabolism type

Arcellinida (lobose testate amoebae) are abundant and diverse in many ecosystems, especially in moist to aquatic environments. Molecular phylogeny has shown that overall test morphology (e.g., spherical or elongate) is generally conserved in Arcellinida lineages, but the taxonomic value of other traits (e.g., size, ornamentation, mixotrophy/heterotrophy metabolism type) has not been systematically evaluated. Morphological and physiological traits that correspond to genetic differences likely represent adaptive traits of ecological significance. We combined high-resolution phylogenetics (NAD9-NAD7 genes) and advanced morphometrics to assess the phylogenetic signal of morphological traits of a group of elongate Difflugia species (Arcellinida). The phylogenetic analyses revealed two clades which could be reliably separated by test size and the presence/absence of mixotrophy. Differences in test size may reflect trophic level, with smaller organisms occupying lower trophic levels. In addition to having larger tests, elongate mixotrophic Difflugia are characterised by wide, flat bases and an inflation of the lower two thirds of their test. These morphological traits may provide additional volume for endosymbionts and/or increased surface area to aid light transmission. Our results showcase greater diversity within the elongate Difflugia and highlight morphological traits of ecological and evolutionary significance

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

Global distribution modelling of a conspicuous Gondwanian soil protist reveals latitudinal dispersal limitation and range contraction in response to climate warming

Aim The diversity and distribution of soil microorganisms and their potential for long-distance dispersal (LDD)are poorly documented, making the threats posed by climate change difficult to assess. If microorganisms do not disperse globally, regional endemism may develop and extinction may occur due to environmental changes. Here, we addressed this question using the testate amoeba Apodera vas, a morphologically conspicuous model soil microorganism in microbial biogeography, commonly found in peatlands and forests mainly of former Gondwana. We first wanted to document its distribution. We next wanted to assess whether its distribution could be explained by dispersal (i.e., matching its climatic niche) or vicariance (i.e., palaeogeography), based on the magnitude of potential range expansions or contractions in response to past and on-going climatic changes. Last, we wanted to assess the likelihood of cryptic diversity and its potential threat from climate and land-use changes (e.g., due to limited LDD). Location Documented records: Southern Hemisphere and inter-tropical zone; modelling: Global. Methods We first built an updated global distribution map of A. vas using 401 validated georeferenced records. We next used these data to develop a climatic niche model to predict its past (LGM, i.e., 21 3 ka BP; PMIP3 IPSL-CM5A-LR), present, and future (IPSL-CMP6A-LR predictions for 2071-2100, SSP3 and 5) potential distributions in responses to climate, by relating the species occurrences to climatic and topographic predictors. We then used these predictions to test our hypotheses (dispersal/vicariance, cryptic diversity, future threat from LDD limitation). Results Our models show that favourable climatic conditions for A. vas currently exist in the British Isles, an especially well-studied region for testate amoebae where this species has never been found. This demonstrates a lack of inter-hemispheric LDD, congruent with the palaeogeography (vicariance) hypothesis. Longitudinal LDD is however confirmed by the presence of A. vas in isolated and geologically young peri-Antarctic islands. Potential distribution maps for past, current, and future climates show favourable climatic conditions existing on parts of all southern continents, with shifts to higher land from LGM to current in the tropics and a strong range contraction from current to future (global warming IPSL-CM6A-LR scenario for 2071-2100, SSP3.70 and SSP5.85) with favourable conditions developing on the Antarctic Peninsula. Main conclusions This study illustrates the value of climate niche models for research on microbial diversity and biogeography, along with exploring the role played by historical factors and dispersal limitation in shaping microbial biogeography. We assess the discrepancy between latitudinal and longitudinal LDD for A. vas, which is possibly due to contrast in wind patterns and/or likelihood of transport by birds. Our models also suggest that climate change may lead to regional extinction of terrestrial microscopic organisms, thus illustrating the pertinence of including microorganisms in biodiversity conservation research and actions