Taxa-area Relationship Research Articles

Distinct Ecological Processes Mediate Domain-Level Differentiation in Microbial Spatial Scaling.

The spatial scaling of biodiversity, such as the taxa-area relationship (TAR) and distance-decay relationship (DDR), is a typical ecological pattern that is followed by both microbes and macrobes in natural ecosystems. Previous studies focusing on microbes mainly aimed to address whether and how different types of microbial taxa differ in spatial scaling patterns, leaving the underlying mechanisms largely untouched. In this study, the spatial scaling of different microbial domains and their associated ecological processes in an intertidal zone were comparatively investigated. The significant spatial scaling of biodiversity could be observed across all microbial domains, including archaea, bacteria, fungi, and protists. Among them, archaea and fungi were found with much stronger DDR slopes than those observed in bacteria and protists. For both TAR and DDR, rare subcommunities were mainly responsible for the observed spatial scaling patterns, except for the DDR of protists and bacteria. This was also evidenced by extending the TAR and DDR diversity metrics to Hill numbers. Further statistical analyses demonstrated that different microbial domains were influenced by different environmental factors and harbored distinct local community assembly processes. Of these, drift was mainly responsible for the compositional variations of bacteria and protists. Archaea were shaped by strong homogeneous selection, whereas fungi were more affected by dispersal limitation. Such differing ecological processes resulted in the domain-level differentiation of microbial spatial scaling. This study links ecological processes with microbial spatial scaling and provides novel mechanistic insights into the diversity patterns of microbes that belong to different trophic levels. IMPORTANCE As the most diverse and numerous life form on Earth, microorganisms play indispensable roles in natural ecological processes. Revealing their diversity patterns across space and through time is of essential importance to better understand the underlying ecological mechanisms controlling the distribution and assembly of microbial communities. However, the diversity patterns and their underlying ecological mechanisms for different microbial domains and/or trophic levels require further exploration. In this study, the spatial scaling of different microbial domains and their associated ecological processes in a mudflat intertidal zone were investigated. The results showed different spatial scaling patterns for different microbial domains. Different ecological processes underlie the domain-level differentiation of microbial spatial scaling. This study links ecological processes with microbial spatial scaling to provide novel mechanistic insights into the diversity patterns of microorganisms that belong to different trophic levels.

Long-Term Effects of Soil Remediation with Willow Short Rotation Coppice on Biogeographic Pattern of Microbial Functional Genes.

Short rotation coppice (SRC) is increasingly being adopted for bioenergy production, pollution remediation and land restoration. However, its long-term effects on soil microbial communities are poorly characterized. Here, we studied soil microbial functional genes and their biogeographic pattern under SRC with willow trees as compared to those under permanent grassland (C). GeoChip analysis showed a lower functional gene diversity in SRC than in C soil, whereas microbial ATP and respiration did not change. The SRC soil had lower relative abundances of microbial genes encoding for metal(-oid) resistance, antibiotic resistance and stress-related proteins. This indicates a more benign habitat under SRC for microbial communities after relieving heavy metal stress, consistent with the lower phytoavailability of some metals (i.e., As, Cd, Ni and Zn) and higher total organic carbon, NO3−-N and P concentrations. The microbial taxa–area relationship was valid in both soils, but the space turnover rate was higher under SRC within 0.125 m2, which was possibly linked to a more benign environment under SRC, whereas similar values were reached beyond thisarea. Overall, we concluded that SRC management can be considered as a phytotechnology that ameliorates the habitat for soil microorganisms, owing to TOC and nutrient enrichment on the long-term.

Soil parameters, land use, and geographical distance drive soil bacterial communities along a European transect

To better understand the relationship between soil bacterial communities, soil physicochemical properties, land use and geographical distance, we considered for the first time ever a European transect running from Sweden down to Portugal and from France to Slovenia. We investigated 71 sites based on their range of variation in soil properties (pH, texture and organic matter), climatic conditions (Atlantic, alpine, boreal, continental, Mediterranean) and land uses (arable, forest and grassland). 16S rRNA gene amplicon pyrosequencing revealed that bacterial communities highly varied in diversity, richness, and structure according to environmental factors. At the European scale, taxa area relationship (TAR) was significant, supporting spatial structuration of bacterial communities. Spatial variations in community diversity and structure were mainly driven by soil physicochemical parameters. Within soil clusters (k-means approach) corresponding to similar edaphic and climatic properties, but to multiple land uses, land use was a major driver of the bacterial communities. Our analyses identified specific indicators of land use (arable, forest, grasslands) or soil conditions (pH, organic C, texture). These findings provide unprecedented information on soil bacterial communities at the European scale and on the drivers involved; possible applications for sustainable soil management are discussed.

Taxa-area relationship of aquatic fungi on deciduous leaves.

One of the fundamental patterns in macroecology is the increase in the number of observed taxa with size of sampled area. For microbes, the shape of this relationship remains less clear. The current study assessed the diversity of aquatic fungi, by the traditional approach based on conidial morphology (captures reproducing aquatic hyphomycetes) and next generation sequencing (NGS; captures other fungi as well), on graded sizes of alder leaves (0.6 to 13.6 cm2). Leaves were submerged in two streams in geographically distant locations: the Oliveira Stream in Portugal and the Boss Brook in Canada. Decay rates of alder leaves and fungal sporulation rates did not differ between streams. Fungal biomass was higher in Boss Brook than in Oliveira Stream, and in both streams almost 100% of the reads belonged to active fungal taxa. In general, larger leaf areas tended to harbour more fungi, but these findings were not consistent between techniques. Morphospecies-based diversity increased with leaf area in Boss Brook, but not in Oliveira Stream; metabarcoding data showed an opposite trend. The higher resolution of metabarcoding resulted in steeper taxa-accumulation curves than morphospecies-based assessments (fungal conidia morphology). Fungal communities assessed by metabarcoding were spatially structured by leaf area in both streams. Metabarcoding promises greater resolution to assess biodiversity patterns in aquatic fungi and may be more accurate for assessing taxa-area relationships and local to global diversity ratios.

The Protistan Microbiome of Grassland Soil: Diversity in the Mesoscale

Genomic data for less than one quarter of ∼1.8 million named species on earth exist in public databases like GenBank. Little information exists on the estimated one million small sized (1-100μm) heterotrophic nanoflagellates and ciliates and their taxa-area relationship. We analyzed environmental DNA from 150 geo-referenced grassland plots representing topographical and land-use ranges typical for Central Europe. High through-put barcoding allowed the identification of operational taxonomic units (OTUs) at species level, with high pairwise identity to reference sequences (≥99.7%), but also the identification of sequences at the genus (≥97%) and class (≥80%) taxonomic level. Species richness analyses revealed, on average, 100 genus level OTUs (332 unique individual read (UIR) and 56 class level OTUs per gram of soil sample in the mesoscale (1-1000km). Database shortfalls were highlighted by increased uncertain taxonomic lineages at lower resolution (≥80% sequence identity). No single barcode occurred ubiquitously across all sites. Taxa-area relationships indicated that OTUs spread over the entire mesoscale were more similar than in the local scale and increased land-use (fertilization, mowing and grazing) promoted taxa-area separation. Only a small fraction of sequences strictly matched reference library sequences, suggesting a large protistan "dark matter" in soil which warrants further research.

Dry Season Constrains Bacterial Phylogenetic Diversity in a Semi-Arid Rhizosphere System.

The rhizosphere is viewed as a deterministic environment led by the interaction between plants and microorganisms. In the case of semi-arid plants, this interaction is strengthened by the harshness of the environment. We tested the hypothesis that dry season represents a constraint on the bacterial diversity of the rhizosphere from semi-arid plants. To accomplish this, we sampled two leguminous species at five locations during the dry and rainy seasons in the Caatinga biome and characterised bacterial community structures using qPCR and 16S rRNA sequencing. We found that the main differences between seasons were due to reduced phylogenetic diversity caused by dryness. Variation partitioning indicated that environmental characteristics significant impacts in β-diversity. Additionally, distance decay relationship and taxa area relationship indicate a higher spatial turnover at the rainy season. During the dry season, decreased bacterial abundance is likely due to the selection of resistant or resilient microorganisms; with the return of the rain, the sensitive populations start to colonise the rhizosphere by a process that is strongly influenced by environmental characteristics. Thus, we propose that the reduction of PD and strong influence of environmental parameters on the assemblage of these communities make them prone to functional losses caused by climatic disturbances.

Biogeographic patterns of soil diazotrophic communities across six forests in North America.

Soil diazotrophs play important roles in ecosystem functioning by converting atmospheric N2 into biologically available ammonium. However, the diversity and distribution of soil diazotrophic communities in different forests and whether they follow biogeographic patterns similar to macroorganisms still remain unclear. By sequencing nifH gene amplicons, we surveyed the diversity, structure and biogeographic patterns of soil diazotrophic communities across six North American forests (126 nested samples). Our results showed that each forest harboured markedly different soil diazotrophic communities and that these communities followed traditional biogeographic patterns similar to plant and animal communities, including the taxa-area relationship (TAR) and latitudinal diversity gradient. Significantly higher community diversity and lower microbial spatial turnover rates (i.e. z-values) were found for rainforests (~0.06) than temperate forests (~0.1). The gradient pattern of TARs and community diversity was strongly correlated (r(2) >0.5) with latitude, annual mean temperature, plant species richness and precipitation, and weakly correlated (r(2) <0.25) with pH and soil moisture. This study suggests that even microbial subcommunities (e.g. soil diazotrophs) follow general biogeographic patterns (e.g. TAR, latitudinal diversity gradient), and indicates that the metabolic theory of ecology and habitat heterogeneity may be the major underlying ecological mechanisms shaping the biogeographic patterns of soil diazotrophic communities.

Distance-decay and taxa-area relationships for bacteria, archaea and methanogenic archaea in a tropical lake sediment.

The study of of the distribution of microorganisms through space (and time) allows evaluation of biogeographic patterns, like the species-area index (z). Due to their high dispersal ability, high reproduction rates and low rates of extinction microorganisms tend to be widely distributed, and they are thought to be virtually cosmopolitan and selected primarily by environmental factors. Recent studies have shown that, despite these characteristics, microorganisms may behave like larger organisms and exhibit geographical distribution. In this study, we searched patterns of spatial diversity distribution of bacteria and archaea in a contiguous environment. We collected 26 samples of a lake sediment, distributed in a nested grid, with distances between samples ranging from 0.01 m to 1000 m. The samples were analyzed using T-RFLP (Terminal restriction fragment length polymorphism) targeting mcrA (coding for a subunit of methyl-coenzyme M reductase) and the genes of Archaeal and Bacterial 16S rRNA. From the qualitative and quantitative results (relative abundance of operational taxonomic units) we calculated the similarity index for each pair to evaluate the taxa-area and distance decay relationship slopes by linear regression. All results were significant, with mcrA genes showing the highest slope, followed by Archaeal and Bacterial 16S rRNA genes. We showed that the microorganisms of a methanogenic community, that is active in a contiguous environment, display spatial distribution and a taxa-area relationship.

Improving soil bacterial taxa-area relationships assessment using DNA meta-barcoding.

The evaluation of the taxa-area relationship (TAR) with molecular fingerprinting data demonstrated the spatial structuration of soil microorganisms and provided insights into the processes shaping their diversity. The increasing use of massive sequencing technologies in biodiversity investigations has now raised the question of the advantages of such technologies over the fingerprinting approach for elucidation of the determinism of soil microbial community assembly in broad-scale biogeographic studies. Our objectives in this study were to compare DNA fingerprinting and meta-barcoding approaches for evaluating soil bacterial TAR and the determinism of soil bacterial community assembly on a broad scale. This comparison was performed on 392 soil samples from four French geographic regions with different levels of environmental heterogeneity. Both molecular approaches demonstrated a TAR with a significant slope but, because of its more sensitive description of soil bacterial community richness, meta-barcoding provided significantly higher and more accurate estimates of turnover rates. Both approaches were useful in evidencing the processes shaping bacterial diversity variations on a broad scale. When different taxonomic resolutions were considered for meta-barcoding data, they significantly influenced the estimation of turnover rates but not the relative importance of each component process. Altogether, DNA meta-barcoding provides a more accurate evaluation of the TAR and may lead to re-examination of the processes shaping soil bacterial community assembly. This should provide new insights into soil microbial ecology in the context of sustainable use of soil resources.

Bacterial taxa–area and distance–decay relationships in marine environments

The taxa–area relationship (TAR) and the distance–decay relationship (DDR) both describe spatial turnover of taxa and are central patterns of biodiversity. Here, we compared TAR and DDR of bacterial communities across different marine realms and ecosystems at the global scale. To obtain reliable global estimates for both relationships, we quantified the poorly assessed effects of sequencing depth, rare taxa removal and number of sampling sites. Slope coefficients of bacterial TARs were within the range of those of plants and animals, whereas slope coefficients of bacterial DDR were much lower. Slope coefficients were mostly affected by removing rare taxa and by the number of sampling sites considered in the calculations. TAR and DDR slope coefficients were overestimated at sequencing depth <4000 sequences per sample. Noticeably, bacterial TAR and DDR patterns did not correlate with each other both within and across ecosystem types, suggesting that (i) TAR cannot be directly derived from DDR and (ii) TAR and DDR may be influenced by different ecological factors. Nevertheless, we found marine bacterial TAR and DDR to be steeper in ecosystems associated with high environmental heterogeneity or spatial isolation, namely marine sediments and coastal environments compared with pelagic ecosystems. Hence, our study provides information on macroecological patterns of marine bacteria, as well as methodological and conceptual insights, at a time when biodiversity surveys increasingly make use of high-throughput sequencing technologies.

Turnover of soil bacterial diversity driven by wide-scale environmental heterogeneity

Spatial scaling and determinism of the wide-scale distribution of macroorganism diversity has been largely demonstrated over a century. For microorganisms, and especially for soil bacteria, this fundamental question requires more thorough investigation, as little information has been reported to date. Here by applying the taxa-area relationship to the largest spatially explicit soil sampling available in France (2,085 soils, area covered ~5.3 × 10(5) km(2)) and developing an innovative evaluation of the habitat-area relationship, we show that the turnover rate of bacterial diversity in soils on a wide scale is highly significant and strongly correlated with the turnover rate of soil habitat. As the diversity of micro- and macroorganisms appears to be driven by similar processes (dispersal and selection), maintaining diverse and spatially structured habitats is essential for soil biological patrimony and the resulting ecosystem services.

Taxa–area relationship and neutral dynamics influence the diversity of fungal communities on senesced tree leaves

This study utilized individual senesced sugar maple and beech leaves as natural sampling units within which to quantify saprotrophic fungal diversity. Quantifying communities in individual leaves allowed us to determine if fungi display a classic taxa-area relationship (species richness increasing with area). We found a significant taxa-area relationship for sugar maple leaves, but not beech leaves, consistent with Wright's species-energy theory. This suggests that energy availability as affected plant biochemistry is a key factor regulating the scaling relationships of fungal diversity. We also compared taxa rank abundance distributions to models associated with niche or neutral theories of community assembly, and tested the influence of leaf type as an environmental niche factor controlling fungal community composition. Among rank abundance distribution models, the zero-sum model derived from neutral theory showed the best fit to our data. Leaf type explained only 5% of the variability in community composition. Habitat (vernal pool, upland or riparian forest floor) and site of collection explained > 40%, but could be attributed to either niche or neutral processes. Hence, although niche dynamics may regulate fungal communities at the habitat scale, our evidence points towards neutral assembly of saprotrophic fungi on individual leaves, with energy availability constraining the taxa-area relationship.

Biogeography of soil microbial communities: a review and a description of the ongoing french national initiative

Microbial biogeography is the study of the distribution of microbial diversity on large scales of space and time. This science aims at understanding biodiversity regulation and its link with ecosystem biological functioning, goods and services such as maintenance of productivity, of soil and atmospheric quality, and of soil health. Although the initial concept dates from the early 20th century (Beijerinck (1913) De infusies en de ontdekking der backterien, in: Jaarboek van de Knoniklijke Akademie van Wetenschappen, Muller, Amsterdam), only recently have an increasing number of studies have investigated the biogeographical patterns of soil microbial diversity. A such delay is due to the constraints of the microbial models, the need to develop relevant molecular and bioinformatic tools to assess microbial diversity, and the non-availability of an adequate sampling strategy. Consequently, the conclusions from microbial ecology studies have rarely been generally applicable and even the fundamental power-laws differ because the taxa-area relationship and the influence of global and distal parameters on the spatial distribution of microbial communities have not been examined. In this article we define and discuss the scientific, technical and operational limits and outcomes resulting from soil microbial biogeography together with the technical and logistical feasibility. The main results are that microbial communities are not stochastically distributed on a wide scale and that biogeographical patterns are more influenced by local parameters such as soil type and land use than by distal ones, e.g. climate and geomorphology, contrary to plants and animals. We then present the European soil biological survey network, focusing on the French national initiative and the „ECOMIC-RMQS” project. The objective of the ECOMIC-RMQS project is to characterise the density and diversity of bacterial communities in all soils in the RMQS library in order to assess, for the first time, not only microbial biogeography across the whole of France but also the impact of land use on soil biodiversity (Reseau de Mesures de la Qualite des Sols = French Soil Quality Monitoring Network, 2200 soils covering all the French territory with a systematic grid of sampling). The scientific, technical and logistical outputs are examined with a view to the future prospects needed to develop this scientific domain and its applications in sustainable land use.

The Concept of Taxon Invariance in Ecology: Do Diversity Patterns Vary with Changes in Taxonomic Resolution?

Diversity patterns cannot be properly interpreted without a theory providing criteria for their evaluation. We propose a concept to prevent artifictions caused by improper consideration of changes in observed patterns due to variation in taxon delimitation. Most biodiversity patterns concern assemblages of species of given higher taxon (e.g. class). Some patterns seem to be universal, e.g., body size distribution, species-abundance distribution, species-area relationship, or the relationship between diversity and energy availability. However, truly universal patterns should not change when we change taxonomic scope by focusing on subtaxa or when we merge several sister taxa together and analyze patterns in resulting higher taxon. Similarly, some patterns may not change when changing the basic unit of the study e.g., when replacing species by genera or families (or any monophyletic clades), although other patterns may not be invariant against the variation of the basic unit. In fact, there are only two possibilities: biodiversity patterns are either taxon-invariant or they vary systematically with taxonomic resolution, which would indicate some fundamental taxonomic level with interesting implications for biological processes behind those patterns. Here we develop the concept of taxon invariance of diversity patterns and apply it on the abovementioned patterns. We show that simple theoretical considerations markedly constrain the set of possible patterns, as some of them cannot be simultaneously valid for both a taxon and its subtaxa – frequency distributions of abundances cannot be simultaneously lognormal for a given taxon and all its subtaxa, the taxa-area relationship cannot follow a power-law for all levels of taxonomic resolution, and energy availability cannot affect diversity of all taxonomic units in the same way. Analyses of the variation in the form of biodiversity patterns with changing taxonomic resolution thus provide an extremely useful tool for revealing properties of respective patterns, their universality and logical consistency.

Numerical abundance and biodiversity of below‐ground taxocenes along a pH gradient across the Netherlands

AbstractAim Taxocenes are regulated by different kinds of predictors, but can broad‐scale patterns of prokaryotes (bacteria) and eukaryotes (such as fungi and invertebrates) be ascribed to soil acidity? We sought to test for relationships between the numerical abundances of bacteria, microfungi, nematodes and arthropods along a pH gradient.Location 284 agro‐ecosystems on Pleistocene sand across the Netherlands.Methods Generalized Linear Models (GLM) and stepwise regressions were applied, using soil‐ and leaf‐litter organisms sampled from a land‐cover network.Results The major variation in the numerical abundance of the organisms belonging to the investigated taxocenes could be ascribed to soil acidity. Contrary to expectations, the effects of temperature on numerical abundance were significant only for Fungi and Nematoda (P &lt; 0.0001). Geographical co‐ordinates always play a minor role. The often‐suggested close correlation between the numerical abundance of eukaryotes and their local taxonomic diversity applied only to Arthropoda and Fungi (P &lt; 0.00001). Only the number of bacterial DNA bands seemed to reflect the taxa–area relationship (F‐value = 22.45,P &lt; 0.0001).Main conclusions There were strong relationships between the numerical abundances of all the investigated taxocenes and the field‐measured soil acidity (P &lt; 0.0001). The largest effects were detected in the Fungi, which tended to be much more acid‐tolerant than Bacteria. These patterns imply ecological shifts in the detrital soil food web and deserve further investigation.

A taxa–area relationship for bacteria

A positive power-law relationship between the number of species in an area and the size of that area has been observed repeatedly in plant and animal communities. This species-area relationship, thought to be one of the few laws in ecology, is fundamental to our understanding of the distribution of global biodiversity. However, such a relationship has not been reported for bacteria, and little is known regarding the spatial distribution of bacteria, relative to what is known of plants and animals. Here we describe a taxa-area relationship for bacteria over a scale of centimetres to hundreds of metres in salt marsh sediments. We found that bacterial communities located close together were more similar in composition than communities located farther apart, and we used the decay of community similarity with distance to show that bacteria can exhibit a taxa-area relationship. This relationship was driven primarily by environmental heterogeneity rather than geographic distance or plant composition.

Spatial scaling of microbial eukaryote diversity

Patterns in the spatial distribution of organisms provide important information about mechanisms that regulate the diversity of life and the complexity of ecosystems. Although microorganisms may comprise much of the Earth's biodiversity and have critical roles in biogeochemistry and ecosystem functioning, little is known about their spatial diversification. Here we present quantitative estimates of microbial community turnover at local and regional scales using the largest spatially explicit microbial diversity data set available (> 10(6) sample pairs). Turnover rates were small across large geographical distances, of similar magnitude when measured within distinct habitats, and did not increase going from one vegetation type to another. The taxa-area relationship of these terrestrial microbial eukaryotes was relatively flat (slope z = 0.074) and consistent with those reported in aquatic habitats. This suggests that despite high local diversity, microorganisms may have only moderate regional diversity. We show how turnover patterns can be used to project taxa-area relationships up to whole continents. Taxa dissimilarities across continents and between them would strengthen these projections. Such data do not yet exist, but would be feasible to collect.