Niche types and community assembly.

Studies of niche differentiation and biodiversity often focus on a few niche dimensions due to the methodological challenge of describing hyperdimensional niche space. However, this may limit our understanding of community assembly processes. We used the full spectrum of realized niche types to study arbuscular mycorrhizal fungal communities: distinguishing abiotic and biotic, and condition and resource, axes. Estimates of differentiation in relation to different niche types were only moderately correlated. However, coexisting taxon niches were consistently less differentiated than expected, based on a regional null model, indicating the importance of habitat filtering at that scale. Nonetheless, resource niches were relatively more differentiated than condition niches, which is consistent with the effect of a resource niche-based coexistence mechanism. Considering niche types, and in particular distinguishing resource and condition niches, provides a more complete understanding of community assembly, compared with studying individual niche axes or the full niche.

Connecting the multiple dimensions of global soil fungal diversity.

How the multiple facets of soil fungal diversity vary worldwide remains virtually unknown, hindering the management of this essential species-rich group. By sequencing high-resolution DNA markers in over 4000 topsoil samples from natural and human-altered ecosystems across all continents, we illustrate the distributions and drivers of different levels of taxonomic and phylogenetic diversity of fungi and their ecological groups. We show the impact of precipitation and temperature interactions on local fungal species richness (alpha diversity) across different climates. Our findings reveal how temperature drives fungal compositional turnover (beta diversity) and phylogenetic diversity, linking them with regional species richness (gamma diversity). We integrate fungi into the principles of global biodiversity distribution and present detailed maps for biodiversity conservation and modeling of global ecological processes.

Plant-symbiotic fungal diversity tracks variation in vegetation and the abiotic environment along an extended elevational gradient in the Himalayas.

Arbuscular mycorrhizal (AM) fungi can benefit plants under environmental stress, and influence plant adaptation to warmer climates. However, very little is known about the ecology of these fungi in alpine environments. We sampled plant roots along a large fraction (1941-6150 m asl (above sea level)) of the longest terrestrial elevational gradient on Earth and used DNA metabarcoding to identify AM fungi. We hypothesized that AM fungal alpha and beta diversity decreases with increasing elevation, and that different vegetation types comprise dissimilar communities, with cultured (putatively ruderal) taxa increasingly represented at high elevations. We found that the alpha diversity of AM fungal communities declined linearly with elevation, whereas within-site taxon turnover (beta diversity) was unimodally related to elevation. The composition of AM fungal communities differed between vegetation types and was influenced by elevation, mean annual temperature, and precipitation. In general, Glomeraceae taxa dominated at all elevations and vegetation types; however, higher elevations were associated with increased presence of Acaulosporaceae, Ambisporaceae, and Claroideoglomeraceae. Contrary to our expectation, the proportion of cultured AM fungal taxa in communities decreased with elevation. These results suggest that, in this system, climate-induced shifts in habitat conditions may facilitate more diverse AM fungal communities at higher elevations but could also favour ruderal taxa.

Metabarcoding of soil environmental DNA to estimate plant diversity globally.

Introduction: Traditional approaches to collecting large-scale biodiversity data pose huge logistical and technical challenges. We aimed to assess how a comparatively simple method based on sequencing environmental DNA (eDNA) characterises global variation in plant diversity and community composition compared with data derived from traditional plant inventory methods. Methods: We sequenced a short fragment (P6 loop) of the chloroplast trnL intron from from 325 globally distributed soil samples and compared estimates of diversity and composition with those derived from traditional sources based on empirical (GBIF) or extrapolated plant distribution and diversity data. Results: Large-scale plant diversity and community composition patterns revealed by sequencing eDNA were broadly in accordance with those derived from traditional sources. The success of the eDNA taxonomy assignment, and the overlap of taxon lists between eDNA and GBIF, was greatest at moderate to high latitudes of the northern hemisphere. On average, around half (mean: 51.5% SD 17.6) of local GBIF records were represented in eDNA databases at the species level, depending on the geographic region. Discussion: eDNA trnL gene sequencing data accurately represent global patterns in plant diversity and composition and thus can provide a basis for large-scale vegetation studies. Important experimental considerations for plant eDNA studies include using a sampling volume and design to maximise the number of taxa detected and optimising the sequencing depth. However, increasing the coverage of reference sequence databases would yield the most significant improvements in the accuracy of taxonomic assignments made using the P6 loop of the trnL region.

Global diversity and distribution of nitrogen-fixing bacteria in the soil.

Our knowledge of microbial biogeography has advanced in recent years, yet we lack knowledge of the global diversity of some important functional groups. Here, we used environmental DNA from 327 globally collected soil samples to investigate the biodiversity patterns of nitrogen-fixing bacteria by focusing on the nifH gene but also amplifying the general prokaryotic 16S SSU region. Globally, N-fixing prokaryotic communities are driven mainly by climatic conditions, with most groups being positively correlated with stable hot or seasonally humid climates. Among soil parameters, pH, but also soil N content were most often shown to correlate with the diversity of N-fixer groups. However, specific groups of N-fixing prokaryotes show contrasting responses to the same variables, notably in Cyanobacteria that were negatively correlated with stable hot climates, and showed a U-shaped correlation with soil pH, contrary to other N-fixers. Also, the non-N-fixing prokaryotic community composition was differentially correlated with the diversity and abundance of N-fixer groups, showing the often-neglected impact of biotic interactions among bacteria.

Do commercial arbuscular mycorrhizal inoculants contain the species that they claim?

The use of arbuscular mycorrhizal (AM) fungal inoculants as a means to promote plant growth is gaining momentum worldwide. Although there is an increasing number of commercial products available for various applications, the quality of these remains uncertain. We determined the AM fungal species composition in eleven inoculants from four producers by using DNA metabarcoding and compared them to the AM fungal species declared on the product labels. Our DNA metabarcoding of the inoculants revealed a concerning discrepancy between the declared and detected AM fungal species compositions of the products. While nine products contained at least one declared species, two did not contain any matching species and all inoculants but one contained additional species not declared on the product label. These findings highlight the need for better guidelines and industry standards to ensure consumer protection in the AM fungal inoculum market. Additionally, we call for caution when using commercial AM fungal inoculants in scientific experiments without confirmatory information about their species composition.

Global patterns in endemicity and vulnerability of soil fungi.

Fungi are highly diverse organisms, which provide multiple ecosystem services. However, compared with charismatic animals and plants, the distribution patterns and conservation needs of fungi have been little explored. Here, we examined endemicity patterns, global change vulnerability and conservation priority areas for functional groups of soil fungi based on six global surveys using a high-resolution, long-read metabarcoding approach. We found that the endemicity of all fungi and most functional groups peaks in tropical habitats, including Amazonia, Yucatan, West-Central Africa, Sri Lanka, and New Caledonia, with a negligible island effect compared with plants and animals. We also found that fungi are predominantly vulnerable to drought, heat and land-cover change, particularly in dry tropical regions with high human population density. Fungal conservation areas of highest priority include herbaceous wetlands, tropical forests, and woodlands. We stress that more attention should be focused on the conservation of fungi, especially root symbiotic arbuscular mycorrhizal and ectomycorrhizal fungi in tropical regions as well as unicellular early-diverging groups and macrofungi in general. Given the low overlap between the endemicity of fungi and macroorganisms, but high conservation needs in both groups, detailed analyses on distribution and conservation requirements are warranted for other microorganisms and soil organisms.

Dominance, diversity, and niche breadth in arbuscular mycorrhizal fungal communities.

Classical theory identifies resource competition as the major structuring force of biotic communities and predicts that (i) levels of dominance and richness in communities are inversely related, (ii) narrow niches allow dense "packing" in niche space and thus promote diversity, and (iii) dominants are generalists with wide niches, such that locally abundant taxa also exhibit wide distributions. Current empirical support, however, is mixed. We tested these expectations using published data on arbuscular mycorrhizal (AM) fungal community composition worldwide. We recorded the expected negative relationship between dominance and richness and, to a degree, the positive association between local and global dominance. However, contrary to expectations, dominance was pronounced in communities where more specialists were present and, conversely, richness was higher in communities with more generalists. Thus, resource competition and niche packing appear to be of limited importance in AM fungal community assembly; rather, patterns of dominance and diversity seem more consistent with habitat filtering and stochastic processes.

Global taxonomic and phylogenetic assembly of AM fungi.

Arbuscular mycorrhizal (AM) fungi are a ubiquitous group of plant symbionts, yet processes underlying their global assembly - in particular the roles of dispersal limitation and historical drivers - remain poorly understood. Because earlier studies have reported niche conservatism in AM fungi, we hypothesized that variation in taxonomic community composition (i.e., unweighted by taxon relatedness) should resemble variation in phylogenetic community composition (i.e., weighted by taxon relatedness) which reflects ancestral adaptations to historical habitat gradients. Because of the presumed strong dispersal ability of AM fungi, we also anticipated that the large-scale structure of AM fungal communities would track environmental conditions without regional discontinuity. We used recently published AM fungal sequence data (small-subunit ribosomal RNA gene) from soil samples collected worldwide to reconstruct global patterns in taxonomic and phylogenetic community variation. The taxonomic structure of AM fungal communities was primarily driven by habitat conditions, with limited regional differentiation, and there were two well-supported clusters of communities - occurring in cold and warm conditions. Phylogenetic structure was driven by the same factors, though all relationships were markedly weaker. This suggests that niche conservatism with respect to habitat associations is weakly expressed in AM fungal communities. We conclude that the composition of AM fungal communities tracks major climatic and edaphic gradients, with the effects of dispersal limitation and historic factors considerably less apparent than those of climate and soil.

Temperature and pH define the realised niche space of arbuscular mycorrhizal fungi.

The arbuscular mycorrhizal (AM) fungi are a globally distributed group of soil organisms that play critical roles in ecosystem function. However, the ecological niches of individual AM fungal taxa are poorly understood. We collected > 300 soil samples from natural ecosystems worldwide and modelled the realised niches of AM fungal virtual taxa (VT; approximately species-level phylogroups). We found that environmental and spatial variables jointly explained VT distribution worldwide, with temperature and pH being the most important abiotic drivers, and spatial effects generally occurring at local to regional scales. While dispersal limitation could explain some variation in VT distribution, VT relative abundance was almost exclusively driven by environmental variables. Several environmental and spatial effects on VT distribution and relative abundance were correlated with phylogeny, indicating that closely related VT exhibit similar niche optima and widths. Major clades within the Glomeraceae exhibited distinct niche optima, Acaulosporaceae generally had niche optima in low pH and low temperature conditions, and Gigasporaceae generally had niche optima in high precipitation conditions. Identification of the realised niche space occupied by individual and phylogenetic groups of soil microbial taxa provides a basis for building detailed hypotheses about how soil communities respond to gradients and manipulation in ecosystems worldwide.

Microbial island biogeography: isolation shapes the life history characteristics but not diversity of root-symbiotic fungal communities.

Island biogeography theory is one of the most influential paradigms in ecology. That island characteristics, including remoteness, can profoundly modulate biological diversity has been borne out by studies of animals and plants. By contrast, the processes influencing microbial diversity in island systems remain largely undetermined. We sequenced arbuscular mycorrhizal (AM) fungal DNA from plant roots collected on 13 islands worldwide and compared AM fungal diversity on islands with existing data from mainland sites. AM fungal communities on islands (even those >6000 km from the closest mainland) comprised few endemic taxa and were as diverse as mainland communities. Thus, in contrast to patterns recorded among macro-organisms, efficient dispersal appears to outweigh the effects of taxogenesis and extinction in regulating AM fungal diversity on islands. Nonetheless, AM fungal communities on more distant islands comprised a higher proportion of previously cultured and large-spored taxa, indicating that dispersal may be human-mediated or require tolerance of significant environmental stress, such as exposure to sunlight or high salinity. The processes driving large-scale patterns of microbial diversity are a key consideration for attempts to conserve and restore functioning ecosystems in this era of rapid global change.

Anthropogenic disturbance equalizes diversity levels in arbuscular mycorrhizal fungal communities.

The arbuscular mycorrhizal (AM) symbiosis is a key plant-microbe interaction in sustainable functioning ecosystems. Increasing anthropogenic disturbance poses a threat to AM fungal communities worldwide, but there is little empirical evidence about its potential negative consequences. In this global study, we sequenced AM fungal DNA in soil samples collected from pairs of natural (undisturbed) and anthropogenic (disturbed) plots in two ecosystem types (10 naturally wooded and six naturally unwooded ecosystems). We found that ecosystem type had stronger directional effects than anthropogenic disturbance on AM fungal alpha and beta diversity. However, disturbance increased alpha and beta diversity at sites where natural diversity was low and decreased diversity at sites where natural diversity was high. Cultured AM fungal taxa were more prevalent in anthropogenic than natural plots, probably due to their efficient colonization strategies and ability to recover from disturbance. We conclude that anthropogenic disturbance does not have a consistent directional effect on AM fungal diversity; rather, disturbance equalizes levels of diversity at large scales and causes changes in community functional structure.

Fungal root symbionts of high-altitude vascular plants in the Himalayas.

Arbuscular mycorrhizal fungi (AMF) and dark septate endophytes (DSE) form symbiotic relationships with plants influencing their productivity, diversity and ecosystem functions. Only a few studies on these fungi, however, have been conducted in extreme elevations and none over 5500 m a.s.l., although vascular plants occur up to 6150 m a.s.l. in the Himalayas. We quantified AMF and DSE in roots of 62 plant species from contrasting habitats along an elevational gradient (3400-6150 m) in the Himalayas using a combination of optical microscopy and next generation sequencing. We linked AMF and DSE communities with host plant evolutionary history, ecological preferences (elevation and habitat type) and functional traits. We detected AMF in elevations up to 5800 m, indicating it is more constrained by extreme conditions than the host plants, which ascend up to 6150 m. In contrast, DSE were found across the entire gradient up to 6150 m. AMF diversity was unimodally related to elevation and positively related to the intensity of AMF colonization. Mid-elevation steppe and alpine plants hosted more diverse AMF communities than plants from deserts and the subnival zone. Our results bring novel insights to the abiotic and biotic filters structuring AMF and DSE communities in the Himalayas.

Applying the dark diversity concept to nature conservation.

Linking diversity to biological processes is central for developing informed and effective conservation decisions. Unfortunately, observable patterns provide only a proportion of the information necessary for fully understanding the mechanisms and processes acting on a particular population or community. We suggest conservation managers use the often overlooked information relative to species absences and pay particular attention to dark diversity (i.e., a set of species that are absent from a site but that could disperse to and establish there, in other words, the absent portion of a habitat-specific species pool). Together with existing ecological metrics, concepts, and conservation tools, dark diversity can be used to complement and further develop conservation prioritization and management decisions through an understanding of biodiversity relativized by its potential (i.e., its species pool). Furthermore, through a detailed understanding of the population, community, and functional dark diversity, the restoration potential of degraded habitats can be more rigorously assessed and so to the likelihood of successful species invasions. We suggest the application of the dark diversity concept is currently an underappreciated source of information that is valuable for conservation applications ranging from macroscale conservation prioritization to more locally scaled restoration ecology and the management of invasive species.

The Root-Associated Microbial Community of the World's Highest Growing Vascular Plants.

Upward migration of plants to barren subnival areas is occurring worldwide due to raising ambient temperatures and glacial recession. In summer 2012, the presence of six vascular plants, growing in a single patch, was recorded at an unprecedented elevation of 6150 m.a.s.l. close to the summit of Mount Shukule II in the Western Himalayas (Ladakh, India). Whilst showing multiple signs of stress, all plants have managed to establish stable growth and persist for several years. To learn about the role of microbes in the process of plant upward migration, we analysed the root-associated microbial community of the plants (three individuals from each) using microscopy and tagged amplicon sequencing. No mycorrhizae were found on the roots, implying they are of little importance to the establishment and early growth of the plants. However, all roots were associated with a complex bacterial community, with richness and diversity estimates similar or even higher than the surrounding bare soil. Both soil and root-associated communities were dominated by members of the orders Sphingomonadales and Sphingobacteriales, which are typical for hot desert soils, but were different from communities of temperate subnival soils and typical rhizosphere communities. Despite taxonomic similarity on the order level, the plants harboured a unique set of highly dominant operational taxonomic units which were not found in the bare soil. These bacteria have been likely transported with the dispersing seeds and became part of the root-associated community following germination. The results indicate that developing soils act not only as a source of inoculation to plant roots but also possibly as a sink for plant-associated bacteria.

Vegetation dynamics at the upper elevational limit of vascular plants in Himalaya.

A rapid warming in Himalayas is predicted to increase plant upper distributional limits, vegetation cover and abundance of species adapted to warmer climate. We explored these predictions in NW Himalayas, by revisiting uppermost plant populations after ten years (2003-2013), detailed monitoring of vegetation changes in permanent plots (2009-2012), and age analysis of plants growing from 5500 to 6150 m. Plant traits and microclimate variables were recorded to explain observed vegetation changes. The elevation limits of several species shifted up to 6150 m, about 150 vertical meters above the limit of continuous plant distribution. The plant age analysis corroborated the hypothesis of warming-driven uphill migration. However, the impact of warming interacts with increasing precipitation and physical disturbance. The extreme summer snowfall event in 2010 is likely responsible for substantial decrease in plant cover in both alpine and subnival vegetation and compositional shift towards species preferring wetter habitats. Simultaneous increase in summer temperature and precipitation caused rapid snow melt and, coupled with frequent night frosts, generated multiple freeze-thaw cycles detrimental to subnival plants. Our results suggest that plant species responses to ongoing climate change will not be unidirectional upward range shifts but rather multi-dimensional, species-specific and spatially variable.