Rare taxa maintain the stability of crop mycobiomes and ecosystem functions

Plants harbour highly diverse mycobiomes which sustain essential functions for host health and productivity. However, ecological processes that govern the plant–mycobiome assembly, interactions and their impact on ecosystem functions remain poorly known. Here we characterized the ecological role and community assembly of both abundant and rare fungal taxa along the soil–plant continuums (rhizosphere, phyllosphere and endosphere) in the maize–wheat/barley rotation system under different fertilization practices at two contrasting sites. Our results indicate that mycobiome assembly is shaped predominantly by compartment niche and host species rather than by environmental factors. Moreover, crop-associated fungal communities are dominated by few abundant taxa mainly belonging to Sordariomycetes and Dothideomycetes, while the majority of diversity within mycobiomes are represented by rare taxa. For plant compartments, the abundant sub-community is mainly determined by stochastic processes. In contrast, the rare sub-community is more sensitive to host selection and mainly governed by deterministic processes. Furthermore, our results demonstrate that rare taxa play an important role in fungal co-occurrence network and ecosystem functioning like crop yield and soil enzyme activities. These results significantly advance our understanding of crop mycobiome assembly and highlight the key role of rare taxa in sustaining the stability of crop mycobiomes and ecosystem functions.     

Biogeographical patterns of abundant and rare bacterial biospheres in paddy soils across East Asia

Soil bacterial communities play fundamental roles in ecosystem functioning and often display a skewed distribution of abundant and rare taxa. So far, relatively little is known about the biogeographical patterns and mechanisms structuring the assembly of abundant and rare biospheres of soil bacterial communities. Here, we studied the geographical distribution of different bacterial sub-communities by examining the relative influence of environmental selection and dispersal limitation on taxa distributions in paddy soils across East Asia. Our results indicated that the geographical patterns of four different bacterial sub-communities consistently displayed significant distance–decay relationships (DDRs). In addition, we found niche breadth and dispersal rates to significantly explain differences in community assembly of abundant and rare taxa, directly affecting the strength of DDRs. While conditionally rare and abundant taxa displayed the strongest DDR due to higher environmental filtering and dispersal limitation, moderate taxa sub-communities had the weakest DDR due to greater environmental tolerance and dispersal rate. Random forest models indicated that soil pH (9.13%–49.78%) and average annual air temperature (16.59%–46.49%) were the most important predictors of the variation in the bacterial community. This study advances our understanding of the intrinsic links between fundamental ecological processes and microbial biogeographical patterns in paddy soils.     

Interaction and assembly processes of abundant and rare microbial communities during a diatom bloom process

Diatom blooms can significantly influence the dynamics of microbial communities, yet little is known about the interaction and assembly mechanisms of abundant and rare taxa during bloom process. Here, using 16S rRNA gene amplicon sequencing, we investigated the co-occurrence patterns and assembly processes of abundant and rare microbial communities during an early spring diatom bloom in Xiangshan bay. Our results showed that α-diversity indices in the rare subcommunity (RS) were significantly higher than those in the abundant and common subcommunities. β-Diversity of the RS was the highest among three subcommunities, and the variation of β-diversity in the three subcommunities was mainly induced by species turnover, which was also the highest in the RS. The assembly of microbial communities was mainly driven by the neutral processes, but the roles of neutral processes might differ in each subcommunity. Co-occurrence network analysis revealed that abundant and common operational taxonomic units were more often located in central positions within the network. Most of the modules in the network were specific to a particular bloom stage, owing to the succession of Skeletonema costatum. Overall, these findings expand current understanding of the microbial interaction and assembly mechanisms in marine environment suffering harmful algal bloom disturbance.     

Environmental and biotic drivers of soil microbial β‐diversity across spatial and phylogenetic scales

Soil microbial communities play a key role in ecosystem functioning but still little is known about the processes that determine their turnover (β‐diversity) along ecological gradients. Here, we characterize soil microbial β‐diversity at two spatial scales and at multiple phylogenetic grains to ask how archaeal, bacterial and fungal communities are shaped by abiotic processes and biotic interactions with plants. We characterized microbial and plant communities using DNA metabarcoding of soil samples distributed across and within eighteen plots along an elevation gradient in the French Alps. The recovered taxa were placed onto phylogenies to estimate microbial and plant β‐diversity at different phylogenetic grains (i.e. resolution). We then modeled microbial β‐diversities with respect to plant β‐diversities and environmental dissimilarities across plots (landscape scale) and with respect to plant β‐diversities and spatial distances within plots (plot scale). At the landscape scale, fungal and archaeal β‐diversities were mostly related to plant β‐diversity, while bacterial β‐diversities were mostly related to environmental dissimilarities. At the plot scale, we detected a modest covariation of bacterial and fungal β‐diversities with plant β‐diversity; as well as a distance–decay relationship that suggested the influence of ecological drift on microbial communities. In addition, the covariation between fungal and plant β‐diversity at the plot scale was highest at fine or intermediate phylogenetic grains hinting that biotic interactions between those clades depends on early‐evolved traits. Altogether, we show how multiple ecological processes determine soil microbial community assembly at different spatial scales and how the strength of these processes change among microbial clades. In addition, we emphasized the imprint of microbial and plant evolutionary history on today's microbial community structure.     

Biogeography and ecological diversity patterns of rare and abundant bacteria in oil‐contaminated soils

Revealing the biogeographies and ecologies of rare and abundant microorganisms is crucial to understand ecosystem diversity and function. In this study, we investigated the biogeographic assemblies and ecological diversity patterns of rare and abundant bacteria in long‐term oil‐contaminated soils at intervals of 46–360 km by performing high‐throughput sequencing of 16S rRNA genes. The results clearly revealed distinct distribution patterns for rare and abundant bacteria in soil samples. Rare taxa were unevenly distributed; however, abundant taxa were ubiquitous across all samples. Both rare and abundant subcommunities showed significant distance–decay relationships, and their assemblies were driven by different factors. The rare subcommunity primarily exhibited a spatially structured distribution (i.e., stochastic processes), while edaphic factors (i.e., deterministic processes) largely contributed to the structure of the abundant subcommunity. A network analysis revealed closer relationships between abundant bacteria and their heightened influence on other co‐occurrences in the community compared with rare species. In conclusion, rare microbial taxa may play potential roles in maintaining ecosystem diversity, although they do not appear to be central to microbial networks. Abundant microbes are vital for microbial co‐occurrences in oil‐contaminated soils, and high relative abundance and ubiquitous distribution suggest potential roles in the degradation of organic pollutants.     

Higher contribution of globally rare bacterial taxa reflects environmental transitions across the surface ocean

Microbial taxa range from being ubiquitous and abundant across space to extremely rare and endemic, depending on their ecophysiology and on different processes acting locally or regionally. However, little is known about how cosmopolitan or rare taxa combine to constitute communities and whether environmental variations promote changes in their relative abundances. Here we identified the Spatial Abundance Distribution (SpAD) of individual prokaryotic taxa (16S rDNA‐defined Operational Taxonomic Units, OTUs) across 108 globally‐distributed surface ocean stations. We grouped taxa based on their SpAD shape (“normal‐like”‐ abundant and ubiquitous; “logistic”‐ globally rare, present in few sites; and “bimodal”‐ abundant only in certain oceanic regions), and investigated how the abundance of these three categories relates to environmental gradients. Most surface assemblages were numerically dominated by a few cosmopolitan “normal‐like” OTUs, yet there was a gradual shift towards assemblages dominated by “logistic” taxa in specific areas with productivity and temperature differing the most from the average conditions in the sampled stations. When we performed the SpAD categorization including additional habitats (deeper layers and particles of varying sizes), the SpAD of many OTUs changed towards fewer “normal‐like” shapes, and OTUs categorized as globally rare in the surface ocean became abundant. This suggests that understanding the mechanisms behind microbial rarity and dominance requires expanding the context of study beyond local communities and single habitats. We show that marine bacterial communities comprise taxa displaying a continuum of SpADs, and that variations in their abundances can be linked to habitat transitions or barriers that delimit the distribution of community members.     

Soil pH and temperature regulate assembly processes of abundant and rare bacterial communities in agricultural ecosystems

The factors determining stochastic and deterministic processes that drive microbial community structure, specifically the balance of abundant and rare bacterial taxa, remain underexplored. Here we examined biogeographic patterns of abundant and rare bacterial taxa and explored environmental factors influencing their community assembly processes in agricultural fields across eastern China. More phylogenetic turnover correlating with spatial distance was observed in abundant than rare sub-communities. Homogeneous selection was the main assembly process for both the abundant and rare sub-communities; however, the abundant sub-community was more tightly clustered phylogenetically and was more sensitive to dispersal limitations than the rare sub-community. Rare sub-community of rice fields and abundant sub-community of maize fields were more governed by stochastic assembly processes, which showed higher operational taxonomic unit richness. We propose a conceptual paradigm wherein soil pH and mean annual temperature mediate the assembly of the abundant and rare sub-communities respectively. A higher soil pH leads to deterministic assembly of the abundant sub-community. For the rare sub-community, the dominance of stochasticity in low-temperature regions indicates weaker niche-based exclusion and the arrival of more evolutionary lineages. These findings suggest that the community assembly processes for abundant and rare bacterial taxa are dependent on distinct environmental variables in agro-ecosystems.     

Environmental filtering affects soil fungal community composition more than dispersal limitation at regional scales

The relative importance of dispersal limitation versus environmental filtering for community assembly has received much attention for macroorganisms. These processes have only recently been examined in microbial communities. Instead, microbial dispersal has mostly been measured as community composition change over space (i.e., distance decay). Here we directly examined fungal composition in airborne wind currents and soil fungal communities across a 40 000 km² regional landscape to determine if dispersal limitation or abiotic factors were structuring soil fungal communities. Over this landscape, neither airborne nor soil fungal communities exhibited compositional differences due to geographic distance. Airborne fungal communities shifted temporally while soil fungal communities were correlated with abiotic parameters. These patterns suggest that environmental filtering may have the largest influence on fungal regional community assembly in soils, especially for aerially dispersed fungal taxa. Furthermore, we found evidence that dispersal of fungal spores differs between fungal taxa and can be both a stochastic and deterministic process. The spatial range of soil fungal taxa was correlated with their average regional abundance across all sites, which may imply stochastic dispersal mechanisms. Nevertheless, spore volume was also negatively correlated with spatial range for some species. Smaller volume spores may be adapted to long-range dispersal, or establishment, suggesting that deterministic fungal traits may also influence fungal distributions. Fungal life-history traits may influence their distributions as well. Hypogeous fungal taxa exhibited high local abundance, but small spatial ranges, while epigeous fungal taxa had lower local abundance, but larger spatial ranges. This study is the first, to our knowledge, to directly sample air dispersal and soil fungal communities simultaneously across a regional landscape. We provide some of the first evidence that soil fungal communities are mostly assembled through environmental filtering and experience little dispersal limitation.     

Soil fungal communities of grasslands are environmentally structured at a regional scale in the Alps

Studying patterns of species distributions along elevation gradients is frequently used to identify the primary factors that determine the distribution, diversity and assembly of species. However, despite their crucial role in ecosystem functioning, our understanding of the distribution of below‐ground fungi is still limited, calling for more comprehensive studies of fungal biogeography along environmental gradients at various scales (from regional to global). Here, we investigated the richness of taxa of soil fungi and their phylogenetic diversity across a wide range of grassland types along a 2800 m elevation gradient at a large number of sites (213), stratified across a region of the Western Swiss Alps (700 km²). We used 454 pyrosequencing to obtain fungal sequences that were clustered into operational taxonomic units (OTUs). The OTU diversity–area relationship revealed uneven distribution of fungal taxa across the study area (i.e. not all taxa are everywhere) and fine‐scale spatial clustering. Fungal richness and phylogenetic diversity were found to be higher in lower temperatures and higher moisture conditions. Climatic and soil characteristics as well as plant community composition were related to OTU alpha, beta and phylogenetic diversity, with distinct fungal lineages suggesting distinct ecological tolerances. Soil fungi, thus, show lineage‐specific biogeographic patterns, even at a regional scale, and follow environmental determinism, mediated by interactions with plants.     

Fungal infection alters the selection,dispersal and drift processes structuring the amphibian skin microbiome

Symbiotic microbial communities are important for host health, but the processes shaping these communities are poorly understood. Understanding how community assembly processes jointly affect microbial community composition is limited because inflexible community models rely on rejecting dispersal and drift before considering selection. We developed a flexible community assembly model based on neutral theory to ask: How do dispersal, drift and selection concurrently affect the microbiome across environmental gradients? We applied this approach to examine how a fungal pathogen affected the assembly processes structuring the amphibian skin microbiome. We found that the rejection of neutrality for the amphibian microbiome across a fungal gradient was not strictly due to selection processes, but was also a result of species‐specific changes in dispersal and drift. Our modelling framework brings the qualitative recognition that niche and neutral processes jointly structure microbiomes into quantitative focus, allowing for improved predictions of microbial community turnover across environmental gradients.     

High salinity gradients and intermediate spatial scales shaped similar biogeographical and co-occurrence patterns of microeukaryotes in a tropical freshwater-saltwater ecosystem

Microeukaryotes play key ecological roles in the microbial web of aquatic ecosystems. However, large knowledge gaps urgently need to be filled regarding the biogeography with associated shaping mechanisms and co-occurrence patterns of microeukaryotes under freshwater-saltwater gradients, especially true in tropical regions. Here, we investigated microeukaryotes of six mixed freshwater-saltwater regions in the Pearl River Estuary and surrounding coasts in southern China, with salinity ranging 0.1–32.0% and distances spanned up to 500 km, using molecular ecological methods. Results indicate that the biogeography of abundant and rare microeukaryotic communities was similar, both their co-occurrence patterns and biogeographical patterns were driven by deterministic and stochastic processes. The environmental factors with higher selective pressure than dispersal limitation meant that the role of deterministic process in structuring communities was more significant than that of stochastic process, and salinity played important role in structuring both microeukaryotic communities and networks. The abundant communities had stronger influence on entire microeukaryotic communities and seemed to be more sensitive to environmental changes than their rare counterparts, while rare ones had stronger interspecific relationships. Finally, the geographic scale and environmental gradients of study regions should firstly be clarified in future research on the ecological processes of microeukaryotes before conclusions are drawn.     

Abundant and rare picoeukaryotic sub‐communities present contrasting patterns in the epipelagic waters of marginal seas in the northwestern Pacific Ocean

In this work, they compared patterns of abundant and rare picoeukaryotic sub‐communities in the epipelagic waters (surface and 40–75 m depth subsurface layers) of the East and South China Seas across seasons via 454 pyrosequencing of the V4 region of 18S rDNA. They also examined the relative effects of environmental filtering, dispersal limitations and seasonality on community assembly. Their results indicated that (i) in the surface layer, abundant taxa are primarily influenced by dispersal limitations and rare taxa are primarily influenced by environmental filtering, whereas (ii) in the subsurface layer, both abundant and rare sub‐communities are only weakly influenced by environmental filtering but are strongly influenced by dispersal limitations. Moreover, (iii) abundant taxa exhibit stronger temporal variability than rare taxa. They also found that abundant and rare sub‐communities display similar spatial richness patterns that are negatively correlated with latitude and chlorophyll a and positively correlated with temperature. In summary, environmental filtering and dispersal limitations have different effects on abundant and rare picoeukaryotic sub‐communities in different layers. Thus, depth appears as an essential variable that governs the structuring patterns of picoeukaryotic communities in the oceans and should be thoroughly considered to develop a more comprehensive understanding of oceanic microbial assemblages.     

Phylogenetic plant community structure along elevation is lineage specific

The trend of closely related taxa to retain similar environmental preferences mediated by inherited traits suggests that several patterns observed at the community scale originate from longer evolutionary processes. While the effects of phylogenetic relatedness have been previously studied within a single genus or family, lineage‐specific effects on the ecological processes governing community assembly have rarely been studied for entire communities or flora. Here, we measured how community phylogenetic structure varies across a wide elevation gradient for plant lineages represented by 35 families, using a co‐occurrence index and net relatedness index (NRI). We propose a framework that analyses each lineage separately and reveals the trend of ecological assembly at tree nodes. We found prevailing phylogenetic clustering for more ancient nodes and overdispersion in more recent tree nodes. Closely related species may thus rapidly evolve new environmental tolerances to radiate into distinct communities, while older lineages likely retain inherent environmental tolerances to occupy communities in similar environments, either through efficient dispersal mechanisms or the exclusion of older lineages with more divergent environmental tolerances. Our study illustrates the importance of disentangling the patterns of community assembly among lineages to better interpret the ecological role of traits. It also sheds light on studies reporting absence of phylogenetic signal, and opens new perspectives on the analysis of niche and trait conservatism across lineages.     

Fungal community responses to precipitation

Understanding how fungal communities are affected by precipitation is an essential aspect of predicting soil functional responses to future climate change and the consequences of those responses for the soil carbon cycle. We tracked fungal abundance, fungal community composition, and soil carbon across 4 years in long‐term field manipulations of rainfall in northern California. Fungi responded directly to rainfall levels, with more abundant, diverse, and consistent communities predominating under drought conditions, and less abundant, less diverse, and more variable communities emerging during wetter periods and in rain‐addition treatments. Soil carbon storage itself did not vary with rainfall amendments, but increased decomposition rates foreshadow longer‐term losses of soil carbon under conditions of extended seasonal rainfall. The repeated recovery of fungal diversity and abundance during periodic drought events suggests that species with a wide range of environmental tolerances coexist in this community, consistent with a storage effect in soil fungi. Increased diversity during dry periods further suggests that drought stress moderates competition among fungal taxa. Based on the responses observed here, we suggest that there may be a relationship between the timescale at which soil microbial communities experience natural environmental fluctuations and their ability to respond to future environmental change.     

Distance decay relationships in foliar fungal endophytes are driven by rare taxa

Foliar fungal endophytes represent a diverse and species‐rich plant microbiome. Their biogeography provides essential clues to their cryptic relationship with hosts and the environment in which they disperse. We present species composition, diversity, and dispersal patterns of endophytic fungi associated with needles of Pinus taeda trees across regional scales in the absence of strong environmental gradients as well as within individual trees. An empirical designation of rare and abundant taxa enlightens us on the structure of endophyte communities. We report multiple distance‐decay patterns consistent with effects of dispersal limitation, largely driven by community changes in rare taxa, those taxonomic units that made up less than 0.31% of reads per sample on average. Distance‐decay rates and community structure also depended on specific classes of fungi and were predominantly influenced by rare members of Dothideomycetes. Communities separated by urban areas also revealed stronger effects of distance on community similarity, confirming that host density and diversity plays an important role in symbiont biogeography, which may ultimately lead to a mosaic of functional diversity as well as rare species diversity across landscapes.     

Experimental insights into the importance of ecologically dissimilar bacteria to community assembly along a salinity gradient

The response of local communities to marine–freshwater transitions and the processes that underlie community assembly are unclear, particularly with respect to bacteria that differ in their life strategies. Here, we implemented a transplant experiment where bacterioplankton from three regions of the Baltic Sea with differing salinities (～3, 7 and 28 psu) were exposed to each other's environmental conditions. We found that habitat specialists were more abundant than generalists after exposure to salinity changes, irrespective of their origins. Most specialists that were selected following a salinity change were rare in the starting communities. Selection for generalists, however, was not specifically driven by the recruitment of either rare or abundant members, suggesting that taxon's initial abundance is minor relevant to the growth of generalists. Patterns in phylogenetic relatedness indicated that environmental filtering was the most influential assembly mechanism for specialists, whereas competitive interaction was more important for the assembly of generalists. Altogether, this study shows that large salinity changes promote the establishment of habitat specialists and that deterministic processes vary during community assembly for ecologically dissimilar taxa. We, therefore, propose that distinguishing assembly mechanisms of different community members helps understand and predict community dynamics in response to environmental change.     

Niche modelling predicts that soil fungi occupy a precarious climate in boreal forests

Aim

Efforts to predict the responses of soil fungal communities to climate change are hindered by limited information on how fungal niches are distributed across environmental hyperspace. We predict the climate sensitivity of North American soil fungal assemblage composition by modelling the ecological niches of several thousand fungal species.

Location

One hundred and thirteen sites in the United States and Canada spanning all biomes except tropical rain forest.

Major Taxa Studied

Fungi.

Time Period

2011–2018.

Methods

We combine internal transcribed spacer (ITS) sequences from two continental-scale sampling networks in North America and cluster them into operational taxonomic units (OTUs) at 97% similarity. Using climate and soil data, we fit ecological niche models (ENMs) based on logistic ridge regression for all OTUs present in at least 10 sites (n = 8597). To describe the compositional turnover of soil fungal assemblages over climatic gradients, we introduce a novel niche-based metric of climate sensitivity, the Sørensen climate sensitivity index. Finally, we map climate sensitivity across North America.

Results

ENMs have a mean out-of-sample predictive accuracy of 73.8%, with temperature variables being strong predictors of fungal distributions. Soil fungal climate niches clump together across environmental space, which suggests common physiological limits and predicts abrupt changes in composition with respect to changes in climate. Soil fungi in North American climates are more likely to be limited by cold and dry conditions than by warm and wet conditions, and ectomycorrhizal fungi generally tolerate colder temperatures than saprotrophic fungi. Sørensen climate sensitivity exhibits a multimodal distribution across environmental space, with a peak in climates corresponding to boreal forests.

Main Conclusions

The boreal forest occupies an especially precarious region of environmental space for the composition of soil fungal assemblages in North America, as even small degrees of warming could trigger large compositional changes characterized mainly by an influx of warm-adapted species.     

Delving into the dark ecology: A continent-wide assessment of patterns of composition in soil fungal communities from Australian tussock grasslands

Soil fungi play essential roles in many terrestrial processes, but our knowledge of the forces governing fungal distribution and community composition along broad-scale environmental gradients is still limited. In this study, we explored biogeographic distribution and composition of soil fungal communities associated with 62 tussock grasslands across different regions of Australia. Climatic parameters had only a limited correlation with fungal community structure, while edaphic variables and spatial distance were significantly associated with changes in fungal community composition. We also observed high variations in composition among fungal assemblages from different ecological regions, suggesting some regional endemism in these communities. The discrete distribution of fungi in soil was further confirmed by indicator analysis, which identified distinct indicator operational taxonomic units associated with grasslands from different climatic regions. Finally, fungi with flexible trophic interactions had a central role in the network architecture of both arid and temperate communities. Taken together, the results from our study confirm the prominent role of soil physico-chemical status and geographic location in determining fungal biogeographic patterns over large scales in Australia.     

The biogeography of abundant and rare bacterioplankton in the lakes and reservoirs of China

Bacteria play key roles in the ecology of both aquatic and terrestrial ecosystems; however, little is known about their diversity and biogeography, especially in the rare microbial biosphere of inland freshwater ecosystems. Here we investigated aspects of the community ecology and geographical distribution of abundant and rare bacterioplankton using high-throughput sequencing and examined the relative influence of local environmental variables and regional (spatial) factors on their geographical distribution patterns in 42 lakes and reservoirs across China. Our results showed that the geographical patterns of abundant and rare bacterial subcommunities were generally similar, and both of them showed a significant distance–decay relationship. This suggests that the rare bacterial biosphere is not a random assembly, as some authors have assumed, and that its distribution is most likely subject to the same ecological processes that control abundant taxa. However, we identified some differences between the abundant and rare groups as both groups of bacteria showed a significant positive relationship between sites occupancy and abundance, but the abundant bacteria exhibited a weaker distance–decay relationship than the rare bacteria. Our results implied that rare subcommunities were mostly governed by local environmental variables, whereas the abundant subcommunities were mainly affected by regional factors. In addition, both local and regional variables that were significantly related to the spatial variation of abundant bacterial community composition were different to those of rare ones, suggesting that abundant and rare bacteria may have discrepant ecological niches and may play different roles in natural ecosystems.