The root microbiota—a fingerprint in the soil?

Background

The root system of a plant is known to host a wide diversity of microbes that can be essential or detrimental to the plant. Microbial ecologists have long struggled to understand what factors structure the composition of these communities. An overlooked part of the microbial community succession in root systems has been the potential for individual variation among plants shaped by early colonisation events such as microbial exposure of the seed inside the parent plant and during dispersal.

Scope

In this review we outline life events of the plant that can affect the composition of its root microbiota and relate ecological theory of community assembly to the formation of the root microbiota.

Conclusion

All plants are exposed to environmental conditions and events throughout their lifetime that shape their phenotype. The microbial community associated with the plant is ultimately an extension of this phenotype. Therefore, only by following a plant from its origin inside the flower to senescence, can we fully understand how the associated microbial community was assembled and what determined its composition.     

Assembly of seed-associated microbial communities within and across successive plant generations

Background and aims

Seeds are involved in the transmission of microorganisms from one plant generation to another and consequently may act as the initial inoculum source for the plant microbiota. In this work, we assessed the structure and composition of the seed microbiota of radish (Raphanus sativus) across three successive plant generations.

Methods

Structure of seed microbial communities were estimated on individual plants through amplification and sequencing of genes that are markers of taxonomic diversity for bacteria (gyrB) and fungi (ITS1). The relative contribution of dispersal and ecological drift in inter-individual fluctuations were estimated with a neutral community model.

Results

Seed microbial communities of radish display a low heritability across plant generations. Fluctuations in microbial community profiles were related to changes in community membership and composition across plant generations, but also to variation between individual plants. Ecological drift was an important driver of the structure of seed bacterial communities, while dispersal was involved in the assembly of the fungal fraction of the seed microbiota.

Conclusions

These results provide a first glimpse of the governing processes driving the assembly of the seed microbiota.

     

Contrasting Microbial Community Assembly Hypotheses: A Reconciling Tale from the Río Tinto

Background

The Río Tinto (RT) is distinguished from other acid mine drainage systems by its natural and ancient origins. Microbial life from all three domains flourishes in this ecosystem, but bacteria dominate metabolic processes that perpetuate environmental extremes. While the patchy geochemistry of the RT likely influences the dynamics of bacterial populations, demonstrating which environmental variables shape microbial diversity and unveiling the mechanisms underlying observed patterns, remain major challenges in microbial ecology whose answers rely upon detailed assessments of community structures coupled with fine-scale measurements of physico-chemical parameters.

Methodology/Principal Findings

By using high-throughput environmental tag sequencing we achieved saturation of richness estimators for the first time in the RT. We found that environmental factors dictate the distribution of the most abundant taxa in this system, but stochastic niche differentiation processes, such as mutation and dispersal, also contribute to observed diversity patterns.

Conclusions/Significance

We predict that studies providing clues to the evolutionary and ecological processes underlying microbial distributions will reconcile the ongoing debate between the Baas Becking vs. Hubbell community assembly hypotheses.     

Ecological rules for the assembly of microbiome communities

Humans and many other hosts establish a diverse community of beneficial microbes anew each generation. The order and identity of incoming symbionts is critical for health, but what determines the success of the assembly process remains poorly understood. Here we develop ecological theory to identify factors important for microbial community assembly. Our method maps out all feasible pathways for the assembly of a given microbiome—with analogies to the mutational maps underlying fitness landscapes in evolutionary biology. Building these “assembly maps” reveals a tradeoff at the heart of the assembly process. Ecological dependencies between members of the microbiota make assembly predictable—and can provide metabolic benefits to the host—but these dependencies may also create barriers to assembly. This effect occurs because interdependent species can fail to establish when each relies on the other to colonize first. We support our predictions with published data from the assembly of the preterm infant microbiota, where we find that ecological dependence is associated with a predictable order of arrival. Our models also suggest that hosts can overcome barriers to assembly via mechanisms that either promote the uptake of multiple symbiont species in one step or feed early colonizers. This predicted importance of host feeding is supported by published data on the impacts of breast milk in the assembly of the human microbiome. We conclude that both microbe to microbe and host to microbe interactions are important for the trajectory of microbiome assembly.

Humans and many other hosts establish a diverse community of beneficial microbes anew each generation, but what determines the success of the assembly process remains poorly understood. This study develops ecological theory that reveals the rules underlying the assembly of such host-associated microbiota.     

Biogeography at the limits of life: Do extremophilic microbial communities show biogeographical regionalization?

Aim

Biogeographical regions are the fundamental geographical units for grouping Earth's biodiversity. Biogeographical regionalization has been demonstrated for many higher taxa, such as terrestrial plants and vertebrates, but not in microbial communities. Therefore, we sought to test empirically whether microbial communities, or taxa, show patterns consistent with biogeographical regionalization.

Location

Within halite (NaCl) crystals from coastal solar salterns of western Europe, the Mediterranean and east Africa.

Time period

Modern (2006–2013).

Major taxa studied

Archaea.

Methods

Using high‐throughput Illumina amplicon sequencing, we generated the most high‐resolution characterization of halite‐associated archaeal communities to date, using samples from 17 locations. We grouped communities into biogeographical clusters based on community turnover to test whether these communities show biogeographical regionalization. To examine whether individual taxa, rather than communities, show biogeographical patterns, we also tested whether the relative abundance of individual genera may be indicative of a community's biogeographical origins using machine learning methods, specifically random forest classification.

Results

We found that the rate of community turnover was greatest over subregional spatial scales (< 500 km), whereas at regional spatial scales the turnover was independent of geographical distance. Biogeographical clusters of communities were either not statistically robust or lacked spatial coherence, inconsistent with biogeographical regionalization. However, we identified several archaeal genera that were good indicators of biogeographical origin, providing classification error rates of < 10%.

Main conclusions

Overall, our results provide little support for the concept of biogeographical regions in these extremophilic microbial communities, despite the fact that some taxa do show biogeographical patterns. We suggest that variable dispersal ability among the halite‐associated Archaea may disrupt biogeographical patterns at the community level, preventing the formation of biogeographical regions. This means that the processes that lead to the formation of biogeographical regions operate differentially on individual microbial taxa rather than on entire communities.     

Environmental filtering governs consistent vertical zonation in sedimentary microbial communities across disconnected mountain lakes

Subsurface microorganisms make up the majority of Earth's microbial biomass, but ecological processes governing surface communities may not explain community patterns at depth because of burial. Depth constrains dispersal and energy availability, and when combined with geographic isolation across landscapes, may influence community assembly. We sequenced the 16S rRNA gene of bacteria and archaea from 48 sediment cores across 36 lakes in four disconnected mountain ranges in Wyoming, USA and used null models to infer assembly processes across depth, spatial isolation, and varying environments. Although we expected strong dispersal limitations across these isolated settings, community composition was primarily shaped by environmental selection. Communities consistently shifted from domination by organisms that degrade organic matter at the surface to methanogenic, low-energy adapted taxa in deeper zones. Stochastic processes—like dispersal limitation—contributed to differences among lakes, but because these effects weakened with depth, selection processes ultimately governed subsurface microbial biogeography.     

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.     

Unraveling negative biotic interactions determining soil microbial community assembly and functioning

Microbial communities play important roles in all ecosystems and yet a comprehensive understanding of the ecological processes governing the assembly of these communities is missing. To address the role of biotic interactions between microorganisms in assembly and for functioning of the soil microbiota, we used a top-down manipulation approach based on the removal of various populations in a natural soil microbial community. We hypothesized that removal of certain microbial groups will strongly affect the relative fitness of many others, therefore unraveling the contribution of biotic interactions in shaping the soil microbiome. Here we show that 39% of the dominant bacterial taxa across treatments were subjected to competitive interactions during soil recolonization, highlighting the importance of biotic interactions in the assembly of microbial communities in soil. Moreover, our approach allowed the identification of microbial community assembly rule as exemplified by the competitive exclusion between members of Bacillales and Proteobacteriales. Modified biotic interactions resulted in greater changes in activities related to N- than to C-cycling. Our approach can provide a new and promising avenue to study microbial interactions in complex ecosystems as well as the links between microbial community composition and ecosystem function.Subject terms: Soil microbiology, Ecology     

Co-occurring grass species differ in their associated microbial community composition in a temperate native grassland

Background and aims

Specific associations exist between plant species and the soil microbial community and these associations vary between habitat types and different plant groups. However, there is evidence that the associations are highly specific. Hence, we aimed to determine the specificity of plant-microbe relationships amongst co-occurring grass species in a temperate grassland.

Methods and results

We examined the broad microbial groups of bacteria and fungi as well as a specific fungal group, the arbuscular mycorrhizal community amongst two dominant C₃ and C₄ species and one sub-dominant C₃ species using terminal restriction fragment length polymorphism (T-RFLP) analysis. We found that the two dominant species were more similar to each other in their bacterial and arbuscular mycorrhizal community composition than either was to the sub-dominant species, but not in their fungal community composition. We also found no clear evidence that those differences were directly linked to soil chemical properties.

Conclusions

Our results demonstrate that co-occurring grass species have a distinct soil microbial community and T-RFLP analysis is able to detect plant species effect on the microbial community composition on an extremely local scale, providing an insight into the differences in the response of bacterial, fungal and arbuscular mycorrhizal communities to different, but similar and co-occurring, plant species.     

Macrosystem community change in lake phytoplankton and its implications for diversity and function

Aim

We use lake phytoplankton community data to quantify the spatio-temporal and scale-dependent impacts of eutrophication, land-use and climate change on species niches and community assembly processes while accounting for species traits and phylogenetic constraints.

Location

Finland.

Time period

1977–2017.

Major taxa

Phytoplankton.

Methods

We use hierarchical modelling of species communities (HMSC) to model metacommunity trajectories at 853 lakes over four decades of environmental change, including a hierarchical spatial structure to account for scale-dependent processes. Using a “region of common profile” approach, we evaluate compositional changes of species communities and trait profiles and investigate their temporal development.

Results

We demonstrate the emergence of novel and widespread community composition clusters in previously more compositionally homogeneous communities, with cluster-specific community trait profiles, indicating functional differences. A strong phylogenetic signal of species responses to the environment implies similar responses among closely related taxa. Community cluster-specific species prevalence indicates lower taxonomic dispersion within the current dominant clusters compared with the historically dominant cluster and an overall higher prevalence of smaller species sizes within communities. Our findings denote profound spatio-temporal structuring of species co-occurrence patterns and highlight functional differences of lake phytoplankton communities.

Main conclusions

Diverging community trajectories have led to a nationwide reshuffling of lake phytoplankton communities. At regional and national scales, lakes are not single entities but metacommunity hubs in an interconnected waterscape. The assembly mechanisms of phytoplankton communities are strongly structured by spatio-temporal dynamics, which have led to novel community types, but only a minor part of this reshuffling could be linked to temporal environmental change.     

Among-Population Variation in Microbial Community Structure in the Floral Nectar of the Bee-Pollinated Forest Herb Pulmonaria officinalis L

Background

Microbial communities in floral nectar have been shown to be characterized by low levels of species diversity, yet little is known about among-plant population variation in microbial community composition.

Methodology/Principal Findings

We investigated the microbial community structure (yeasts and bacteria) in floral nectar of ten fragmented populations of the bee-pollinated forest herb Pulmonaria officinalis. We also explored possible relationships between plant population size and microbial diversity in nectar, and related microbial community composition to the distance separating plant populations. Culturable bacteria and yeasts occurring in the floral nectar of a total of 100 plant individuals were isolated and identified by partially sequencing the 16S rRNA gene and D1/D2 domains of the 26S rRNA gene, respectively. A total of 9 and 11 yeast and 28 and 39 bacterial OTUs was found, taking into account a 3% (OTU_0.03) and 1% sequence dissimilarity cut-off (OTU_0.01). OTU richness at the plant population level (i.e. the number of OTUs per population) was low for yeasts (mean: 1.7, range: 0–4 OTUs_0.01/0.03 per population), whereas on average 6.9 (range: 2–13) OTUs_0.03 and 7.9 (range 2–16) OTUs_0.01 per population were found for bacteria. Both for yeasts and bacteria, OTU richness was not significantly related to plant population size. Similarity in community composition among populations was low (average Jaccard index: 0.14), and did not decline with increasing distance between populations.

Conclusions/Significance

We found low similarity in microbial community structure among populations, suggesting that the assembly of nectar microbiota is to a large extent context-dependent. Although the precise factors that affect variation in microbial community structure in floral nectar require further study, our results indicate that both local and regional processes may contribute to among-population variation in microbial community structure in nectar.     

Ecological drift and local exposures drive enteric bacterial community differences within species of Galápagos iguanas

Diet strongly influences the intestinal microbial communities through species sorting. Alternatively, these communicates may differ because of chance variation in local microbial exposures or species losses among allopatric host populations (i.e. ecological drift). We investigated how these forces shape enteric communities of Galápagos marine and land iguanas. Geographically proximate populations shared more similar communities within a host ecotype, suggesting a role for ecological drift during host colonization of the islands. Additionally, evidence of taxa sharing between proximate heterospecific host populations suggests that contemporary local exposures also influence the gut community assembly. While selective forces such as host-bacterial interactions or dietary differences are dominant drivers of intestinal community differences among hosts, historical and contemporary processes of ecological drift may lead to differences in bacterial composition within a host species. Whether such differences in community structure translate into geographic variation in benefits derived from these intimate microbial communities remains to be explored.     

Mechanisms of soil bacterial and fungal community assembly differ among and within islands

The study of islands has made substantial contributions to the development of evolutionary and ecological theory. However, we know little about microbial community assembly on islands. Using soil microbial data collected from 29 lake islands and nearby mainland, we examined the assembly mechanisms of soil bacterial and fungal communities among and within islands. We found that deterministic processes, especially homogeneous selection, tended to be more important in shaping the assembly of soil bacterial communities among islands, while stochastic processes tended to be more important within islands. Moreover, increasing island area increased the importance of homogeneous selection, but reduced the importance of variable selection, for soil bacterial community assembly within islands. By contrast, stochastic processes tended to dominate soil fungal community assembly both among and within islands, with dispersal limitation playing a more important role within than among islands. Our results highlight the scale- and taxon-dependence of insular soil microbial community assembly, suggesting that spatial scale should be explicitly considered when evaluating the influences of habitat fragmentation on soil microbial communities.     

Effects of condensed tannins in conifer leaves on the composition and activity of the soil microbial community in a tropical montane forest

Background and aims

Condensed tannins, a dominant class of plant secondary metabolites, play potentially important roles in plant-soil feedbacks by influencing the soil microbial community. Effects of condensed tannins on the soil microbial community and activity were examined by a short-term tannin-addition experiment under field and laboratory conditions.

Methods

Condensed tannins were extracted from the leaves of a dominant conifer (Dacrydium gracilis) in a tropical montane forest on Mt. Kinabalu, Borneo. The extracted tannins were added to soils beneath the conifer and a dominant broadleaf (Lithocarpus clementianus) to evaluate the dependence of the response to tannin addition on the initial composition of the soil microbial community.

Results

Enzyme activities in the field tannin-addition treatment were lower than in the deionized-water treatment. Carbon and nitrogen mineralization were also inhibited by tannin-addition. The fungi-to-bacteria ratio after tannin-addition was higher compared with the distilled-water treatment in the laboratory experiment.

Conclusions

Based on our results, we suggest that the higher concentration of condensed tannins in the leaf tissues of Dacrydium than in those of Lithocarpus is a factor influencing the microbial community and activity. This may have influences on subsequent plant performance, which induces plant-soil feedback processes that can control dynamics of the tropical montane forest ecosystem.     

Plant selenium hyperaccumulation- Ecological effects and potential implications for selenium cycling and community structure

Background

Selenium (Se) hyperaccumulation occurs in ~50 plant taxa native to seleniferous soils in Western USA. Hyperaccumulator tissue Se levels, 1000–15,000?mg/kg dry weight, are typically 100 times higher than surrounding vegetation. Relative to other species, hyperaccumulators also transform Se more into organic forms.

Response of soil microbial activity to grazing, nitrogen deposition, and exotic cover in a serpentine grassland

Background and aims

Exotic species, nitrogen (N) deposition, and grazing are major drivers of change in grasslands. However little is known about the interactive effects of these factors on below-ground microbial communities.

Methods

We simulated realistic N deposition increases with low-level fertilization and manipulated grazing with fencing in a split-plot experiment in California’s largest serpentine grassland. We also monitored grazing intensity using camera traps and measured total available N to assess grazing and nutrient enrichment effects on microbial extracellular enzyme activity (EEA), microbial N mineralization, and respiration rates in soil.

Results

Continuous measures of grazing intensity and N availability showed that increased grazing and N were correlated with increased microbial activity and were stronger predictors than the categorical grazing and fertilization measures. Exotic cover was also generally correlated with increased microbial activity resulting from exotic-driven nutrient cycling alterations. Seasonal effects, on abiotic factors and plant phenology, were also an important factor in EEA with lower activity occurring at peak plant biomass.

Conclusions

In combination with previous studies from this serpentine grassland, our results suggest that grazing intensity and soil N availability may affect the soil microbial community indirectly via effects on exotic cover and associated changes in nutrient cycling while grazing directly impacts soil community function.     

UniFrac – An online tool for comparing microbial community diversity in a phylogenetic context

Background  

Moving beyond pairwise significance tests to compare many microbial communities simultaneously is critical for understanding large-scale trends in microbial ecology and community assembly. Techniques that allow microbial communities to be compared in a phylogenetic context are rapidly gaining acceptance, but the widespread application of these techniques has been hindered by the difficulty of performing the analyses.     

Impact of the plant community composition on labile soil organic carbon, soil microbial activity and community structure in semi-natural grassland ecosystems of different productivity

Aims

The main objective was to describe the effects of plant litter on SOC and on soil microbial activity and structure in extensively managed grasslands in Central Germany that vary in biomass production and plant community composition.

Methods

The decomposition of shoot and root litter was studied in an incubation experiment. Labile C and N were isolated by hot water extraction (C_HWE, N_HWE), while functional groups of microbes were identified by PLFA analysis and microbial activity was measured using a set of soil exo-enzymes.

Results

The plant community composition, particulary legume species affected SOC dynamics and below-ground microbial processes, especially via roots. This was reflected in about 20% lower decomposition of root litter in low productivity grassland soil. The C_HWE soil pool was found to be a key driver of the below-ground food web, controlling soil microbial processes.

Conclusions

Below-ground responses appear to be related to the presence of legume species, which affected the microbial communities, as well as the ratio between fungal and bacterial biomass and patterns of soil enzyme activity. Low productivity fungal-dominated grasslands with slow C turnover rates may play an important role in SOC accumulation. The approach used here is of particular importance, since associated biological and biochemical processes are fundamental to ecosystem functioning.     

Do bacterial and fungal communities assemble differently during primary succession?

High‐throughput sequencing technologies are now allowing us to study patterns of community assembly for diverse microbial assemblages across environmental gradients and during succession. Here we discuss potential explanations for similarities and differences in bacterial and fungal community assembly patterns along a soil chronosequence in the foreland of a receding glacier. Although the data are not entirely conclusive, they do indicate that successional trajectories for bacteria and fungi may be quite different. Recent empirical and theoretical studies indicate that smaller microbes (like most bacteria) are less likely to be dispersal limited than are larger microbes – which could result in a more deterministic community assembly pattern for bacteria during primary succession. Many bacteria are also better adapted (than are fungi) to life in barren, early‐successional sediments in that some can fix nitrogen and carbon from the atmosphere – traits not possessed by any fungi. Other differences between bacteria and fungi are discussed, but it is apparent from this and other recent studies of microbial succession that we are a long way from understanding the mechanistic underpinnings of microbial community assembly during ecosystem succession. We especially need a better understanding of global and regional patterns of microbial dispersal and what environmental factors control the development of microbial communities in complex natural systems.