Temporal variability in nutrient use among Streptomyces suggests dynamic niche partitioning.

Soil bacteria spend significant periods in dormant or semi-dormant states that are interrupted by resource pulses which can lead to periods of rapid growth and intense nutrient competition. Microbial populations have evolved diverse strategies to circumvent competitive interactions and facilitate coexistence. Here, we show that nutrient use of soilborne Streptomyces is temporally partitioned during experimental resource pulses, leading to reduced niche overlap, and potential coexistence. Streptomyces grew rapidly on the majority of distinct 95 carbon sources but varied in which individual resources were utilized in the first 24 h. Only a handful of carbon sources (19 out of 95) were consistently utilized (>95% of isolates) most rapidly in the first 24 h. These consistently utilized carbon sources also generated the majority of biomass accumulated by isolates. Our results shed new light on a novel mechanism microbes may employ to alleviate competitive interactions by temporally partitioning the consumption of carbon resources. As competitive interactions have been proposed to drive the suppression of disease-causing microbes in agronomic soils, our findings may hold widespread implications for soil management for plant health.

Seasonal shifts from plant diversity to consumer control of grassland productivity.

Plant biodiversity and consumers are important mediators of energy and carbon fluxes in grasslands, but their effects on within-season variation of plant biomass production are poorly understood. Here we measure variation in control of plant biomass by consumers and plant diversity throughout the growing season and their impact on plant biomass phenology. To do this, we analysed 5 years of biweekly biomass measures (NDVI) in an experiment manipulating plant species richness and three consumer groups (foliar fungi, soil fungi and arthropods). Positive plant diversity effects on biomass were greatest early in the growing season, whereas the foliar fungicide and insecticide treatments increased biomass most late in the season. Additionally, diverse plots and plots containing foliar fungi reached maximum biomass almost a month earlier than monocultures and plots treated with foliar fungicide, demonstrating the dynamic and interactive roles that biodiversity and consumers play in regulating biomass production through the growing season.

Harnessing intercellular signals to engineer the soil microbiome.

Covering: Focus on 2015 to 2020Plant and soil microbiomes consist of diverse communities of organisms from across kingdoms and can profoundly affect plant growth and health. Natural product-based intercellular signals govern important interactions between microbiome members that ultimately regulate their beneficial or harmful impacts on the plant. Exploiting these evolved signalling circuits to engineer microbiomes towards beneficial interactions with crops is an attractive goal. There are few reports thus far of engineering the intercellular signalling of microbiomes, but this article argues that it represents a tremendous opportunity for advancing the field of microbiome engineering. This could be achieved through the selection of synergistic consortia in combination with genetic engineering of signal pathways to realise an optimised microbiome.

Foliar fungi and plant diversity drive ecosystem carbon fluxes in experimental prairies.

Plant diversity and plant-consumer/pathogen interactions likely interact to influence ecosystem carbon fluxes but experimental evidence is scarce. We examined how experimental removal of foliar fungi, soil fungi and arthropods from experimental prairies planted with 1, 4 or 16 plant species affected instantaneous rates of carbon uptake (GPP), ecosystem respiration (Re ) and net ecosystem exchange (NEE). Increasing plant diversity increased plant biomass, GPP and Re , but NEE remained unchanged. Removing foliar fungi increased GPP and NEE, with the greatest effects at low plant diversity. After accounting for plant biomass, we found that removing foliar fungi increased mass-specific flux rates in the low-diversity plant communities by altering plant species composition and community-wide foliar nitrogen content. However, this effect disappeared when soil fungi and arthropods were also removed, demonstrating that both plant diversity and interactions among consumer groups determine the ecosystem-scale effects of plant-fungal interactions.

Towards a unified data infrastructure to support European and global microbiome research: a call to action.

High-quality microbiome research relies on the integrity, management and quality of supporting data. Currently biobanks and culture collections have different formats and approaches to data management. This necessitates a standard data format to underpin research, particularly in line with the FAIR data standards of findability, accessibility, interoperability and reusability. We address the importance of a unified, coordinated approach that ensures compatibility of data between that needed by biobanks and culture collections, but also to ensure linkage between bioinformatic databases and the wider research community.

Inhibitory and nutrient use phenotypes among coexisting Fusarium and Streptomyces populations suggest local coevolutionary interactions in soil.

Bacteria and fungi are key components of virtually all natural habitats, yet the significance of fungal-bacterial inhibitory interactions for the ecological and evolutionary dynamics of specific bacterial and fungal populations in natural habitats have been overlooked. More specifically, despite the broad consensus that antibiotics play a key role in providing a fitness advantage to competing microbes, the significance of antibiotic production in mediating cross-kingdom coevolutionary interactions has received relatively little attention. Here, we characterize reciprocal inhibition among Streptomyces and Fusarium populations from prairie soil, and explore antibiotic inhibition in relation to niche overlap among sympatric and allopatric populations. We found evidence for local adaptation between Fusarium and Streptomyces populations as indicated by significantly greater inhibition among sympatric than allopatric populations. Additionally, for both taxa, there was a significant positive correlation between the strength of inhibition against the other taxon and the intensity of resource competition from that taxon among sympatric but not allopatric populations. These data suggest that coevolutionary antagonistic interactions between Fusarium and Streptomyces are driven by resource competition, and support the hypothesis that antibiotics act as weapons in mediating bacterial-fungal interactions in soil.

Complete genome sequences of Streptomyces spp. isolated from disease-suppressive soils.

BACKGROUND: Bacteria within the genus Streptomyces remain a major source of new natural product discovery and as soil inoculants in agriculture where they promote plant growth and protect from disease. Recently, Streptomyces spp. have been implicated as important members of naturally disease-suppressive soils. To shine more light on the ecology and evolution of disease-suppressive microbial communities, we have sequenced the genome of three Streptomyces strains isolated from disease-suppressive soils and compared them to previously sequenced isolates. Strains selected for sequencing had previously showed strong phenotypes in competition or signaling assays. RESULTS: Here we present the de novo sequencing of three strains of the genus Streptomyces isolated from disease-suppressive soils to produce high-quality complete genomes. Streptomyces sp. GS93-23, Streptomyces sp. 3211-3, and Streptomyces sp. S3-4 were found to have linear chromosomes of 8.24 Mb, 8.23 Mb, and greater than 7.5 Mb, respectively. In addition, two of the strains were found to have large, linear plasmids. Each strain harbors between 26 and 38 natural product biosynthetic gene clusters, on par with previously sequenced Streptomyces spp. We compared these newly sequenced genomes with those of previously sequenced organisms. We see substantial natural product biosynthetic diversity between closely related strains, with the gain/loss of episomal DNA elements being a primary driver of genome evolution. CONCLUSIONS: Long read sequencing data facilitates large contig assembly for high-GC Streptomyces genomes. While the sample number is too small for a definitive conclusion, we do not see evidence that disease suppressive soil isolates are particularly privileged in terms of numbers of biosynthetic gene clusters. The strong sequence similarity between GS93-23 and previously isolated Streptomyces lydicus suggests that species recruitment may contribute to the evolution of disease-suppressive microbial communities.

Stability of grassland production is robust to changes in the consumer food web.

Theory predicts that consumers may stabilise or destabilise plant production depending on model assumptions, and tests in aquatic food webs suggest that trophic interactions are stabilising. We quantified the effects of trophic interactions on temporal variability (standard deviation) and temporal stability (mean/standard deviation) of grassland biomass production and the plant diversity-stability relationship by experimentally removing heterotrophs (large vertebrates, arthropods, foliar and soil fungi) from naturally and experimentally assembled grasslands of varying diversity. In both grassland types, trophic interactions proportionately decreased plant community biomass mean and variability over the course of 6 years, leading to no net change in temporal stability or the plant diversity-stability relationship. Heterotrophs also mediated plant coexistence; their removal reduced diversity in naturally assembled grasslands. Thus, herbivores and fungi reduce biomass production, concurrently reducing the temporal variability of energy and material fluxes. Because of this coupling, grassland stability is robust to large food web perturbations.

Impacts of Sampling Design on Estimates of Microbial Community Diversity and Composition in Agricultural Soils.

Soil microbiota play important and diverse roles in agricultural crop nutrition and productivity. Yet, despite increasing efforts to characterize soil bacterial and fungal assemblages, it is challenging to disentangle the influences of sampling design on assessments of communities. Here, we sought to determine whether composite samples-often analyzed as a low cost and effort alternative to replicated individual samples-provide representative summary estimates of microbial communities. At three Minnesota agricultural research sites planted with an oat cover crop, we conducted amplicon sequencing for soil bacterial and fungal communities (16SV4 and ITS2) of replicated individual or homogenized composite soil samples. We compared soil microbiota from within and among plots and then among agricultural sites using both sampling strategies. Results indicated that single or multiple replicated individual samples, or a composite sample from each plot, were sufficient for distinguishing broad site-level macroecological differences among bacterial and fungal communities. Analysis of a single sample per plot captured only a small fraction of the distinct OTUs, diversity, and compositional variability detected in the analysis of multiple individual samples or a single composite sample. Likewise, composite samples captured only a fraction of the diversity represented by the six individual samples from which they were formed, and, on average, analysis of two or three individual samples offered greater compositional coverage (i.e., greater number of OTUs) than a single composite sample. We conclude that sampling design significantly impacts estimates of bacterial and fungal communities even in homogeneously managed agricultural soils, and our findings indicate that while either strategy may be sufficient for broad macroecological investigations, composites may be a poor substitute for replicated samples at finer spatial scales.

No evidence for trade-offs in plant responses to consumer food web manipulations.

Plants face a range of trade-offs as they attempt to maximize their fitness within a complex web composed of competitors, mutualists, and herbivores. In addition to growth-defense and competition-defense trade-offs, plants must balance their response to a wide range of potential enemies including pathogens and vertebrate and invertebrate herbivores. We tested for trade-offs in plant species' responses to different types of consumers using a foodweb manipulation experiment in which we selectively excluded large vertebrate herbivores and removed foliar fungi, soil fungi, and insects from natural and experimentally planted grassland communities. We found no evidence for trade-offs in the ability of plants to defend themselves against different sets of consumers, although plants varied widely in their responses to removal of different consumer groups. In addition, the species-level responses to consumer removal in monoculture were uncorrelated with each species' response in more diverse communities, highlighting the important role of local context (e.g., competition and apparent competition) in determining the effects of consumers. Plants must balance their allocation of energy among a wide variety of tasks including growing, competing for limited resources, and defending themselves against an array of potential enemies. We found that while plant species differed greatly in their response to the removal of consumers, species that were susceptible to the effects of one consumer group (e.g., insect herbivores) also were susceptible to other consumer groups (e.g., fungal pathogens). This suggests that plants differ in their overall allocation to defense, but defense investment can proffer protection against a wide array of natural enemies. We also found that plant responses to consumers depended on the diversity of the surrounding plant community, suggesting that among-plant interactions can alter their susceptibility to the impacts of consumers.

Food webs obscure the strength of plant diversity effects on primary productivity.

Plant diversity experiments generally find that increased diversity causes increased productivity; however, primary productivity is typically measured in the presence of a diverse food web, including pathogens, mutualists and herbivores. If food web impacts on productivity vary with plant diversity, as predicted by both theoretical and empirical studies, estimates of the effect of plant diversity on productivity may be biased. We experimentally removed arthropods, foliar fungi and soil fungi from the longest-running plant diversity experiment. We found that fungi and arthropods removed a constant, large proportion of biomass leading to a greater reduction of total biomass in high diversity plots. As a result, the effect of diversity on measured plant productivity was much higher in the absence of fungi and arthropods. Thus, diversity increases productivity more than reported in previous studies that did not control for the effects of heterotrophic consumption.

Plant Community Richness Mediates Inhibitory Interactions and Resource Competition between Streptomyces and Fusarium Populations in the Rhizosphere.

Plant community characteristics impact rhizosphere Streptomyces nutrient competition and antagonistic capacities. However, the effects of Streptomyces on, and their responses to, coexisting microorganisms as a function of plant host or plant species richness have received little attention. In this work, we characterized antagonistic activities and nutrient use among Streptomyces and Fusarium from the rhizosphere of Andropogon gerardii (Ag) and Lespedeza capitata (Lc) plants growing in communities of 1 (monoculture) or 16 (polyculture) plant species. Streptomyces from monoculture were more antagonistic against Fusarium than those from polyculture. In contrast, Fusarium isolates from polyculture had greater inhibitory capacities against Streptomyces than isolates from monoculture. Although Fusarium isolates had on average greater niche widths, the collection of Streptomyces isolates in total used a greater diversity of nutrients for growth. Plant richness, but not plant host, influenced the potential for resource competition between the two taxa. Fusarium isolates had greater niche overlap with Streptomyces in monoculture than polyculture, suggesting greater potential for Fusarium to competitively challenge Streptomyces in monoculture plant communities. In contrast, Streptomyces had greater niche overlap with Fusarium in polyculture than monoculture, suggesting that Fusarium experiences greater resource competition with Streptomyces in polyculture than monoculture. These patterns of competitive and inhibitory phenotypes among Streptomyces and Fusarium populations are consistent with selection for Fusarium-antagonistic Streptomyces populations in the presence of strong Fusarium resource competition in plant monocultures. Similarly, these results suggest selection for Streptomyces-inhibitory Fusarium populations in the presence of strong Streptomyces resource competition in more diverse plant communities. Thus, landscape-scale variation in plant species richness may be critical to mediating the coevolutionary dynamics and selective trajectories for inhibitory and nutrient use phenotypes among Streptomyces and Fusarium populations in soil, with significant implications for microbial community functional characteristics.

Disease Suppressive Soils: New Insights from the Soil Microbiome.

Soils suppressive to soilborne pathogens have been identified worldwide for almost 60 years and attributed mainly to suppressive or antagonistic microorganisms. Rather than identifying, testing and applying potential biocontrol agents in an inundative fashion, research into suppressive soils has attempted to understand how indigenous microbiomes can reduce disease, even in the presence of the pathogen, susceptible host, and favorable environment. Recent advances in next-generation sequencing of microbiomes have provided new tools to reexamine and further characterize the nature of these soils. Two general types of suppression have been described: specific and general suppression, and theories have been developed around these two models. In this review, we will present three examples of currently-studied model systems with features representative of specific and general suppressiveness: suppression to take-all (Gaeumannomyces graminis var. tritici), Rhizoctonia bare patch of wheat (Rhizoctonia solani AG-8), and Streptomyces. To compare and contrast the two models of general versus specific suppression, we propose a number of hypotheses about the nature and ecology of microbial populations and communities of suppressive soils. We outline the potential and limitations of new molecular techniques that can provide novel ways of testing these hypotheses. Finally, we consider how this greater understanding of the phytobiome can facilitate sustainable disease management in agriculture by harnessing the potential of indigenous soil microbes.

Plant diversity and plant identity influence Fusarium communities in soil.

Fusarium communities play important functional roles in soil and in plants as pathogens, endophytes, and saprotrophs. This study tests how rhizosphere Fusarium communities may vary with plant species, changes in the diversity of the surrounding plant community, and soil physiochemical characteristics. Fusarium communities in soil associated with the roots of two perennial prairie plant species maintained as monocultures or growing within polyculture plant communities were characterized using targeted metagenomics. Amplicon libraries targeting the RPB2 locus were generated from rhizosphere soil DNAs and sequenced using pyrosequencing. Sequences were clustered into operational taxonomic units (OTUs) and assigned a taxonomy using the Evolutionary Placement Algorithm. Fusarium community composition was differentiated between monoculture and polyculture plant communities, and by plant species in monoculture, but not in polyculture. Taxonomic classification of the Fusarium OTUs showed a predominance of F. tricinctum and F. oxysporum as well of the presence of a clade previously only found in the Southern Hemisphere. Total Fusarium richness was not affected by changes in plant community richness or correlated with soil physiochemical characteristics. However, OTU richness within two predominant phylogenetic lineages within the genus was positively or negatively correlated with soil physiochemical characteristics among samples within each lineage. This work shows that plant species, plant community richness, and soil physiochemical characteristics may all influence the composition and richness of Fusarium communities in soil.

Tree species effects on pathogen-suppressive capacities of soil bacteria across two tropical dry forests in Costa Rica.

Antibiotic-producing bacteria in the genus Streptomyces can inhibit soil-borne plant pathogens, and have the potential to mediate the impacts of disease on plant communities. Little is known about how antibiotic production varies among soil communities in tropical forests, despite a long history of interest in the role of soil-borne pathogens in these ecosystems. Our objective was to determine how tree species and soils influence variation in antibiotic-mediated pathogen suppression among Streptomyces communities in two tropical dry forest sites (Santa Rosa and Palo Verde). We targeted tree species that co-occur in both sites and used a culture-based functional assay to quantify pathogen-suppressive capacities of Streptomyces communities beneath 50 focal trees. We also measured host-associated litter and soil element concentrations as potential mechanisms by which trees may influence soil microbes. Pathogen-suppressive capacities of Streptomyces communities varied within and among tree species, and inhibitory phenotypes were significantly related to soil and litter element concentrations. Average proportions of inhibitory Streptomyces in soils from the same tree species varied between 1.6 and 3.3-fold between sites. Densities and proportions of pathogen-suppressive bacteria were always higher in Santa Rosa than Palo Verde. Our results suggest that spatial heterogeneity in the potential for antibiotic-mediated disease suppression is shaped by tree species, site, and soil characteristics, which could have significant implications for understanding plant community composition and diversity in tropical dry forests.

Leveraging ecological theory to guide natural product discovery.

Technological improvements have accelerated natural product (NP) discovery and engineering to the point that systematic genome mining for new molecules is on the horizon. NP biosynthetic potential is not equally distributed across organisms, environments, or microbial life histories, but instead is enriched in a number of prolific clades. Also, NPs are not equally abundant in nature; some are quite common and others markedly rare. Armed with this knowledge, random 'fishing expeditions' for new NPs are increasingly harder to justify. Understanding the ecological and evolutionary pressures that drive the non-uniform distribution of NP biosynthesis provides a rational framework for the targeted isolation of strains enriched in new NP potential. Additionally, ecological theory leads to testable hypotheses regarding the roles of NPs in shaping ecosystems. Here we review several recent strain prioritization practices and discuss the ecological and evolutionary underpinnings for each. Finally, we offer perspectives on leveraging microbial ecology and evolutionary biology for future NP discovery.

Do tradeoffs structure antibiotic inhibition, resistance, and resource use among soil-borne Streptomyces?

BACKGROUND: Tradeoffs among competing traits are believed to be crucial to the maintenance of diversity in complex communities. The production of antibiotics to inhibit competitors and resistance to antibiotic inhibition are two traits hypothesized to be critical to microbial fitness in natural habitats, yet data on costs or tradeoffs associated with these traits are limited. In this work we characterized tradeoffs between antibiotic inhibition or resistance capacities and growth efficiencies or niche widths for a broad collection of Streptomyces from soil. RESULTS: Streptomyces isolates tended to have either very little or very high inhibitory capacity. In contrast, Streptomyces isolates were most commonly resistant to antibiotic inhibition by an intermediate number of other isolates. Streptomyces with either very high antibiotic inhibitory or resistance capacities had less efficient growth and utilized a smaller number of resources for growth (smaller niche width) than those with low inhibition or resistance capacities, suggesting tradeoffs between antibiotic inhibitory or resistance and resource use phenotypes. CONCLUSIONS: This work suggests that life-history tradeoffs may be crucial to the maintenance of the vast diversity of antibiotic inhibitory and resistance phenotypes found among Streptomyces in natural communities.

Plant community richness and microbial interactions structure bacterial communities in soil.

Plant species, plant community diversity and microbial interactions can significantly impact soil microbial communities, yet there are few data on the interactive effects of plant species and plant community diversity on soil bacterial communities. We hypothesized that plant species and plant community diversity affect soil bacterial communities by setting the context in which bacterial interactions occur. Specifically, we examined soil bacterial community composition and diversity in relation to plant "host" species, plant community richness, bacterial antagonists, and soil edaphic characteristics. Soil bacterial communities associated with four different prairie plant species (Andropogon gerardii, Schizachyrium scoparium, Lespedeza capitata, and' Lupinus perennis) grown in plant communities of increasing species richness (1, 4, 8, and 16 species) were sequenced. Additionally, soils were evaluated for populations of antagonistic bacteria and edaphic characteristics. Plant species effects on soil bacterial community composition were small and depended on plant community richness. In contrast, increasing plant community richness significantly altered soil bacterial community composition and was negatively correlated with bacterial diversity. Concentrations of soil carbon, organic matter, nitrogen, phosphorus, and potassium were similarly negatively correlated with bacterial diversity, whereas the proportion of antagonistic bacteria was positively correlated with soil bacterial diversity. Results suggest that plant species influences on soil bacterial communities depend on plant community diversity and are mediated through the effects of plant-derived resources on antagonistic soil microbes.

Soil fungal communities respond to grassland plant community richness and soil edaphics.

Fungal communities in soil have significant influences on terrestrial ecosystem dynamics, yet our understanding of the drivers of fungal diversity and community structure in soil is limited. Fungal communities associated with the rhizosphere of four native perennial grassland plant species, two legumes and two grasses, grown in monoculture and polyculture in a long-term field experiment were characterized. Reference databases were developed for, and amplicon libraries sequenced from, multiple-copy rRNA and single-copy protein-coding loci. Clustering and alignment-based pipelines were utilized to evaluate differences in fungal community structure and diversity in response to plant host, plant community richness, and soil edaphics. Fungal diversity increased in the rhizosphere of plants growing in polyculture plant communities as compared to monoculture plant communities. Fungal community structure was differentiated between legumes and grasses growing in monoculture but not in polyculture. To specifically monitor fungi in the genus Fusarium in the soil, the protein-coding locus was used to increase phylogenetic resolution and enrich for this taxon. These data show that fungal community richness and structure are strongly linked with plant community dynamics and associated soil edaphic characteristics in these grassland soils.

Diffuse symbioses: roles of plant-plant, plant-microbe and microbe-microbe interactions in structuring the soil microbiome.

A conceptual model emphasizing direct host-microbe interactions has dominated work on host-associated microbiomes. To understand plant-microbiome associations, however, broader influences on microbiome composition and functioning must be incorporated, such as those arising from plant-plant and microbe-microbe interactions. We sampled soil microbiomes associated with target plant species (Andropogon gerardii, Schizachyrium scoparium, Lespedeza capitata, Lupinus perennis) grown in communities varying in plant richness (1-, 4-, 8- or 16-species). We assessed Streptomyces antagonistic activity and analysed bacterial and Streptomyces populations via 454 pyrosequencing. Host plant species and plant richness treatments altered networks of coassociation among bacterial taxa, suggesting the potential for host plant effects on the soil microbiome to include changes in microbial interaction dynamics and, consequently, co-evolution. Taxa that were coassociated in the rhizosphere of a given host plant species often showed consistent correlations between operational taxonomic unit (OTU) relative abundance and Streptomyces antagonistic activity, in the rhizosphere of that host. However, in the rhizosphere of a different host plant species, the same OTUs showed no consistency, or a different pattern of responsiveness to such biotic habitat characteristics. The diversity and richness of bacterial and Streptomyces communities exhibited distinct relationships with biotic and abiotic soil characteristics. The rhizosphere soil microbiome is influenced by a complex and nested array of factors at varying spatial scales, including plant community, plant host, soil edaphics and microbial taxon and community characteristics.