Daniel C. Schlatter

A Coevolutionary Framework for Managing Disease-Suppressive Soils

This review explores a coevolutionary framework for the study and management of disease-suppressive soil microbial communities. Because antagonistic microbial interactions are especially important to disease suppression, conceptual, theoretical, and empirical work on antagonistic coevolution and its relevance to disease suppression is reviewed. In addition, principles of coevolution are used to develop specific predictions regarding the drivers of disease-suppressive potential in soil microbial communities and to highlight important areas for future research. This approach brings an evolutionary perspective to microbial community management and emphasizes the role of species interactions among indigenous nonpathogenic microbes in developing and maintaining disease-suppressive activities in soil.

Streptomyces competition and co-evolution in relation to plant disease suppression

High densities of antagonistic Streptomyces are associated with plant disease suppression in many soils. Here we review use of inoculation and organic matter amendments for enriching antagonistic Streptomyces populations to reduce plant disease and note that effective and consistent disease suppression in response to management has been elusive. We argue that shifting the focus of research from short-term disease suppression to the population ecology and evolutionary biology of antagonistic Streptomyces in soil will enhance prospects for effective management. A framework is presented for considering the impacts of short- and long-term management on competitive and coevolutionary dynamics among Streptomyces populations in relation to disease suppression.

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.

Sympatric inhibition and niche differentiation suggest alternative coevolutionary trajectories among Streptomycetes

Soil bacteria produce a diverse array of antibiotics, yet our understanding of the specific roles of antibiotics in the ecological and evolutionary dynamics of microbial interactions in natural habitats remains limited. Here, we show a significant role for antibiotics in mediating antagonistic interactions and nutrient competition among locally coexisting Streptomycete populations from soil. We found that antibiotic inhibition is significantly more intense among sympatric than allopatric Streptomycete populations, indicating local selection for inhibitory phenotypes. For sympatric but not allopatric populations, antibiotic inhibition is significantly positively correlated with niche overlap, indicating that inhibition is targeted toward bacteria that pose the greatest competitive threat. Our results support the hypothesis that antibiotics serve as weapons in mediating local microbial interactions in soil and suggest that coevolutionary niche displacement may reduce the likelihood of an antibiotic arms race. Further insight into the diverse roles of antibiotics in microbial ecology and evolution has significant implications for understanding the persistence of antibiotic inhibitory and resistance phenotypes in environmental microbes, optimizing antibiotic drug discovery and developing strategies for managing microbial coevolutionary dynamics to enhance inhibitory phenotypes.

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.

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.

Global biogeography of Streptomyces antibiotic inhibition, resistance, and resource use

Although recent molecular techniques have greatly expanded our knowledge of microbial biogeography, the functional biogeography of soil microorganisms remains poorly understood. In this work, we explore geographic variation in Streptomyces phenotypes that are critical to species interactions. Specifically, we characterize Streptomyces from different locations from multiple continents for antibiotic inhibition, resistance, and resource use phenotypes. Streptomyces from different locations varied significantly in antibiotic inhibition, resistance, and resource use indicating that communities vary in functional potential. Among all isolates, there were substantial differences in antibiotic inhibition, resistance, and resource use within and among and within Streptomyces species. Moreover, Streptomyces with near-identical 16S rRNA gene sequences from different locations sometimes differed significantly in inhibition, resistance, and resource use phenotypes, suggesting that these phenotypes may be locally adapted. Thus, in addition to a likely role of environmental filtering, variation in Streptomyces inhibitory, resistance, and resource use phenotypes among locations is likely to be a consequence of local selection mediated by species interactions.

Rapid and Specific Method for Evaluating Streptomyces Competitive Dynamics in Complex Soil Communities

ABSTRACT Quantifying target microbial populations in complex communities remains a barrier to studying species interactions in soil environments. Quantitative PCR (qPCR) assays were developed for quantifying pathogenic Streptomyces scabiei and antibiotic-producing Streptomyces lavendulae strains in complex soil communities. This assay will be useful for evaluating the competitive dynamics of streptomycetes in soil.

Bacterial Communities on Wheat Grown Under Long-Term Conventional Tillage and No-Till in the Pacific Northwest of the United States

Cultural practices, such as tillage, often have widespread impacts on phytobiomes. No-till has been increasingly adopted by wheat growers in the dryland cropping areas of the inland Pacific Northwest in the United States to reduce soil erosion and decrease fuel and labor inputs, yet there are limited data on how conversion to no-till impacts plant-associated bacteria in this highly productive system. To address this knowledge gap, we evaluated bacterial communities in bulk and rhizosphere soil of wheat in two locations (Idaho and Washington) for 2 years, comparing long-term no-till plots and adjacent plots under conventional tillage. In this study, members of phylum Proteobacteria were relatively more abundant in rhizosphere soil, while Acidobacteria and Gemmatimonadetes were more abundant in bulk soil than in the rhizosphere. Bacteroidetes were more frequent under conventional than conservation tillage. In general, bacterial families were more affected by the position of the sample (rhizosphere versus bu...

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

BackgroundTradeoffs 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.ResultsStreptomyces 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.ConclusionsThis 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.