Sarah L. Lebeis

Defining the core Arabidopsis thaliana root microbiome

Land plants associate with a root microbiota distinct from the complex microbial community present in surrounding soil. The microbiota colonizing the rhizosphere (immediately surrounding the root) and the endophytic compartment (within the root) contribute to plant growth, productivity, carbon sequestration and phytoremediation. Colonization of the root occurs despite a sophisticated plant immune system, suggesting finely tuned discrimination of mutualists and commensals from pathogens. Genetic principles governing the derivation of host-specific endophyte communities from soil communities are poorly understood. Here we report the pyrosequencing of the bacterial 16S ribosomal RNA gene of more than 600 Arabidopsis thaliana plants to test the hypotheses that the root rhizosphere and endophytic compartment microbiota of plants grown under controlled conditions in natural soils are sufficiently dependent on the host to remain consistent across different soil types and developmental stages, and sufficiently dependent on host genotype to vary between inbred Arabidopsis accessions. We describe different bacterial communities in two geochemically distinct bulk soils and in rhizosphere and endophytic compartments prepared from roots grown in these soils. The communities in each compartment are strongly influenced by soil type. Endophytic compartments from both soils feature overlapping, low-complexity communities that are markedly enriched in Actinobacteria and specific families from other phyla, notably Proteobacteria. Some bacteria vary quantitatively between plants of different developmental stage and genotype. Our rigorous definition of an endophytic compartment microbiome should facilitate controlled dissection of plant–microbe interactions derived from complex soil communities.

Salicylic acid modulates colonization of the root microbiome by specific bacterial taxa

Immune signals shape root communities To thwart microbial pathogens aboveground, the plant Arabidopsis turns on defensive signaling using salicylic acid. In Arabidopsis plants with modified immune systems, Lebeis et al. show that bacterial communities change in response to salicylic acid signaling in the root zone as well (see the Perspective by Haney and Ausubel). Abundance of some root-colonizing bacterial families increased at the expense of others, partly as a function of whether salicylic acid was used as an immune signal or as a carbon source for microbial growth. Science, this issue p. 860; see also p. 788 Bacteria that are endosymbiotic with the plant root respond to changes in the plant’s signaling status. [Also see Perspective by Haney and Ausubel] Immune systems distinguish “self” from “nonself” to maintain homeostasis and must differentially gate access to allow colonization by potentially beneficial, nonpathogenic microbes. Plant roots grow within extremely diverse soil microbial communities but assemble a taxonomically limited root-associated microbiome. We grew isogenic Arabidopsis thaliana mutants with altered immune systems in a wild soil and also in recolonization experiments with a synthetic bacterial community. We established that biosynthesis of, and signaling dependent on, the foliar defense phytohormone salicylic acid is required to assemble a normal root microbiome. Salicylic acid modulates colonization of the root by specific bacterial families. Thus, plant immune signaling drives selection from the available microbial communities to sculpt the root microbiome.

Microbiota and Host Nutrition across Plant and Animal Kingdoms

Plants and animals each have evolved specialized organs dedicated to nutrient acquisition, and these harbor specific bacterial communities that extend the hosts metabolic repertoire. Similar forces driving microbial community establishment in the gut and plant roots include diet/soil-type, host genotype, and immune system as well as microbe-microbe interactions. Here we show that there is no overlap of abundant bacterial taxa between the microbiotas of the mammalian gut and plant roots, whereas taxa overlap does exist between fish gut and plant root communities. A comparison of root and gut microbiota composition in multiple host species belonging to the same evolutionary lineage reveals host phylogenetic signals in both eukaryotic kingdoms. The reasons underlying striking differences in microbiota composition in independently evolved, yet functionally related, organs in plants and animals remain unclear but might include differences in start inoculum and niche-specific factors such as oxygen levels, temperature, pH, and organic carbon availability.

The potential for give and take in plant–microbiome relationships

Mutualistic microbes present in plant-associate microbial communities provide a variety of benefits for their host, including reciprocal exchange of nutrients and/or protection from biotic and abiotic environmental stresses. Plant microbiomes have remarkably robust composition in comparison to the complex and dynamic microbial environments from which they form, suggesting finely tuned discrimination by the plant host. Here the intersection between the plant immune system and microbiomes will be explored, both as a possible means of shaping community membership and as a consequence elicited by certain colonizing microbes. Notably, the advent of massive parallel sequencing technologies allows the investigation of these beneficial microbial functions within whole community settings, so we can now ask how engagement of the immune response influences subsequent microbial interactions. Thus, we are currently poised for future work defining how the plant immune system impacts microbiomes and consequently host health, allowing us to better understand the potential of plant productivity optimization within complex microbial surroundings.

Giving back to the community: microbial mechanisms of plant–soil interactions

Summary The role of both plants and soil microbes on ecosystem functioning has been long recognized, but the precise feedback mechanisms between them are more elusive. Definition of these interactions is critical if we aim to achieve an integral understanding of ecosystem functioning, and ultimately explain natural, agricultural and synthetic systems. Advances in genomic technologies and the development of more appropriate statistical, mathematical and computational frameworks enable researchers to almost fully describe and measure the diversity of microbial communities in soil, rhizosphere and plant tissues. Under the scaffold of community ecology, we integrate the observed patterns of microbial diversity with current mechanistic understanding of plant–microbe mutualistic and pathogenic interactions, and propose a model in which plant microbial communities are shaped by different ecological forces differentially through the plant life cycle. The same genomic technologies, applied on natural and reconstructed systems, establish that plant genotype has a small, but significant, effect on the microbial community composition in, on and around plant organs. Despite these advances, technical limitations are still important and only a handful of studies exist where a precise genetic element definitively participates in these interactions. Studies at the field or ecosystem level are dominated by agricultural settings, examining microbial species and communities effects on plant productivity; and conversely, that plant genetics and agricultural practices can potentially impose selective pressures on specific microbes and microbial communities. Revitalized interest in plant–soil microbial feedbacks requires researchers to systematically pose and evaluate more complex hypotheses with increasingly more realistic microbial settings. Despite the advances reviewed here, most studies focus on one aspect of plant, microbe and soil interactions. Experiments that simultaneously and methodically manipulate multiple components are necessary to establish the ecological principles, and molecular mechanisms, which drive microbially mediated plant–soil interactions. This knowledge will be critical to predict how environmental changes affect microbial and plant diversity, and will guide efforts to improve agricultural and conservation practices.

Exercising influence: distinct biotic interactions shape root microbiomes.

Root microbiomes are formed from diverse microbial soil settings with extraordinary consistency, suggesting both defined mechanisms of assembly and specific microbial activity. Recent improvements in sequencing technologies, data analysis techniques, and study design, allow definition of the microbiota within these intimate and important relationships with increasing accuracy. Comparing datasets provides powerful insights into the overlap of plant microbiomes, as well as the impacts of surrounding plants and microbes on root microbiomes and long-term soil conditioning. Here we address how recent studies tease apart the impact of various biotic interactions, including: plant-plant, plant-microbe, and microbe-microbe on root microbiome composition.

Bacterial Production of Indole Related Compounds Reveals Their Role in Association Between Duckweeds and Endophytes

Duckweed farming can be a sustainable practice for biofuel production, animal feed supplement, and wastewater treatment, although large scale production remains a challenge. Plant growth promoting bacteria (PGPB) have been shown to improve plant health by producing phytohormones such as auxin. While some of the mechanisms for plant growth promotion have been characterized in soil epiphytes, more work is necessary to understand how plants may select for bacterial endophytes that have the ability to provide an exogenous source of phytohormones such as auxin. We have isolated and characterized forty-seven potentially endophytic bacteria from surface-sterilized duckweed tissues and screened these bacterial strains for production of indole related compounds using the Salkowski colorimetric assay. Indole-3-acetic acid (IAA), indole-3-lactic acid (ILA), and indole produced by various bacterial isolates were verified by mass spectrometry. Using the Salkowski reagent, we found that 79% of the isolated bacterial strains from our collection may be capable of producing indole related compounds to various extents during in vitro growth. Of these bacteria that are producing indole related compounds, 19% are additionally producing indole. There is an apparent correlation between the type of indole related compound produced by a particular bacteria and the duckweed genus from which the bacterial strain is derived. These results suggest the possible association between different duckweed genera and endophytes that are producing distinct types of secondary metabolites. Understanding the role of indole related compounds during interaction between endophytes and the plant host may be useful to help design synthetic bacterial communities that could target specific or multiple species of duckweed in the future to sustainably enhance plant growth.