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.
Giving back to the community Paredes, Sur Herrera; Lebeis, Sarah L.
Functional ecology,
July 2016, Letnik:
30, Številka:
7
Journal Article
Recenzirano
Odprti dostop
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.
Lay Summary
Specific members of complex microbiota can influence host phenotypes, depending on both the abiotic environment and the presence of other microorganisms. Therefore, it is challenging to define ...bacterial combinations that have predictable host phenotypic outputs. We demonstrate that plant-bacterium binary-association assays inform the design of small synthetic communities with predictable phenotypes in the host. Specifically, we constructed synthetic communities that modified phosphate accumulation in the shoot and induced phosphate starvation-responsive genes in a predictable fashion. We found that bacterial colonization of the plant is not a predictor of the plant phenotypes we analyzed. Finally, we demonstrated that characterizing a subset of all possible bacterial synthetic communities is sufficient to predict the outcome of untested bacterial consortia. Our results demonstrate that it is possible to infer causal relationships between microbiota membership and host phenotypes and to use these inferences to rationally design novel communities.
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.
Plants live in biogeochemically diverse soils with diverse microbiota. Plant organs associate intimately with a subset of these microbes, and the structure of the microbial community can be altered ...by soil nutrient content. Plant-associated microbes can compete with the plant and with each other for nutrients, but may also carry traits that increase the productivity of the plant. It is unknown how the plant immune system coordinates microbial recognition with nutritional cues during microbiome assembly. Here we establish that a genetic network controlling the phosphate stress response influences the structure of the root microbiome community, even under non-stress phosphate conditions. We define a molecular mechanism regulating coordination between nutrition and defence in the presence of a synthetic bacterial community. We further demonstrate that the master transcriptional regulators of phosphate stress response in Arabidopsis thaliana also directly repress defence, consistent with plant prioritization of nutritional stress over defence. Our work will further efforts to define and deploy useful microbes to enhance plant performance.
•Soil microbiomes induce reproducible plant phenotypes.•Large collections of plant-associated microbes are available for research.•Plant growth promoting microbial inoculants can persist in soil for ...weeks.•Co-regulation of immune system function and nutritional stress responses exists.•Deployment of consortia may enable more resilient plant phenotypes than single strains.
After a century of incremental research, technological advances, coupled with a need for sustainable crop yield increases, have reinvigorated the study of beneficial plant–microbe interactions with attention focused on how microbiomes alter plant phenotypes. We review recent advances in plant microbiome research, and describe potential applications for increasing crop productivity. The phylogenetic diversity of plant microbiomes is increasingly well characterized, and their functional diversity is becoming more accessible. Large culture collections are available for controlled experimentation, with more to come. Genetic resources are being brought to bear on questions of microbiome function. We expect that microbial amendments of varying complexities will expose rules governing beneficial plant–microbe interactions contributing to plant growth promotion and disease resistance, enabling more sustainable agriculture.
Priority effects, where arrival order and initial relative abundance modulate local species interactions, can exert taxonomic, functional, and evolutionary influences on ecological communities by ...driving them to alternative states. It remains unclear if these wide-ranging consequences of priority effects can be explained systematically by a common underlying factor. Here, we identify such a factor in an empirical system. In a series of field and laboratory studies, we focus on how pH affects nectar-colonizing microbes and their interactions with plants and pollinators. In a field survey, we found that nectar microbial communities in a hummingbird-pollinated shrub,
(formerly
)
, exhibited abundance patterns indicative of alternative stable states that emerge through domination by either bacteria or yeasts within individual flowers. In addition, nectar pH varied among
flowers in a manner that is consistent with the existence of these alternative stable states. In laboratory experiments,
, the bacterium most commonly found in
nectar, exerted a strongly negative priority effect against
, the most common nectar-specialist yeast, by reducing nectar pH. This priority effect likely explains the mutually exclusive pattern of dominance found in the field survey. Furthermore, experimental evolution simulating hummingbird-assisted dispersal between flowers revealed that
could evolve rapidly to improve resistance against the priority effect if constantly exposed to
-induced pH reduction. Finally, in a field experiment, we found that low nectar pH could reduce nectar consumption by hummingbirds, suggesting functional consequences of the pH-driven priority effect for plant reproduction. Taken together, these results show that it is possible to identify an overarching factor that governs the eco-evolutionary dynamics of priority effects across multiple levels of biological organization.
Aging is associated with loss of circadian immune responses and circadian gene transcription in peripheral macrophages. Microglia, the resident macrophages of the brain, also show diurnal rhythmicity ...in regulating local immune responses and synaptic remodeling. To investigate the interaction between aging and microglial circadian rhythmicity, we examined mice deficient in the core clock transcription factor, BMAL1. Aging Cd11b
;Bmal
mice demonstrated accelerated cognitive decline in association with suppressed hippocampal long-term potentiation and increases in immature dendritic spines. C1q deposition at synapses and synaptic engulfment were significantly decreased in aging Bmal1-deficient microglia, suggesting that BMAL1 plays a role in regulating synaptic pruning in aging. In addition to accelerated age-associated hippocampal deficits, Cd11b
;Bmal
mice also showed deficits in the sleep-wake cycle with increased wakefulness across light and dark phases. These results highlight an essential role of microglial BMAL1 in maintenance of synapse homeostasis in the aging brain.
Plants intimately associate with diverse bacteria. Plant-associated bacteria have ostensibly evolved genes that enable them to adapt to plant environments. However, the identities of such genes are ...mostly unknown, and their functions are poorly characterized. We sequenced 484 genomes of bacterial isolates from roots of Brassicaceae, poplar, and maize. We then compared 3,837 bacterial genomes to identify thousands of plant-associated gene clusters. Genomes of plant-associated bacteria encode more carbohydrate metabolism functions and fewer mobile elements than related non-plant-associated genomes do. We experimentally validated candidates from two sets of plant-associated genes: one involved in plant colonization, and the other serving in microbe-microbe competition between plant-associated bacteria. We also identified 64 plant-associated protein domains that potentially mimic plant domains; some are shared with plant-associated fungi and oomycetes. This work expands the genome-based understanding of plant-microbe interactions and provides potential leads for efficient and sustainable agriculture through microbiome engineering.
The second-generation antipsychotic olanzapine is effective in reducing psychotic symptoms but can cause extreme weight gain in human patients. We investigated the role of the gut microbiota in this ...adverse drug effect using a mouse model. First, we used germ-free C57BL/6J mice to demonstrate that gut bacteria are necessary and sufficient for weight gain caused by oral delivery of olanzapine. Second, we surveyed fecal microbiota before, during, and after treatment and found that olanzapine potentiated a shift towards an "obesogenic" bacterial profile. Finally, we demonstrated that olanzapine has antimicrobial activity in vitro against resident enteric bacterial strains. These results collectively provide strong evidence for a mechanism underlying olanzapine-induced weight gain in mouse and a hypothesis for clinical translation in human patients.
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