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At least 541 records · Page 30

The ectomycorrhizal fungus Pisolithus microcarpus encodes a microRNA involved in cross-kingdom gene silencing during symbiosis

Significance Plant genomes encode hundreds of genes controlling the detection, signaling pathways, and immune responses necessary to defend against pathogens. Pathogens, in turn, continually evolve to evade these defenses. Small RNAs, such as microRNAs (miRNAs), are one mechanism used by pathogens to overcome plant defenses and facilitate plant colonization. Mounting evidence would suggest that beneficial microbes, likewise, use miRNAs to facilitate symbiosis. Here, we demonstrate that the beneficial fungus Pisolithus microcarpus encodes a miRNA that enters plant cells and stabilizes the symbiotic interaction. These results demonstrate that beneficial fungi may regulate host gene expression through the use of miRNAs and sheds light on how beneficial microbes have evolved mechanisms to colonize plant tissues.

59 BASIC BIOLOGICAL SCIENCES↗

Comparing in planta accumulation with microbial routes to set targets for a cost-competitive bioeconomy

Plants and microbes share common metabolic pathways for producing a range of bioproducts that are potentially foundational to the future bioeconomy. However, in planta accumulation and microbial production of bioproducts have never been systematically compared on an economic basis to identify optimal routes of production. A detailed technoeconomic analysis of four exemplar compounds (4-hydroxybenzoic acid [4-HBA], catechol, muconic acid, and 2-pyrone-4,6-dicarboxylic acid [PDC]) is conducted with the highest reported yields and accumulation rates to identify economically advantaged platforms and breakeven targets for plants and microbes. The results indicate that in planta mass accumulation ranging from 0.1 to 0.3 dry weight % (dwt%) can achieve costs comparable to microbial routes operating at 40 to 55% of maximum theoretical yields. These yields and accumulation rates are sufficient to be cost competitive if the products are sold at market prices consistent with specialty chemicals ($20 to $50/kg). Prices consistent with commodity chemicals will require an order-of-magnitude-greater accumulation rate for plants and/or yields nearing theoretical maxima for microbial production platforms. This comparative analysis revealed that the demonstrated accumulation rates of 4-HBA (3.2 dwt%) and PDC (3.0 dwt%) in engineered plants vastly outperform microbial routes, even if microbial platforms were to reach theoretical maximum yields. Their recovery and sale as part of a lignocellulosic biorefinery could enable biofuel prices to be competitive with petroleum. Muconic acid and catechol, in contrast, are currently more attractive when produced microbially using a sugar feedstock. Ultimately, both platforms can play an important role in replacing fossil-derived products.

59 BASIC BIOLOGICAL SCIENCES↗

Effects of Desiccation and Freezing on Microbial Ionizing Radiation Survivability: Considerations for Mars Sample Return

Increasingly, national space agencies are expanding their goals to include Mars exploration with sample return. To better protect Earth and its biosphere from potential extraterrestrial sources of contamination, as set forth in the Outer Space Treaty of 1967, international efforts to develop planetary protection measures strive to understand the danger of cross-contamination processes in Mars sample return missions. We aim to better understand the impact of the martian surface on microbial dormancy and survivability. Radiation resistance of microbes is a key parameter in considering survivability of microbes over geologic times on the frigid, arid surface of Mars that is bombarded by solar and galactic cosmic radiation. We tested the influence of desiccation and freezing on the ionizing radiation survival of six model microorganisms: vegetative cells of two bacteria (Deinococcus radiodurans, Escherichia coli) and a strain of budding yeast (Saccharomyces cerevisiae); and vegetative cells and endospores of three Bacillus bacteria (B. subtilis, B. megaterium, B. thuringiensis). Desiccation and freezing greatly increased radiation survival of vegetative polyploid microorganisms when applied separately, and when combined, desiccation and freezing increased radiation survival even more so. Thus, the radiation survival threshold of polyploid D. radiodurans cells can be extended from the already high value of 25 kGy in liquid culture to an astonishing 140 kGy when the cells are both desiccated and frozen. However, such synergistic radioprotective effects of desiccation and freezing were not observed in monogenomic or digenomic Bacillus cells and endospores, which are generally sterilized by 12 kGy. This difference is associated with a critical requirement for survivability under radiation, that is, repair of genome damage caused by radiation. Deinococcus radiodurans and S. cerevisiae accumulate similarly high levels of the Mn antioxidants that are required for extreme radiation resistance, as do endospores, though they greatly exceed spores in radioresistance because they contain multiple identical genome copies, which in D. radiodurans are joined by persistent Holliday junctions. We estimate ionizing radiation survival limits of polyploid DNA-based life-forms to be hundreds of millions of years of background radiation while buried in the martian subsurface. Our findings imply that forward contamination of Mars will essentially be permanent, and backward contamination is a possibility if life ever existed on Mars.

59 BASIC BIOLOGICAL SCIENCES↗

Viral infections likely mediate microbial controls on ecosystem responses to global warming

Abstract Climate change is affecting how energy and matter flow through ecosystems, thereby altering global carbon and nutrient cycles. Microorganisms play a fundamental role in carbon and nutrient cycling and are thus an integral link between ecosystems and climate. Here, we highlight a major black box hindering our ability to anticipate ecosystem climate responses: viral infections within complex microbial food webs. We show how understanding and predicting ecosystem responses to warming could be challenging—if not impossible—without accounting for the direct and indirect effects of viral infections on different microbes (bacteria, archaea, fungi, protists) that together perform diverse ecosystem functions. Importantly, understanding how rising temperatures associated with climate change influence viruses and virus-host dynamics is crucial to this task, yet is severely understudied. In this perspective, we (i) synthesize existing knowledge about virus-microbe-temperature interactions and (ii) identify important gaps to guide future investigations regarding how climate change might alter microbial food web effects on ecosystem functioning. To provide real-world context, we consider how these processes may operate in peatlands—globally significant carbon sinks that are threatened by climate change. We stress that understanding how warming affects biogeochemical cycles in any ecosystem hinges on disentangling complex interactions and temperature responses within microbial food webs.

54 ENVIRONMENTAL SCIENCES↗

Methanobactin from methanotrophs: genetics, structure, function and potential applications

ABSTRACT Aerobic methane-oxidizing bacteria of the Alphaproteobacteria have been found to express a novel ribosomally synthesized post-translationally modified polypeptide (RiPP) termed methanobactin (MB). The primary function of MB in these microbes appears to be for copper uptake, but MB has been shown to have multiple capabilities, including oxidase, superoxide dismutase and hydrogen peroxide reductase activities, the ability to detoxify mercury species, as well as acting as an antimicrobial agent. Herein, we describe the diversity of known MBs as well as the genetics underlying MB biosynthesis. We further propose based on bioinformatics analyses that some methanotrophs may produce novel forms of MB that have yet to be characterized. We also discuss recent findings documenting that MBs play an important role in controlling copper availability to the broader microbial community, and as a result can strongly affect the activity of microbes that require copper for important enzymatic transformations, e.g. conversion of nitrous oxide to dinitrogen. Finally, we describe procedures for the detection/purification of MB, as well as potential medical and industrial applications of this intriguing RiPP.

54 ENVIRONMENTAL SCIENCES↗

Grf10 regulates the response to copper, iron, and phosphate in Candida albicans

Abstract The pathogenic yeast, Candida albicans, and other microbes must be able to handle drastic changes in nutrient availability within the human host. Copper, iron, and phosphate are essential micronutrients for microbes that are sequestered by the human host as nutritional immunity; yet high copper levels are employed by macrophages to induce toxic oxidative stress. Grf10 is a transcription factor important for regulating genes involved in morphogenesis (filamentation, chlamydospore formation) and metabolism (adenylate biosynthesis, 1-carbon metabolism). The grf10Δ mutant exhibited resistance to excess copper in a gene dosage-dependent manner but grew the same as the wild type in response to other metals (calcium, cobalt, iron, manganese, and zinc). Point mutations in the conserved residues D302 and E305, within a protein interaction region, conferred resistance to high copper and induced hyphal formation similar to strains with the null allele. The grf10Δ mutant misregulated genes involved with copper, iron, and phosphate uptake in YPD medium and mounted a normal transcriptional response to high copper. The mutant accumulated lower levels of magnesium and phosphorus, suggesting that copper resistance is linked to phosphate metabolism. Our results highlight new roles for Grf10 in copper and phosphate homeostasis in C. albicans and underscore the fundamental role of Grf10 in connecting these with cell survival.

59 BASIC BIOLOGICAL SCIENCES↗

Microbiome-enabled genomic selection improves prediction accuracy for nitrogen-related traits in maize

Root-associated microbiomes in the rhizosphere (rhizobiomes) are increasingly known to play an important role in nutrient acquisition, stress tolerance, and disease resistance of plants. However, it remains largely unclear to what extent these rhizobiomes contribute to trait variation for different genotypes and if their inclusion in the genomic selection protocol can enhance prediction accuracy. To address these questions, we developed a microbiome-enabled genomic selection method that incorporated host SNPs and amplicon sequence variants from plant rhizobiomes in a maize diversity panel under high and low nitrogen (N) field conditions. Our cross-validation results showed that the microbiome-enabled genomic selection model significantly outperformed the conventional genomic selection model for nearly all time-series traits related to plant growth and N responses, with an average relative improvement of 3.7%. The improvement was more pronounced under low N conditions (8.4–40.2% of relative improvement), consistent with the view that some beneficial microbes can enhance N nutrient uptake, particularly in low N fields. However, our study could not definitively rule out the possibility that the observed improvement is partially due to the amplicon sequence variants being influenced by microenvironments. Using a high-dimensional mediation analysis method, our study has also identified microbial mediators that establish a link between plant genotype and phenotype. Some of the detected mediator microbes were previously reported to promote plant growth. The enhanced prediction accuracy of the microbiome-enabled genomic selection models, demonstrated in a single environment, serves as a proof-of-concept for the potential application of microbiome-enabled plant breeding for sustainable agriculture.

60 APPLIED LIFE SCIENCES↗

Needle bacterial community structure across the species range of limber pine

Abstract Bacteria on and inside leaves can influence forest tree health and resilience. The distribution and limits of a tree species’ range can be influenced by various factors, with biological interactions among the most significant. We investigated the processes shaping the bacterial needle community across the species distribution of limber pine, a widespread Western conifer inhabiting a range of extreme habitats. We tested four hypotheses: (i) Needle community structure varies across sites, with site-specific factors more important to microbial assembly than host species selection; (ii) dispersal limitation structures foliar communities across the range of limber pine; (iii) the relative significance of dispersal and selection differs across sites in the tree species range; and (iv) needle age structures bacterial communities. We characterized needle communities from the needle surface and tissue of limber pine and co-occurring conifers across 16 sites in the limber pine distribution. Our findings confirmed that site characteristics shape the assembly of bacterial communities across the host species range and showed that these patterns are not driven by dispersal limitation. Furthermore, the strength of selection by the host varied by site, possibly due to differences in available microbes. Our study, by focusing on trees in their natural setting, reveals real needle bacterial dynamics in forests, which is key to understanding the balance between stochastic and deterministic processes in shaping forest tree-microbe interactions. Such understanding will be necessary to predict or manipulate these interactions to support forest ecosystem productivity or assist plant migration and adaptation in the face of global change.

59 BASIC BIOLOGICAL SCIENCES↗

Microbial community dynamics in the soil-root continuum are linked with plant species turnover during secondary succession

Grazing exclusion and land abandonment are commonly adopted to restore degraded ecosystems in semiarid and arid regions worldwide. However, the temporal variation in the soil- versus root-associated microbiome over plant species turnover during secondary succession has rarely been quantified. Using the chronosequence restored from fenced grassland and abandoned farmlands on the Loess Plateau of China, we characterized the dynamics of the soil- and root-associated microbiome of host plant with different dominance statuses during secondary succession from 0 to 40 years. Our results revealed that the root microhabitat, the host plant and their interactions were the main contributors to the bacterial community shift (R 2 = 15.5%, 8.1%, and 22.3%, respectively), and plant interspecies replacement had a greater effect on the shift in the root-associated microbial community than intraspecies replacement did during succession. The root-associated bacterial community of pioneer plants was particularly responsive to succession, especially the endosphere community. Endosphere microbial diversity was positively correlated with host plant coverage change, and the diversity and abundance of taxon recruitment into the endosphere of pioneer plants from the surrounding environment decreased as succession progressed. The community assembly processes also indicated that the endosphere microbiota are strongly selected in younger host plants, whereas stochastic processes dominate in aged host plants. Our study provides evidence of the unique response of the root-associated microbiome to the replacement of plant species during secondary succession, and the function of endosphere microbes should be considered when studying plant–microbe feedback.

59 BASIC BIOLOGICAL SCIENCES↗

Soil microbial community response to corrinoids is shaped by a natural reservoir of vitamin B12

Abstract Soil microbial communities perform critical ecosystem services through the collective metabolic activities of numerous individual organisms. Most microbes use corrinoids, a structurally diverse family of cofactors related to vitamin B12. Corrinoid structure influences the growth of individual microbes, yet how these growth responses scale to the community level remains unknown. Analysis of metagenome-assembled genomes suggests that corrinoids are supplied to the community by members of the archaeal and bacterial phyla Thermoproteota, Actinobacteria, and Proteobacteria. Corrinoids were found largely adhered to the soil matrix in a grassland soil, at levels exceeding those required by cultured bacteria. Enrichment cultures and soil microcosms seeded with different corrinoids showed distinct shifts in bacterial community composition, supporting the hypothesis that corrinoid structure can shape communities. Environmental context influenced both community- and taxon-specific responses to specific corrinoids. These results implicate corrinoids as key determinants of soil microbiome structure and suggest that environmental micronutrient reservoirs promote community stability.

58 GEOSCIENCES↗

Bacterial population-level trade-offs between drought tolerance and resource acquisition traits impact decomposition

Microbes drive fundamental ecosystem processes, such as decomposition. Environmental stressors are known to affect microbes, their fitness, and the ecosystem functions that they perform; yet, understanding the causal mechanisms behind this influence has been difficult. We used leaf litter on soil surface as a model in situ system to assess changes in bacterial genomic traits and decomposition rates for 18 months with drought as a stressor. We hypothesized that genome-scale trade-offs due to investment in stress tolerance traits under drought reduce the capacity for bacterial populations to carry out decomposition, and that these population-level trade-offs scale up to impact emergent community traits, thereby reducing decomposition rates. We observed drought tolerance mechanisms that were heightened in bacterial populations under drought, identified as higher gene copy numbers in metagenome-assembled genomes. A subset of populations under drought had reduced carbohydrate-active enzyme genes that suggested—as a trade-off—a decline in decomposition capabilities. These trade-offs were driven by community succession and taxonomic shifts as distinct patterns appeared in populations. We show that trait–trade-offs in bacterial populations under drought could scale up to reduce overall decomposition capabilities and litter decay rates. Using a trait-based approach to assess the population ecology of soil bacteria, we demonstrate genome-level trade-offs in response to drought with consequences for decomposition rates.

59 BASIC BIOLOGICAL SCIENCES↗

Functional team selection as a framework for local adaptation in plants and their belowground microbiomes

Abstract Multicellular organisms are hosts to diverse communities of smaller organisms known as microbiomes. Plants have distinctive microbiomes that can provide important functions related to nutrition, defense, and stress tolerance. Empirical studies provide convincing evidence that in some—but not all—circumstances, belowground microbiomes help plants adapt to their local environment. The purpose of this review is to develop functional team selection (FTS) as a framework to help predict the conditions necessary for root microbiomes to generate local adaptation for their plant hosts. FTS envisions plants and their microbiomes as complex adaptive systems, and plant adaptations as emergent properties of these systems. If plants have the capacity to recognize and cultivate beneficial microbes and suppress pathogens, then it is possible for plants to evolve the capacity to gain adaptations by curating their microbiome. In resource-limited and stressful environments, the emergent functions of complex microbial systems may contribute to positive feedback linked to plant vigor, and ultimately, local adaptation. The key factors in this process are: (i) selective force, (ii) host constitution, (iii) microbial diversity, and (iv) time. There is increasing interest in harnessing beneficial microbial interactions in agriculture and many microbial growth-promoting products are commercially available, but their use is controversial because a large proportion of these products fail to consistently enhance plant growth. The FTS framework may help direct the development of durable plant-microbiome systems that enhance crop production and diminish pathogens. It may also provide valuable insights for understanding and managing other kinds of host-microbe systems.

Environmental Sciences & Ecology↗

Electroactive biofilms: how microbial electron transfer enables bioelectrochemical applications

Abstract Microbial biofilms are ubiquitous. In marine and freshwater ecosystems, microbe–mineral interactions sustain biogeochemical cycles, while biofilms found on plants and animals can range from pathogens to commensals. Moreover, biofouling and biocorrosion represent significant challenges to industry. Bioprocessing is an opportunity to take advantage of biofilms and harness their utility as a chassis for biocommodity production. Electrochemical bioreactors have numerous potential applications, including wastewater treatment and commodity production. The literature examining these applications has demonstrated that the cell–surface interface is vital to facilitating these processes. Therefore, it is necessary to understand the state of knowledge regarding biofilms’ role in bioprocessing. This mini-review discusses bacterial biofilm formation, cell–surface redox interactions, and the role of microbial electron transfer in bioprocesses. It also highlights some current goals and challenges with respect to microbe-mediated bioprocessing and future perspectives.

59 BASIC BIOLOGICAL SCIENCES↗

Quantitative elemental imaging in eukaryotic algae

Abstract All organisms, fundamentally, are made from the same raw material, namely the elements of the periodic table. Biochemical diversity is achieved by how these elements are utilized, for what purpose, and in which physical location. Determining elemental distributions, especially those of trace elements that facilitate metabolism as cofactors in the active centers of essential enzymes, can determine the state of metabolism, the nutritional status, or the developmental stage of an organism. Photosynthetic eukaryotes, especially algae, are excellent subjects for quantitative analysis of elemental distribution. These microbes utilize unique metabolic pathways that require various trace nutrients at their core to enable their operation. Photosynthetic microbes also have important environmental roles as primary producers in habitats with limited nutrient supplies or toxin contaminations. Accordingly, photosynthetic eukaryotes are of great interest for biotechnological exploitation, carbon sequestration, and bioremediation, with many of the applications involving various trace elements and consequently affecting their quota and intracellular distribution. A number of diverse applications were developed for elemental imaging, allowing subcellular resolution, with X-ray fluorescence microscopy (XFM, XRF) being at the forefront, enabling quantitative descriptions of intact cells in a non-destructive method. This Tutorial Review summarizes the workflow of a quantitative, single-cell elemental distribution analysis of a eukaryotic alga using XFM.

59 BASIC BIOLOGICAL SCIENCES↗

Frontiers and opportunities in bioenergy crop microbiome research networks

Researchers from across the four U.S. Department of Energy Bioenergy Research Centers engaged in a microbiome workshop that focused on identifying challenges and collaboration opportunities to better understand bioenergy-relevant plant–microbe interactions. The virtual workshop included hands-on educational sessions and a keynote address on current best practices in microbiome science and community microbiome standards, as well as breakout sessions aimed at identifying microbiome-related data and measurements that should be prioritized, opportunities for and barriers to integrating plant metabolites to microbiome research, and strategies for more effectively integrating microbiome data and processes into existing models. Based on participant discussion, key findings of the workshop were the need to prioritize scaling data sharing across BRCs and the broader research community and securing collaborative infrastructure in the areas of microbiome-ecosystem modeling and molecular plant-microbe interactions. This workshop review highlights additional main findings from this event, to encourage cross-site and more holistic meta-analyses while promoting wide scientific community engagement across plant microbiome sciences.

09 BIOMASS FUELS↗

Impacts of Soil Microbiome Variations on Root Colonization by Fungi and Bacteria and on the Metabolome of Populus tremula × alba

Trees depend on beneficial interactions between roots and soil microbes for their nutrition and protection against stresses. The soil microbiome provides the main reservoir of microbes for root colonization and is subject to natural variations that can affect its composition. It is not clear whether the tree’s root system is able to buffer the natural variations occurring in the soil microbiome to capture a stable and effective microbiome or whether these variations affect its microbiome to impact its physiology. To address this question, we planted cuttings of Gray Poplar (Populus tremula × alba clone 717-1B4) in natural soil taken from a poplar stand under the same tree over two consecutive years and grew them in a greenhouse. We analyzed the soil and root microbiomes by high throughput Illumina MiSeq sequencing of fungal rDNA internal transcribed spacer and bacterial 16S rRNA amplicons and we characterized the root metabolome by gas chromatography-mass spectrometry. Soil and root microbial communities significantly shifted over the 2 years. A modification of the balance between endophytes, saprophytes, and mycorrhizal fungi occurred in the roots as well as a replacement of some dominant operational taxonomic units by others. These modifications were correlated with a significant alteration of the levels of about 10% of primary and secondary metabolites, suggesting that natural fluctuations in soil microbial communities can have a profound impact on tree root metabolism and physiology. Tree roots functioning may thus be indirectly strongly affected by the effects of future extreme climatic variations on the soil microbiome.

59 BASIC BIOLOGICAL SCIENCES↗

Unraveling Bacterial Adaptation Strategies in the Microbiome Shaped by the Chemical Environment of the Plant Rhizosphere

The rhizosphere is a dynamic environment where rhizodeposits that include primary and secondary metabolites and mucilage serve as nutrient sources for soil microorganisms, attracting them toward plant roots. However, understanding how these microbes specifically respond to plant root chemical signals has been hindered by the challenges of disentangling physical and chemical interactions between the microbes and plant roots. To address this, we implemented an innovative filter-based experimental setup on plant roots that creates a physical barrier while facilitating the exchange of chemical signals. The proteomic analysis of 10 Populus root-associated bacterial strains grown in the presence or absence of a plant in either individual or mixed community conditions provided detailed insights into the functional responses of these strains to the root chemical environment. Additionally, this approach allowed us to discern the impact of root exudates on overall community dynamics. In particular, metaproteomic analyses revealed that each of these 10 microbial members responds uniquely to the presence of the plant, with Bacillus and Pantoea exhibiting the most dramatic favorable impact. Proteomic examination revealed the details of metabolism fine-tuning, including processes such as chemotaxis and ATP-binding cassette transporter proteins. This study demonstrates the application of a filter-based experimental setup to study microbial responses to plant chemicals and sheds light on adaptation strategies employed by various bacterial strains for survival in the rhizosphere.

37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CH↗

MicroFisher: Fungal taxonomic classification for metatranscriptomic and metagenomic data using multiple short hypervariable markers

AbstractProfiling the taxonomic and functional composition of microbes using metagenomic (MG) and metatranscriptomic (MT) sequencing is advancing our understanding of microbial functions. However, the sensitivity and accuracy of microbial classification using genome– or core protein-based approaches, especially the classification of eukaryotic organisms, is limited by the availability of genomes and the resolution of sequence databases. To address this, we propose the MicroFisher, a novel approach that applies multiple hypervariable marker genes to profile fungal communities from MGs and MTs. This approach utilizes the hypervariable regions of ITS and large subunit (LSU) rRNA genes for fungal identification with high sensitivity and resolution. Simultaneously, we propose a computational pipeline (MicroFisher) to optimize and integrate the results from classifications using multiple hypervariable markers. To test the performance of our method, we applied MicroFisher to the synthetic community profiling and found high performance in fungal prediction and abundance estimation. In addition, we also used MGs from forest soil and MTs of root eukaryotic microbes to test our method and the results showed that MicroFisher provided more accurate profiling of environmental microbiomes compared to other classification tools. Overall, MicroFisher serves as a novel pipeline for classification of fungal communities from MGs and MTs.

Wang, Haihua↗