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Understanding the ancestral transition from anaerobic to aerobic lifestyles is essential for comprehending life's early evolution. However, the biological adaptations occurring during this crucial transition remain largely unexplored. Thiamine is an important cofactor involved in central carbon metabolism and aerobic respiration. Here, we explored the phylogenetic and global distribution of thiamine-auxotrophic and thiamine-prototrophic bacteria based on the thiamine biosynthetic pathway in 154 838 bacterial genomes. We observed strong coincidences of the origin of thiamine-synthetic bacteria with the "Great Oxygenation Event," indicating that thiamine biosynthesis in bacteria emerged as an adaptation to aerobic respiration. Furthermore, we demonstrated that thiamine-mediated metabolic interactions are fundamental factors influencing the assembly and diversity of bacterial communities by a global survey across 4245 soil samples. Through our newly established stable isotope probing-metabolic modeling method, we uncovered the active utilization of thiamine-mediated metabolic interactions by bacterial communities in response to changing environments, thus revealing an environmental adaptation strategy employed by bacteria at the community level. Our study demonstrates the widespread thiamine-mediated metabolic interactions in bacterial communities and their crucial roles in setting the stage for an evolutionary transition from anaerobic to aerobic lifestyles and subsequent environmental adaptation. These findings provide new insights into early bacterial evolution and their subsequent growth and adaptations to environments.

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In plant environments, there exist heterogeneous microbial communities, referred to as the plant microbiota, which are recruited by plants and play crucial roles in promoting plant growth, aiding in resistance against pathogens and environmental stresses, thereby maintaining plant health. These microorganisms, along with their genomes, collectively form the plant microbiome. Research on the plant microbiome can help unravel the intricate interactions between plants and microbes, providing a theoretical foundation to reduce pesticide use, enhance agricultural productivity, and promote environmental sustainability. Despite significant progress in the field of research, unresolved challenges persist due to ongoing technological limitations and the complexities inherent in studying microorganisms at small scales. Recently, synthetic community (SynCom) has emerged as a novel technique for microbiome research, showing promising prospects for applications in the plant microbiome field. This article systematically introduces the origin and distribution of plant microbiota, the processes of their recruitment and colonization, and the mechanisms underlying their beneficial functions for plants, from the aspects of composition, assembly, and function. Furthermore, we discuss the principles, applications, challenges, and prospects of SynCom for promoting plant health.

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Existing models of the human skin have aided our understanding of skin health and disease. However, they currently lack a microbial component, despite microbes' demonstrated connections to various skin diseases. Here, we present a robust, standardized model of the skin microbial community (SkinCom) to support in vitro and in vivo investigations. Our methods lead to the formation of an accurate, reproducible, and diverse community of aerobic and anaerobic bacteria. Subsequent testing of SkinCom on the dorsal skin of mice allowed for DNA and RNA recovery from both the applied SkinCom and the dorsal skin, highlighting its practicality for in vivo studies and -omics analyses. Furthermore, 66% of the responses to common cosmetic chemicals in vitro were in agreement with a human trial. Therefore, SkinCom represents a valuable, standardized tool for investigating microbe-metabolite interactions and facilitates the experimental design of in vivo studies targeting host-microbe relationships.

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The study aimed to develop a synthetic microbial community capable of managing postharvest black spot disease in winter jujube. The research revealed that treatment with Debaryomyces nepalensis altered the surface microbial community, reducing the presence of harmful fungi such as Alternaria, Penicillium, Fusarium, and Botrytis, while boosting beneficial bacteria like Pantoea, Bacillus, Staphylococcus, and Pseudomonas, leading to a decreased decay rate in date fruits. A synthetic community was crafted, integrating D. nepalensis with seven other bacterial strains selected for their abundance, compatibility, culturability, and interactions. This community was refined through homo-pore damage experiments and safety assessments to a final formulation consisting of D. nepalensis and six other bacteria: Bacillus subtilis, Bacillus velezensis, Staphylococcus arlettae, Staphylococcus gallinarum, Pseudomonas sp., and Pseudomonas psychrotolerans. Fruit inoculation tests demonstrated that this synthetic community (6 + 1) significantly lowered the incidence and size of black spot lesions compared to single-strain treatments. By the 10th day of storage, the incidence was 69.23 % lower than the control and 52.94 % lower than the group treated solely with D. nepalensis. Mechanistic studies of the synthetic community's antibacterial effects showed that it can produce volatile compounds, proteases, and ß-1,3-glucanase to inhibit pathogen growth. Additionally, the community forms a biofilm to compete for nutrients and induce jujube resistance to disease.

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Synthetic microbial community has widely concerned in the fields of agriculture, food and environment over the past few years. However, there is little consensus on the method to synthetic microbial community from construction to functional verification. Here, we review the concept, characteristics, history and applications of synthetic microbial community, summarizing several methods for synthetic microbial community construction, such as isolation culture, core microbiome mining, automated design, and gene editing. In addition, we also systematically summarized the design concepts, technological thresholds, and applicable scenarios of various construction methods, and highlighted their advantages and limitations. Ultimately, this review provides four efficient, detailed, easy-to-understand and -follow steps for synthetic microbial community construction, with major implications for agricultural practices, food production, and environmental governance.

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The rhizosphere constitutes a dynamic interface between plant hosts and their associated microbial communities. Despite the acknowledged potential for enhancing plant fitness by manipulating the rhizosphere, the engineering of the rhizosphere microbiome through inoculation has posed significant challenges. These challenges are thought to arise from the competitive microbial ecosystem where introduced microbes must survive, and the absence of adaptation to the specific metabolic and environmental demands of the rhizosphere. Here, we engineered a synthetic rhizosphere community (SRC1) with the anticipation that it would exhibit a selective advantage in colonizing the host Sorghum bicolor, thereby potentially fostering its growth. SRC1 was assembled from bacterial isolates identified either for their potential role in community cohesion through network analysis or for their ability to benefit from host-specific exudate compounds. The growth performance of SRC1 was assessed in vitro on solid media, in planta under gnotobiotic laboratory conditions, and in the field. Our findings reveal that SRC1 cohesion is most robust when cultivated in the presence of the plant host under laboratory conditions, with lineages being lost from the community when grown either in vitro or in a native field setting. We establish that SRC1 effectively promotes the growth of both above- and below-ground plant phenotypes in both laboratory and native field contexts. Furthermore, in laboratory conditions, these growth enhancements correlate with the transcriptional dampening of lignin biosynthesis in the host. Collectively, these results underscore the potential utility of synthetic microbial communities for modulating crop performance in controlled and native environments alike.

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The use of rhizospheric SynComs can be a new and sustainable strategy in the agrobiotechnology sector. The objective of this study was to create the most appropriate SynCom composition; examine the ability to dissolve natural rock phosphate (RP) from Morocco in liquid-modified NBRIP medium; determine organic acids, and phytohormones; and verify plant growth promoting and nutrition uptake effect in the pot experiments of winter wheat (Triticum aestivum). A total of nine different microorganisms were isolated, which belonged to three different genera: Bacillus, Pseudomonas, and Streptomyces. Out of the 21 treatments tested, four SynComs had the best phosphate-dissolving properties: IJAK-27+44+91 (129.17 mg L-1), IIBEI-32+40 (90.95 µg mL-1), IIIDEG-45+41 (122.78 mg L-1), and IIIDEG-45+41+72 (120.78 mg L-1). We demonstrate that these SynComs are capable of producing lactic, acetic, gluconic, malic, oxalic, citric acids, and phytohormones such as indole-3-acetic acid, zeatin, gibberellic acid, and abscisic acid. In pot experiments with winter wheat, we also demonstrated that the designed SynComs were able to effectively colonize the plant root rhizosphere and contributed to more abundant plant growth characteristics and nutrient uptake as uninoculated treatment or uninoculated treatment with superphosphate (NPK 0-19-0). The obtained results show that the SynCom compositions of IJAK-27+44+91, IIBEI-32+40, IIIDEG-45+41, and IIIDEG-45+41+72 can be considered as promising candidates for developing biofertilizers to facilitate P absorption and increase plant nutrition.

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BACKGROUND: Plant microbiota contributes to plant growth and health, including enhancing plant resistance to various diseases. Despite remarkable progress in understanding diseases resistance in plants, the precise role of rhizosphere microbiota in enhancing watermelon resistance against soil-borne diseases remains unclear. Here, we constructed a synthetic community (SynCom) of 16 core bacterial strains obtained from the rhizosphere of grafted watermelon plants. We further simplified SynCom and investigated the role of bacteria with synergistic interactions in promoting plant growth through a simple synthetic community. RESULTS: Our results demonstrated that the SynCom significantly enhanced the growth and disease resistance of ungrafted watermelon grown in non-sterile soil. Furthermore, analysis of the amplicon and metagenome data revealed the pivotal role of Pseudomonas in enhancing plant health, as evidenced by a significant increase in the relative abundance and biofilm-forming pathways of Pseudomonas post-SynCom inoculation. Based on in vitro co-culture experiments and bacterial metabolomic analysis, we selected Pseudomonas along with seven other members of the SynCom that exhibited synergistic effects with Pseudomonas. It enabled us to further refine the initially constructed SynCom into a simplified SynCom comprising the eight selected bacterial species. Notably, the plant-promoting effects of simplified SynCom were similar to those of the initial SynCom. Furthermore, the simplified SynCom protected plants through synergistic effects of bacteria. CONCLUSIONS: Our findings suggest that the SynCom proliferate in the rhizosphere and mitigate soil-borne diseases through microbial synergistic interactions, highlighting the potential of synergistic effects between microorganisms in enhancing plant health. This study provides a novel insight into using the functional SynCom as a promising solution for sustainable agriculture. Video Abstract.

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BACKGROUND: Apple Replant Disease (ARD) is common in major apple-growing regions worldwide, but the role of rhizosphere microbiota in conferring ARD resistance and promoting plant growth remains unclear. RESULTS: In this study, a synthetic microbial community (SynCom) was developed to enhance apple plant growth and combat apple pathogens. Eight unique bacteria selected via microbial culture were used to construct the antagonistic synthetic community, which was then inoculated into apple seedlings in greenhouse experiments. Changes in the rhizomicroflora and the growth of aboveground plants were monitored. The eight strains, belonging to the genera Bacillus and Streptomyces, have the ability to antagonize pathogens such as Fusarium oxysporum, Rhizoctonia solani, Botryosphaeria ribis, and Physalospora piricola. Additionally, these eight strains can stably colonize in apple rhizosphere and some of them can produce siderophores, ACC deaminase, and IAA. Greenhouse experiments with Malus hupehensis Rehd indicated that SynCom promotes plant growth (5.23%) and increases the nutrient content of the soil, including soil organic matter (9.25%) and available K (1.99%), P (7.89%), and N (0.19%), and increases bacterial richness and the relative abundance of potentially beneficial bacteria. SynCom also increased the stability of the rhizosphere microbial community, the assembly of which was dominated by deterministic processes (|ß NTI| > 2). CONCLUSIONS: Our results provide insights into the contribution of the microbiome to pathogen inhibition and host growth. The formulation and manipulation of similar SynComs may be a beneficial strategy for promoting plant growth and controlling soil-borne disease.

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BACKGROUND: After two decades of extensive microbiome research, the current forefront of scientific exploration involves moving beyond description and classification to uncovering the intricate mechanisms underlying the coalescence of microbial communities. Deciphering microbiome assembly has been technically challenging due to their vast microbial diversity but establishing a synthetic community (SynCom) serves as a key strategy in unravelling this process. Achieving absolute quantification is crucial for establishing causality in assembly dynamics. However, existing approaches are primarily designed to differentiate a specific group of microorganisms within a particular SynCom. RESULTS: To address this issue, we have developed the differential fluorescent marking (DFM) strategy, employing three distinguishable fluorescent proteins in single and double combinations. Building on the mini-Tn7 transposon, DFM capitalises on enhanced stability and broad applicability across diverse Proteobacteria species. The various DFM constructions are built using the pTn7-SCOUT plasmid family, enabling modular assembly, and facilitating the interchangeability of expression and antibiotic cassettes in a single reaction. DFM has no detrimental effects on fitness or community assembly dynamics, and through the application of flow cytometry, we successfully differentiated, quantified, and tracked a diverse six-member SynCom under various complex conditions like root rhizosphere showing a different colonisation assembly dynamic between pea and barley roots. CONCLUSIONS: DFM represents a powerful resource that eliminates dependence on sequencing and/or culturing, thereby opening new avenues for studying microbiome assembly. Video Abstract.

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Plant can recruit beneficial microbes to enhance their ability to resist disease. Selenium is well established as a beneficial element in plant growth, but its role in mediating microbial disease resistance remained poorly understood. Here, we investigated the correlation between selenium, oilseed rape rhizosphere microbes and Sclerotinia sclerotiorum. Soil application of 0.5 and 1.0 mg/kg selenium significantly increased the resistance of oilseed rape to Sclerotinia sclerotiorum compared with no selenium application, and the disease inhibition rate was higher than 20%. The disease resistance of oilseed rape was related to rhizosphere microorganisms, and beneficial bacteria isolated from the rhizosphere inhibited Sclerotinia stem rot. Burkholderia cepacia, and synthetic community enhanced plant disease resistance through transcriptional regulation and activated plant-induced systemic resistance to protect plants. Besides, inoculation of isolated bacteria optimized the bacterial community structure of leaves and enriched beneficial microorganisms such as Bacillus, Pseudomonas and Sphingomonas. Bacillus isolated from the leaves were sprayed on the detached leaves, and it also performed a significant inhibition effect on Sclerotinia sclerotiorum. Overall, our results suggested that selenium drive plant rhizosphere microorganisms to increase resistance to Sclerotinia sclerotiorum in oilseed rape.

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The precise impact of species and strain diversity on fungal-bacterial interactions and the overall community functioning has remained unclear. First, our study revealed how Debaryomyces hansenii influences diverse bacteria to accumulate key metabolites in a simulated fermented food system. For flavor, D. hansenii promoted the accumulation of branched-chain esters in Staphylococcus xylosus by promoting growth and facilitating the precursor branched-chain acids transformations but hindered the accumulation of Staphylococcus equorum. Furthermore, fungal-bacterial interactions displayed diversity among S. equorum strains. For bioactive compounds, species and strain diversity of lactic acid bacteria (LAB) also influences the production of indole derivatives. Then, we investigated specific metabolic exchanges under reciprocal interaction. Amino acids, rather than vitamins, were identified as the primary drivers of the bacterial growth promotion. Moreover, precursor transformations by D. hansenii played a significant role in branched-chain esters production. Finally, a synthetic community capable of producing high concentrations of branched-chain esters and indole derivatives was successfully constructed. These results provide valuable insights into understanding and designing synthetic communities for fermented sausages.

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AIMS: In this study, the control effects of synthetic microbial communities composed of peanut seed bacteria against seed aflatoxin contamination caused by Aspergillus flavus and root rot by Fusarium oxysporum were evaluated. METHODS AND RESULTS: Potentially conserved microbial synthetic communities (C), growth-promoting synthetic communities (S), and combined synthetic communities (CS) of peanut seeds were constructed after 16S rRNA Illumina sequencing, strain isolation, and measurement of plant growth promotion indicators. Three synthetic communities showed resistance to root rot and CS had the best effect after inoculating into peanut seedlings. This was achieved by increased defense enzyme activity and activated salicylic acid (SA)-related, systematically induced resistance in peanuts. In addition, CS also inhibited the reproduction of A. flavus on peanut seeds and the production of aflatoxin. These effects are related to bacterial degradation of toxins and destruction of mycelia. CONCLUSIONS: Inoculation with a synthetic community composed of seed bacteria can help host peanuts resist the invasion of seeds by A. flavus and seedlings by F. oxysporum and promote the growth of peanut seedlings.

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Synthetic Communities (SynComs) are being developed and tested to manipulate plant microbiota and improve plant health. To date, only few studies proposed the use of SynCom on seed despite its potential for plant microbiota engineering. We developed and presented a simple and effective seedling microbiota engineering method using SynCom inoculation on seeds. The method was successful using a wide diversity of SynCom compositions and bacterial strains that are representative of the common bean seed microbiota. First, this method enables the modulation of seed microbiota composition and community size. Then, SynComs strongly outcompeted native seed and potting soil microbiota and contributed on average to 80% of the seedling microbiota. We showed that strain abundance on seed was a main driver of an effective seedling microbiota colonization. Also, selection was partly involved in seed and seedling colonization capacities since strains affiliated to Enterobacteriaceae and Erwiniaceae were good colonizers while Bacillaceae and Microbacteriaceae were poor colonizers. Additionally, the engineered seed microbiota modified the recruitment and assembly of seedling and rhizosphere microbiota through priority effects. This study shows that SynCom inoculation on seeds represents a promising approach to study plant microbiota assembly and its consequence on plant fitness.

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During prolonged resource limitation, bacterial cells can persist in metabolically active states of non-growth. These maintenance periods, such as those experienced in stationary phase, can include upregulation of secondary metabolism and release of exometabolites into the local environment. As resource limitation is common in many environmental microbial habitats, we hypothesized that neighboring bacterial populations employ exometabolites to compete or cooperate during maintenance and that these exometabolite-facilitated interactions can drive community outcomes. Here, we evaluated the consequences of exometabolite interactions over the stationary phase among three environmental strains: Burkholderia thailandensis E264, Chromobacterium subtsugae ATCC 31532, and Pseudomonas syringae pv. tomato DC3000. We assembled them into synthetic communities that only permitted chemical interactions. We compared the responses (transcripts) and outputs (exometabolites) of each member with and without neighbors. We found that transcriptional dynamics were changed with different neighbors and that some of these changes were coordinated between members. The dominant competitor B. thailandensis consistently upregulated biosynthetic gene clusters to produce bioactive exometabolites for both exploitative and interference competition. These results demonstrate that competition strategies during maintenance can contribute to community-level outcomes. It also suggests that the traditional concept of defining competitiveness by growth outcomes may be narrow and that maintenance competition could be an additional or alternative measure. IMPORTANCE: Free-living microbial populations often persist and engage in environments that offer few or inconsistently available resources. Thus, it is important to investigate microbial interactions in this common and ecologically relevant condition of non-growth. This work investigates the consequences of resource limitation for community metabolic output and for population interactions in simple synthetic bacterial communities. Despite non-growth, we observed active, exometabolite-mediated competition among the bacterial populations. Many of these interactions and produced exometabolites were dependent on the community composition but we also observed that one dominant competitor consistently produced interfering exometabolites regardless. These results are important for predicting and understanding microbial interactions in resource-limited environments.

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Bacterial communities in the phyllosphere, the above-ground parts of plants, are diverse yet understudied. These bacteria are important for plant health and also for inter-kingdom interactions with beneficial and pest insect species. Here, we present draft genomes of eight culturable bacterial isolates from leaf surfaces in the Pisum sativum phyllosphere.

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IMPORTANCE: We report here efforts to benchmark performance of two widespread approaches for virome analysis, which target either virion-associated nucleic acids (VANA) or highly purified double-stranded RNAs (dsRNAs). This was achieved using synthetic communities of varying complexity levels, up to a highly complex community of 72 viral agents (115 viral molecules) comprising isolates from 21 families and 61 genera of plant viruses. The results obtained confirm that the dsRNA-based approach provides a more complete representation of the RNA virome, in particular, for high complexity ones. However, for viromes of low to medium complexity, VANA appears a reasonable alternative and would be the preferred choice if analysis of DNA viruses is of importance. Several parameters impacting performance were identified as well as a direct relationship between the completeness of virome description and sample sequencing depth. The strategy, results, and tools used here should prove useful in a range of virome analysis efforts.

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BACKGROUND: Shrimp cultured in a biofloc system (BFS) have a lower disease incidence than those farmed in a water exchange system (WES). Although a number of studies have reported that the gut bacterial community induced by BFS is highly associated with shrimp disease resistance, the causal relationship remains unknown. Here, the promotive roles of gut bacterial community induced by BFS in pathogenic Vibrio infection resistance and its potential micro-ecological and physiological mechanisms were investigated by gut bacterial consortium transplantation and synthetic community (SynCom) construction. RESULTS: The BFS induced a more stable and resistant gut bacterial community, and significantly enriched some beneficial bacterial taxa, such as Paracoccus, Ruegeria, Microbacterium, Demequina, and Tenacibaculum. Transplantation of a gut bacterial consortium from BFS shrimp (EnrichBFS) greatly enhanced the stability of the bacterial community and resistance against pathogenic V. parahaemolyticus infection in WES shrimp, while transplantation of a gut bacterial consortium from WES shrimp significantly disrupted the bacterial community and increased pathogen susceptibility in both WES and BFS shrimp. The addition of EnrichBFS in shrimp postlarvae also improved the pathogen resistance through increasing the relative abundances of beneficial bacterial taxa and stability of bacterial community. The corresponding strains of five beneficial bacterial taxa enriched in BFS shrimp were isolated to construct a SynComBFS. The addition of SynComBFS could not only suppress disease development, but also improve shrimp growth, boost the digestive and immune activities, and restore health in diseased shrimp. Furthermore, the strains of SynComBFS well colonized shrimp gut to maintain a high stability of bacterial community. CONCLUSIONS: Our study reveals an important role for native microbiota in protecting shrimp from bacterial pathogens and provides a micro-ecological regulation strategy towards the development of probiotics to ameliorate aquatic animal diseases. Video Abstract.

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Microbial interactions play an important role in regulating the metabolic function of fermented food communities, especially the production of key flavor compounds. However, little is known about specific molecular mechanisms that regulate the production of key flavor compounds through microbial interactions. Here, we designed a synthetic consortium containing Debaryomyces hansenii D1, Staphylococcus xylosus S1, and Pediococcus pentosaceus PP1 to explore the mechanism of the microbial interactions underlying the branched-chain aldehydes production. In this consortium, firstly, D. hansenii secreted amino acids that promoted the growth of P. pentosaceus and S. xylosus. Specifically, D. hansenii D1 secreted alanine, aspartate, glutamate, glutamine, glycine, phenylalanine, serine, and threonine, which were the primary nutrients for bacterial growth. P. pentosaceus PP1 utilized all these eight amino acids through cross-feeding, whereas S. xylosus S1 did not utilize aspartate and serine. Furthermore, D. hansenii D1 promoted the production of branched-chain aldehydes from S. xylosus and P. pentosaceus through cross-feeding of α-keto acids (intermediate metabolites). Thus, the accumulation of 2-methyl-butanal was promoted in all co-culture. Overall, this work revealed the mechanism by which D. hansenii and bacteria cross-feed to produce branched-chain aldehydes in fermented sausages.

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Fungal endophytes play critical roles in helping plants adapt to adverse environmental conditions. The root endophyte Phomopsis liquidambaris can promote the growth and disease control of peanut plants grown under monocropping systems; however, how such beneficial traits are produced is largely unknown. Since the plant endophytic microbiome is directly linked to plant growth and health, and the composition of which has been found to be potentially influenced by microbial inoculants, this study aims to clarify the roles of root endophytic bacterial communities in P. liquidambaris-mediated plant fitness enhancement under monocropping conditions. Here, we found that P. liquidambaris inoculation induced significant changes in the root bacterial community: enriching some beneficial bacteria such as Bradyrhizobium sp. and Streptomyces sp. in the roots, and improving the core microbial-based interaction network. Next, we assembled and simplified a synthetic community (SynII) based on P. liquidambaris-derived key taxa, including Bacillus sp. HB1, Bacillus sp. HB9, Burkholderia sp. MB7, Pseudomonas sp. MB2, Streptomyces sp. MB6, and Bradyrhizobium sp. MB15. Furthermore, the application of the simplified synthetic community suppressed root rot caused by Fusarium oxysporum, promoted plant growth, and increased peanut yields under continuous monocropping conditions. The resistance of synII to F. oxysporum is related to the increased activity of defense enzymes. In addition, synII application significantly increased shoot and root biomass, and yield by 35.56%, 81.19%, and 34.31%, respectively. Collectively, our results suggest that the reshaping of root core microbiota plays an important role in the probiotic-mediated adaptability of plants under adverse environments.

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