抗生素抗性基因（ARGs）作为新兴环境污染物，在农业生态系统中的扩散与累积已成为全世界关注的环境问题之一。集约化农业和畜禽养殖大量使用抗生素，以及含有抗生素抗性基因的畜禽粪肥，使得农田土壤成为ARGs的重要储存库。与此同时，在农业生产中，作物土传病害一直是普遍存在的严峻挑战。土传病原菌为了获得更强的生存优势，在长期的进化过程中逐渐具有了较强的抗生素抗性能力。实验室前期研究也表明，病原青枯菌的入侵增加了ARGs和可移动遗传元件（MGEs）的丰度。已有研究证实，相比于化肥和有机肥，生物有机肥可以显著降低青枯病的发病率。因此研究生物有机肥调控植物土传病害与ARGs长期演变及其微生物生态学机制具有重要意义。通过分析低发病率土壤中微生物组成特征，研究其与ARGs的调控关系，进一步探究代谢对微生物和ARGs的影响机制，为有效抑制发病率和ARGs的扩散提供理论依据。

本研究以番茄连作土壤为对象，比较长期施用化学肥料、有机肥和生物有机肥条件下ARGs的演变和群落响应差异，结合盆栽验证实验，利用16S rRNA基因扩增子测序，宏基因组测序和代谢组测序技术，对以下内容进行了深入研究，（1）阐明长期施用生物有机肥在抑制番茄青枯病发生的同时，缓解其相关ARGs积累风险的微生物生态学机制；（2）解析番茄生育期不同阶段生物有机肥处理对根际土壤中ARGs丰度与组成结构的动态影响；（3）探讨生物有机肥对根际土壤代谢物-微生物-ARGs之间级联响应关系的调控机制；（4）基于不同浓度的解淀粉芽孢杆菌T-5接种实验，研究其调控番茄根际抗生素抗性基因与病原菌（青枯菌）的生态学机制，主要研究结果包括：

1. 本研究基于长期连续施用生物有机肥的田间试验，通过16S rRNA基因扩增子测序技术和宏基因组测序技术，系统评估了生物有机肥对ARGs风险的影响。实验设置不施肥（CK），单施化肥（CF），有机肥（OF）和生物有机肥（BF）四个处理，相关性分析显示，土壤中ARGs丰度与番茄青枯病发病率之间存在显著正相关关系，提示ARGs的累积可能与土传病害发生存在共同加剧的风险。微生物群落分析发现，CF处理因长期单一养分投入导致土壤细菌多样性下降，并富集了变形菌门（Proteobacteria）和拟杆菌门（Bacteroidota）等高ARGs携带潜力的菌群，同时显著积累了抗多粘菌素（polymyxin）、抗多重耐药（multidrug）和抗β-内酰胺类 （β-lactam）等类型的抗性基因；而在有机肥处理中，则以抗甲氧苄氨嘧啶（trimethoprim）、抗四环素（tetracycline）和抗磺胺类（sulfonamide）抗性基因的增加为主。进一步分析表明，与CF和OF处理相比，BF处理降低了Pseudomonas_E、Ralstonia、Agrobacterium和Enterobacte等耐药病原菌的丰度。生物有机肥的长期施用不仅可显著降低番茄青枯病的发病率，还能有效缓解由耐药病原菌增殖带来的ARGs环境风险。

2. 在田间长期定位实验的基础上，分别在番茄的苗期，开花期和结实期采集土壤样品，通过宏基因组测序探究生物有机肥对不同生育期内ARGs动态变化特征的影响，结果显示，在整个生育期内土壤细菌多样性与ARGs丰度呈显著负相关关系，高多样性的微生物群落对ARGs扩散具有“稀释”效应。生物有机肥处理中，在番茄生育期，调节微生物多样性的增加会降低ARGs风险。ARGs在生育期内呈现“先升后降”的趋势，而MGEs则处于持续上升的趋势。值得注意的是，BF处理在番茄生育后期对ARGs的抑制作用最为明显，尤其是在抗MLS、Beta-lactam、tetracycline类抗生素抗性基因的风险控制方面。针对微生物群落演替的进一步分析显示，BF处理通过调控根际土壤微生物群落的演替，促进了有益微生物如Pseudomonas、Bacillus和Streptomyces竞争优势的形成，有效抑制病原菌及其携带的抗性基因传播，从而降低ARGs风险。BF通过提高微生物多样性和促进有益菌优势，显著抑制番茄生育后期的抗性基因扩散，在降低发病率的同时降低了潜在的ARGs风险。

3. 结合前期获得的番茄不同生育期ARGs丰度数据与对应时期的土壤代谢组学数据，本研究进一步解析了生物有机肥介导下微生物-土壤代谢物-ARGs之间的生态互作关系。结果表明，施肥会显著影响代谢物的组成并且调控细菌群落变化进而调控ARGs的组成。脂质和含氮化合物类代谢物是驱动Pseudomonas和Variovorax变化的主要因素，胺类主要影响Bacillus的丰度变化，烃类则显著调控Streptomyces的动态，而Ralstonia的变化主要受酚类和醛类代谢物的影响。这种代谢物与微生物之间的协同作用，可能影响ARGs在土壤环境中的传播。进一步分析表明，醇类和酯类是与ARGs密切相关的关键代谢物。在生物有机肥处理中，醇类促进multidrug和β-lactam类ARGs的增加，酯类的减少同时降低氨基糖苷类（aminoglycoside）ARGs；在有机肥处理中，醇类抑制抗aminoglycoside和tetracycline类ARGs，酯类主要抑制抗multidrug类ARGs。这些结果表明，不同类型的代谢物通过影响关键微生物的群落结构，间接调控了ARGs的生态分布格局。

4. 最后，采集长期施用有机肥的土壤，接种不同浓度（10³ CFU/cm³，10⁵ CFU/cm³，10⁷ CFU/cm³和10⁹ CFU/cm³）Bacillus amyloliquefaciens T-5菌株，通过荧光定量PCR技术和16S rRNA基因扩增子测序技术，评估了外源功能菌对番茄根际ARGs动态的影响。试验结果表明，高浓度接种（例如10⁹ CFU/cm³）可在早期迅速定殖并直接抑制青枯病病原菌的定殖，显著降低发病率以及病原菌带来的ARGs风险；而较低浓度有益菌会通过增加优势细菌属如 Pseudomonas、Massilia、Bacillus、Ralstonia和Flavobacterium等与ARGs显著正相关的类群，提高了ARGs的风险；而在10⁹ CFU/cm³处理中会通过增加Bacillus，降低发病指数间接降低ARGs的相对丰度。总体而言，随着有益菌接种量的增加，番茄根际土壤中ARGs丰度呈现先增加后降低的动态变化，高浓度有益菌通过减少病原菌以及调控微生物群落，降低了ARGs的丰度。

综上所述，长期施用生物有机肥能够驱动土壤微生物区系和根际代谢环境的变化，在有效防控番茄青枯病的同时，缓解了土壤ARGs的扩散和积累风险。生物有机肥作为一种可持续农业管理策略，在减少病害发生和遏制ARGs污染方面具有重要应用价值。本研究为制定农田土壤ARGs风险管控策略和促进农业土壤健康提供了科学依据，体现了兼顾病害防控与ARGs风险控制的双重生态效益。

Antibiotic resistance genes (ARGs), as emerging environmental contaminants, have become a global concern due to their widespread dissemination and accumulation in agricultural ecosystems. Intensive agricultural practices, extensive antibiotic usage in livestock farming, and application of animal manure containing ARGs have led agricultural soils to become critical reservoirs for ARGs. Concurrently, soil-borne diseases remain persistent and serious challenges in agricultural production. Soil-borne pathogens have evolved substantial antibiotic resistance to secure ecological advantages, and previous research has demonstrated that Ralstonia invasion significantly elevates the abundance of ARGs and mobile genetic elements (MGEs). Bio-organic fertilizer has been reported to substantially reduce bacterial wilt disease incidence compared to chemical and organic fertilizers. Therefore, investigating the microbial ecological mechanisms underlying bio-organic fertilizer regulation of soil-borne diseases and ARG dynamics holds significant ecological importance. Studying microbial characteristics in soils with lower disease incidence and their regulatory relationships with ARGs, as well as clarifying the influence of metabolites on microbial communities and ARGs, can provide theoretical bases for effectively reducing both disease incidence and ARG dissemination.

Using tomato continuous cropping soils, this study examined ARG evolution and microbial community responses under long-term application of chemical fertilizer (CF), organic fertilizer (OF), and bio-organic fertilizer (BF). Pot experiments were also conducted to validate the field observations, employing 16S rRNA gene amplicon sequencing, metagenomics, and metabolomics. The objectives were: (1) to elucidate the microbial ecological mechanisms by which long-term BF application reduces tomato bacterial wilt and associated ARG accumulation; (2) to clarify the dynamic impacts of BF on ARG abundance and composition in tomato rhizosphere soils at different growth stages; (3) to explore how BF mediates cascading interactions among rhizosphere metabolites, microbes, and ARGs; and (4) to evaluate the ecological mechanisms underlying different inoculation concentrations of Bacillus amyloliquefaciens T-5 in regulating ARGs and pathogens (Ralstonia solanacearum) in the tomato rhizosphere. The following are the main results:

1. Long-term field trials comparing BF, CF, OF, and no fertilizer control (CK) treatments demonstrated a significant positive correlation between ARG abundance and bacterial wilt incidence, suggesting cumulative ARGs potentially amplify soil-borne disease risk. Microbial community analyses indicated that CF decreased bacterial diversity and enriched ARG-hosting taxa such as Proteobacteria and Bacteroidota, significantly accumulating ARGs related to polymyxin, multidrug resistance, and β-lactam antibiotics. OF primarily increased trimethoprim, tetracycline, and sulfonamide ARGs. Compared to CF and OF, BF reduced the abundance of antibiotic-resistant pathogens including Pseudomonas_E, Ralstonia, Agrobacterium, and Enterobacter, effectively mitigating ARG-associated environmental risks.

2. Metagenomic sequencing conducted at the seedling, flowering, and fruiting stages revealed significant negative correlations between soil bacterial diversity and ARG abundance, supporting a dilution effect hypothesis where increased microbial diversity suppresses ARG dissemination. BF enhanced microbial diversity throughout tomato growth, corresponding with ARG reduction, particularly at late growth stages, effectively controlling MLS, Beta-lactam, and tetracycline ARG risks. BF promoted beneficial microbes such as Pseudomonas, Bacillus, and Streptomyces, which competitively inhibited pathogenic microbes and ARG spread, showcasing dual benefits in disease control and ARG risk reduction.

3. Integrated analysis of ARG abundance and metabolomics data revealed BF significantly influenced soil metabolite composition and microbial dynamics. Lipids and nitrogen-containing compounds primarily regulated Pseudomonas and Variovorax; amines affected Bacillus; hydrocarbons regulated Streptomyces; and phenols and aldehydes influenced Ralstonia dynamics. Alcohols and esters were crucial metabolites correlated with ARG dynamics. Specifically, alcohols increased multidrug and Beta-lactam ARGs in BF soils, whereas esters suppressed aminoglycoside ARGs. These results highlighted indirect ARG regulation via metabolite-microbe interactions.

4. Pot experiments involving different inoculation concentrations (10³, 10⁵, 10⁷, and 10⁹ CFU/cm³) of B. amyloliquefaciens T-5 revealed that high inoculation (10⁹ CFU/cm³) rapidly colonized the rhizosphere, significantly reducing bacterial wilt and associated ARG risks. Lower inoculation levels increased positive correlations between dominant taxa (e.g., Pseudomonas, Massilia, Bacillus, Ralstonia, Flavobacterium) and ARGs, potentially increasing ARG risk. Overall, increasing T-5 inoculation concentrations initially raised but subsequently lowered ARG abundance, demonstrating that higher doses effectively controlled pathogens and reduced ARG risks through microbial community modulation.

In conclusion, long-term application of bio-organic fertilizer reshapes soil microbial communities and rhizosphere metabolites, significantly suppressing tomato bacterial wilt disease and mitigating ARG proliferation and accumulation. Thus, bio-organic fertilizer represents a valuable sustainable agricultural management practice with dual ecological benefits of disease control and ARG pollution mitigation. This research provides a scientific foundation for developing ARG risk management strategies and promoting agricultural soil health.

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