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群体感应淬灭芽孢杆菌通过种间信号作用来塑造柑橘真菌组。

Bacillus quorum quenching shapes the citrus mycobiome through interkingdom signaling.

机构信息

State Key Laboratory for Conservation and Utilization of Bio-Resources in Yunnan, Yunnan Agricultural University, Kunming, China.

State Key Laboratory for Conservation and Utilization of Bio-Resources in Yunnan, Yunnan Agricultural University, Kunming, China.

出版信息

Sci Total Environ. 2024 Dec 15;956:177074. doi: 10.1016/j.scitotenv.2024.177074. Epub 2024 Nov 8.

DOI:10.1016/j.scitotenv.2024.177074
PMID:39454793
Abstract

Microbiomes are sustained through infinite yet mutually interacting microbial communities, with bacteria and fungi serving as the major constituents. In recent times, microbial interventions have become popular for microbiome manipulation to achieve sustainable goals. Whether and how the introduced biocontrol agent drives fungal microbial assemblages (mycobiome) and the role of interkingdom signaling in shaping the microbiome structure and function remain poorly understood. Here, we implemented wild-type (WT) Bacillus subtilis L1-21 and its quorum quenching (QQ) mutants (L1-21Δytnp, and L1-21Δyxel) individually and as consortia to explore the enrichment patterns of key mycobiome members in Huanglongbing (HLB) infected citrus compartments including leaf endosphere, root endosphere, and rhizosphere soil. The application of WT and its QQ mutants produced differential mycobiome enrichment across citrus compartments. Our findings reveal that application of WT B. subtilis enriched beneficial fungi such as Trichoderma (15.82 %) in leaf endosphere. In contrast, pathogenic fungi Fusarium (47.5 %) and Gibberella (0.47 %) involved in citrus root decline were adundant in the L1-21Δytnp treated root endosphere while Nigrospora (11 %) was predominant in L1-21Δyxel treated leaf endosphere, affirming the role of bacterial quorum sensing (QS) molecules in shaping the fungal community composition. In general, based on the fungal functional prediction, fungal pathogens were highly abundant in mutant-treated plants, particularly in leaf endosphere (L1-21Δytnp: 25 %; L1-21Δyxel: 36.35 %) compared to WT (20.93%). Additionally, some fungal members exhibited strong compartment specificity and both mutants induced distinct mycobiome shifts in rhizosphere soil, leaf, and root endopshere. In conclusion, B. subtilis QQ modifies bacterial QS networks facilitating beneficial fungi to establish, while loss of QQ leads to enrichment of pathogenic fungal groups. Our study provides a direct link of perception and regulation of mycobiome through bacterial-based QS and QQ system, and its association with disease outcomes.

摘要

微生物组是由无数相互作用的微生物群落维持的,其中细菌和真菌是主要组成部分。最近,微生物干预已成为一种流行的方法,用于操纵微生物组以实现可持续目标。引入的生物防治剂是否以及如何驱动真菌微生物群(真菌组),以及种间信号在塑造微生物组结构和功能方面的作用,仍知之甚少。在这里,我们分别和联合使用野生型(WT)枯草芽孢杆菌 L1-21 及其群体感应淬灭(QQ)突变体(L1-21Δytnp 和 L1-21Δyxel),探索其在黄龙病(HLB)感染的柑橘隔室(包括叶片内皮层、根内皮层和根际土壤)中关键真菌组成员的富集模式。WT 和其 QQ 突变体的应用在柑橘隔室中产生了不同的真菌组富集。我们的研究结果表明,WT 枯草芽孢杆菌的应用富集了有益真菌,如在叶片内皮层中丰富的木霉(15.82%)。相比之下,参与柑橘根衰退的病原菌真菌镰刀菌(47.5%)和赤霉(0.47%)在 L1-21Δytnp 处理的根内皮层中大量存在,而 Nigrospora(11%)在 L1-21Δyxel 处理的叶片内皮层中占主导地位,证实了细菌群体感应(QS)分子在塑造真菌群落组成方面的作用。一般来说,根据真菌功能预测,真菌病原体在突变体处理的植物中高度丰富,特别是在叶片内皮层(L1-21Δytnp:25%;L1-21Δyxel:36.35%)与 WT(20.93%)相比。此外,一些真菌成员表现出强烈的隔室特异性,两种突变体都在根际土壤、叶片和根内皮层中诱导了不同的真菌组变化。总之,枯草芽孢杆菌 QQ 改变了细菌 QS 网络,促进了有益真菌的建立,而 QQ 的缺失导致了病原真菌群体的富集。我们的研究提供了通过细菌 QS 和 QQ 系统以及其与疾病结果的感知和调节来直接联系真菌组的证据。

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