An iron-binding protein of entomopathogenic fungus suppresses the proliferation of host symbiotic bacteria.

IF 13.8 1区 生物学 Q1 MICROBIOLOGY Microbiome Pub Date : 2024-10-15 DOI:10.1186/s40168-024-01928-4
Juan Li, Jiujie Li, Lili Cao, Qinghua Chen, Ding Ding, Le Kang
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Abstract

Background: Entomopathogenic fungal infection-induced dysbiosis of host microbiota offers a window into understanding the complex interactions between pathogenic fungi and host symbionts. Such insights are critical for enhancing the efficacy of mycoinsecticides. However, the utilization of these interactions in pest control remains largely unexplored.

Results: Here, we found that infection by the host-specialist fungus Metarhizium acridum alters the composition of the symbiotic microbiota and increases the dominance of some bacterial symbionts in locusts. Meanwhile, M. acridum also effectively limits the overgrowth of the predominant bacteria. Comparative transcriptomic screening revealed that the fungus upregulates the production of MaCFEM1, an iron-binding protein, in the presence of bacteria. This protein sequesters iron, thereby limiting its availability. Functionally, overexpression of MaCFEM1 in the fungus induces iron deprivation, which significantly suppresses bacterial growth. Conversely, MaCFEM1 knockout relieves the restriction on bacterial iron availability, resulting in iron reallocation. Upon ΔMaCFEM1 infection, some host bacterial symbionts proliferate uncontrollably, turning into opportunistic pathogens and significantly accelerating host death.

Conclusions: This study elucidates the critical role of pathogenic fungal-dominated iron allocation in mediating the shift of host microbes from symbiosis to pathogenicity. It also highlights a unique biocontrol strategy that jointly exploits pathogenic fungi and bacterial symbionts to increase host mortality. Video Abstract.

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昆虫病原真菌的一种铁结合蛋白抑制宿主共生细菌的增殖。
背景:昆虫病原真菌感染引起的宿主微生物区系失调为了解病原真菌与宿主共生体之间复杂的相互作用提供了一个窗口。这些见解对于提高杀昆虫剂的功效至关重要。然而,在害虫控制中如何利用这些相互作用在很大程度上仍有待探索:结果:在这里,我们发现寄主专性真菌梭菌的感染改变了蝗虫共生微生物群的组成,并增加了某些细菌共生体的优势。同时,尖孢镰刀菌还能有效限制优势细菌的过度生长。比较转录组筛选发现,在有细菌存在的情况下,真菌会上调铁结合蛋白 MaCFEM1 的产量。这种蛋白能螯合铁,从而限制铁的供应。从功能上讲,真菌过量表达 MaCFEM1 会诱导铁匮乏,从而显著抑制细菌的生长。相反,MaCFEM1 基因敲除则会缓解对细菌铁供应的限制,从而导致铁的重新分配。感染ΔMaCFEM1后,宿主的一些细菌共生体会不受控制地增殖,变成机会性病原体,大大加速宿主的死亡:这项研究阐明了致病真菌主导的铁分配在介导宿主微生物从共生向致病转变过程中的关键作用。结论:这项研究阐明了病原真菌主导的铁分配在介导宿主微生物从共生到致病转变过程中的关键作用,同时还强调了一种独特的生物防治策略,即共同利用病原真菌和细菌共生体来增加宿主死亡率。视频摘要。
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来源期刊
Microbiome
Microbiome MICROBIOLOGY-
CiteScore
21.90
自引率
2.60%
发文量
198
审稿时长
4 weeks
期刊介绍: Microbiome is a journal that focuses on studies of microbiomes in humans, animals, plants, and the environment. It covers both natural and manipulated microbiomes, such as those in agriculture. The journal is interested in research that uses meta-omics approaches or novel bioinformatics tools and emphasizes the community/host interaction and structure-function relationship within the microbiome. Studies that go beyond descriptive omics surveys and include experimental or theoretical approaches will be considered for publication. The journal also encourages research that establishes cause and effect relationships and supports proposed microbiome functions. However, studies of individual microbial isolates/species without exploring their impact on the host or the complex microbiome structures and functions will not be considered for publication. Microbiome is indexed in BIOSIS, Current Contents, DOAJ, Embase, MEDLINE, PubMed, PubMed Central, and Science Citations Index Expanded.
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