A Trade-Off Between Antimicrobial Peptide Resistance and Sensitivity to Host Immune Effectors in Staphylococcus aureus In Vivo

IF 3.5 2区生物学 Q1 EVOLUTIONARY BIOLOGY

Evolutionary Applications Pub Date : 2025-02-06 DOI:10.1111/eva.70068

Baydaa El Shazely, Jens Rolff

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Abstract

Antimicrobial peptides (AMPs) are essential immune effectors of multicellular organisms. Bacteria can evolve resistance to AMPs. Surprisingly, when used to challenge the yellow mealworm beetle, Tenebrio molitor, Staphylococcus aureus resistant to an abundant AMP (tenecin 1) of the very same host species did not increase host mortality or bacterial load compared to infections with wild-type S. aureus. A possible explanation is that antimicrobial resistance is costly due to the collaterally increased sensitivity of AMP-resistant strains to other immune effectors. Here, we study the sensitivity of a group of AMP-resistant S. aureus strains (resistant to tenecin 1 or a combination of tenecin 1 + 2) to other immune effectors such as phenoloxidase and other AMPs in vivo. Using RNAi-based knockdown, we investigate S. aureus survival in insect hosts lacking selected immune effectors. We find that all except one AMP-resistant strain displayed collateral sensitivity toward phenoloxidase. Some AMP-resistant strains show sensitivity to components of the yellow mealworm beetle AMP defense cocktail. Our findings are consistent with the idea that resistance to AMPs does not translate into changes in virulence because it is balanced by the collaterally increased sensitivity to other host immune effectors. AMP resistance fails to provide a net survival advantage to S. aureus in a host environment that is dominated by AMPs.

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金黄色葡萄球菌体内抗微生物肽耐药性与对宿主免疫效应物敏感性之间的权衡

抗菌肽（AMPs）是多细胞生物必不可少的免疫效应器。细菌可以进化出对抗菌肽的耐药性。令人惊讶的是，与野生型金黄色葡萄球菌感染相比，金黄色葡萄球菌对相同宿主物种的丰富AMP （tenecin 1）具有抗性，但当用于攻击黄粉虫甲虫（tenbrio molitor）时，并没有增加宿主死亡率或细菌负荷。一种可能的解释是，抗菌素耐药性代价高昂，因为抗amp的菌株对其他免疫效应物的敏感性随之增加。在这里，我们研究了一组抗amp的金黄色葡萄球菌菌株（对tenecin 1或tenecin 1 + 2的组合耐药）对其他免疫效应物（如酚氧化酶和其他amp）的敏感性。利用rnai敲除技术，研究了金黄色葡萄球菌在缺乏特定免疫效应物的昆虫宿主中的存活情况。我们发现除了一种amp抗性菌株外，所有菌株都对酚氧化酶表现出间接敏感性。一些抗AMP的菌株对黄粉虫甲虫AMP防御鸡尾酒的成分敏感。我们的发现与对AMPs的抗性并不转化为毒力变化的观点是一致的，因为它与对其他宿主免疫效应物的附带增加的敏感性相平衡。在AMP占主导地位的宿主环境中，AMP耐药性不能为金黄色葡萄球菌提供净生存优势。

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来源期刊

Evolutionary Applications 生物-进化生物学

CiteScore

8.50

自引率

7.30%

发文量

175

审稿时长

6 months

期刊介绍： Evolutionary Applications is a fully peer reviewed open access journal. It publishes papers that utilize concepts from evolutionary biology to address biological questions of health, social and economic relevance. Papers are expected to employ evolutionary concepts or methods to make contributions to areas such as (but not limited to): medicine, agriculture, forestry, exploitation and management (fisheries and wildlife), aquaculture, conservation biology, environmental sciences (including climate change and invasion biology), microbiology, and toxicology. All taxonomic groups are covered from microbes, fungi, plants and animals. In order to better serve the community, we also now strongly encourage submissions of papers making use of modern molecular and genetic methods (population and functional genomics, transcriptomics, proteomics, epigenetics, quantitative genetics, association and linkage mapping) to address important questions in any of these disciplines and in an applied evolutionary framework. Theoretical, empirical, synthesis or perspective papers are welcome.