A novel Erwiniaceae gut symbiont modulates gene expression of the intracellular bacterium Cardinium in the stored product mite Tyrophagus putrescentiae.

IF 3.7 2区 生物学 Q2 MICROBIOLOGY
mSphere Pub Date : 2025-03-24 DOI:10.1128/msphere.00879-24
Jan Hubert, Eliza Glowska-Patyniak, Scot E Dowd, Pavel B Klimov
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Abstract

We examined host and bacterial gene expression profiles in the stored product mite Tyrophagus putrescentiae co-infected with Wolbachia (wTPut) and Cardinium (cTPut) while varying the presence of the Erwiniaceae symbiont (SLS). SLS, a novel symbiont in the family Erwiniaceae, with a genome size of 1.7 Mb, is found in 16% of mite species in infected cultures. In addition, SLS was detected in mite feces but not in their eggs. Although Wolbachia expression remained unchanged, the presence or absence of SLS significantly affected Cardinium expression. It indicated that the effect of Wolbachia on SLS was neutral. In SLS-positive samples, Cardinium exhibited 29 upregulated and 48 downregulated genes compared to SLS-negative samples. Furthermore, Cardinium gene expression strongly correlated with mite KEGG gene expression in SLS-positive samples. Positive Spearman's correlations between Cardinium gene expression and mite KEGG immune and regulatory pathways were doubled in SLS-positive compared to SLS-negative samples. The diversity of expressed genes in the mite host decreased in the presence of SLS. Cardinium had more interacting genes to mite host in SLS-positive samples than without SLS. Transposases are the most affected Cardinium genes, showing upregulation in the presence of SLS. Correlation analyses revealed interactions between Cardinium and SLS via mite immune and regulatory pathways, including lysosome, ubiquitin-mediated proteolysis, PIK3_Akt, and cGMP-PKG. The results showed that Cardinium indirectly affects the gut symbionts of mites.IMPORTANCEThis study introduces a new model to analyze interactions between intracellular bacterial symbionts, gut bacterial symbionts, and their mite hosts. Using gene expression correlations, we investigated how the intracellular Cardinium responds to the novel Erwiniaceae gut symbiont in the mold mite Tyrophagus putrescentiae. The data showed that both mite and Cardinium gene expression are different in the samples with and without Erwiniaceae symbionts. In the presence of Erwiniaceae symbionts, Cardinium increased the interaction with the mite host in terms of changes in gene expression. The mite immune and regulatory pathway gene expression is differently correlated to Cardinium genes in relation to Erwiniaceae symbionts. As a well-known producer of allergens, T. putrescentiae physiology and thus its allergen production are influenced by both symbionts, potentially affecting the release of allergens into human environments.

一种新的欧文科肠道共生菌可调节贮藏产品螨Tyrophagus putrescentiae体内Cardinium细胞内细菌的基因表达。
我们检测了同时感染沃尔巴克氏菌(wTPut)和红雀菌(cTPut)的储物螨(Tyrophagus purescentiae)中宿主和细菌的基因表达谱,同时改变了Erwiniaceae共生体(SLS)的存在。SLS是Erwiniaceae家族的一种新型共生体,基因组大小为1.7 Mb,在感染培养物中16%的螨种中发现。此外,在螨粪中检测到SLS,而在螨卵中未检测到SLS。虽然沃尔巴克氏体的表达保持不变,但SLS的存在或不存在显著影响了Cardinium的表达。这表明沃尔巴克氏体对SLS的影响是中性的。在sls阳性样品中,与sls阴性样品相比,红雀表现出29个上调基因和48个下调基因。此外,在sls阳性样品中,Cardinium基因表达与螨KEGG基因表达密切相关。与sls阴性样品相比,sls阳性样品中Cardinium基因表达与螨KEGG免疫和调控途径的Spearman正相关增加了一倍。SLS的存在降低了螨寄主表达基因的多样性。与不含SLS的红雀相比,SLS阳性的红雀与宿主的互作基因较多。转座酶是受影响最大的红雀基因,在SLS的存在下表现出上调。相关分析显示,Cardinium与SLS之间通过溶酶体、泛素介导的蛋白水解、PIK3_Akt和cGMP-PKG等螨免疫和调控途径相互作用。结果表明,红雀胺对螨类肠道共生体有间接影响。重要意义本研究引入了一种新的模型来分析细胞内细菌共生体、肠道细菌共生体及其螨宿主之间的相互作用。利用基因表达相关性,我们研究了腐Tyrophagus purescentiae霉菌螨中细胞内的cardinum对新的Erwiniaceae肠道共生体的反应。结果表明,在有和无Erwiniaceae共生体的样品中,螨和cardinum基因表达量不同。在Erwiniaceae共生体存在的情况下,从基因表达的变化来看,cardinum增加了与螨宿主的相互作用。螨免疫和调控通路基因表达与Erwiniaceae共生体的Cardinium基因有不同的相关性。作为一种众所周知的过敏原制造者,腐烂t菌的生理机能及其过敏原的产生受到这两种共生体的影响,可能会影响过敏原释放到人类环境中。
本文章由计算机程序翻译,如有差异,请以英文原文为准。
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来源期刊
mSphere
mSphere Immunology and Microbiology-Microbiology
CiteScore
8.50
自引率
2.10%
发文量
192
审稿时长
11 weeks
期刊介绍: mSphere™ is a multi-disciplinary open-access journal that will focus on rapid publication of fundamental contributions to our understanding of microbiology. Its scope will reflect the immense range of fields within the microbial sciences, creating new opportunities for researchers to share findings that are transforming our understanding of human health and disease, ecosystems, neuroscience, agriculture, energy production, climate change, evolution, biogeochemical cycling, and food and drug production. Submissions will be encouraged of all high-quality work that makes fundamental contributions to our understanding of microbiology. mSphere™ will provide streamlined decisions, while carrying on ASM''s tradition for rigorous peer review.
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