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
{"title":"A novel <i>Erwiniaceae</i> gut symbiont modulates gene expression of the intracellular bacterium <i>Cardinium</i> in the stored product mite <i>Tyrophagus putrescentiae</i>.","authors":"Jan Hubert, Eliza Glowska-Patyniak, Scot E Dowd, Pavel B Klimov","doi":"10.1128/msphere.00879-24","DOIUrl":null,"url":null,"abstract":"<p><p>We examined host and bacterial gene expression profiles in the stored product mite <i>Tyrophagus putrescentiae</i> co-infected with <i>Wolbachia</i> (wTPut) and <i>Cardinium</i> (cTPut) while varying the presence of the <i>Erwiniaceae</i> symbiont (SLS). SLS, a novel symbiont in the family <i>Erwiniaceae</i>, 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 <i>Wolbachia</i> expression remained unchanged, the presence or absence of SLS significantly affected <i>Cardinium</i> expression. It indicated that the effect of <i>Wolbachia</i> on SLS was neutral. In SLS-positive samples, <i>Cardinium</i> exhibited 29 upregulated and 48 downregulated genes compared to SLS-negative samples. Furthermore, <i>Cardinium</i> gene expression strongly correlated with mite KEGG gene expression in SLS-positive samples. Positive Spearman's correlations between <i>Cardinium</i> 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. <i>Cardinium</i> had more interacting genes to mite host in SLS-positive samples than without SLS. Transposases are the most affected <i>Cardinium</i> genes, showing upregulation in the presence of SLS. Correlation analyses revealed interactions between <i>Cardinium</i> and SLS via mite immune and regulatory pathways, including lysosome, ubiquitin-mediated proteolysis, PIK3_Akt, and cGMP-PKG. The results showed that <i>Cardinium</i> 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 <i>Cardinium</i> responds to the novel <i>Erwiniaceae</i> gut symbiont in the mold mite <i>Tyrophagus putrescentiae</i>. The data showed that both mite and <i>Cardinium</i> gene expression are different in the samples with and without <i>Erwiniaceae</i> symbionts. In the presence of <i>Erwiniaceae</i> symbionts, <i>Cardinium</i> 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 <i>Cardinium</i> genes in relation to <i>Erwiniaceae</i> symbionts. As a well-known producer of allergens, <i>T. putrescentiae</i> physiology and thus its allergen production are influenced by both symbionts, potentially affecting the release of allergens into human environments.</p>","PeriodicalId":19052,"journal":{"name":"mSphere","volume":" ","pages":"e0087924"},"PeriodicalIF":3.7000,"publicationDate":"2025-03-24","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"mSphere","FirstCategoryId":"99","ListUrlMain":"https://doi.org/10.1128/msphere.00879-24","RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q2","JCRName":"MICROBIOLOGY","Score":null,"Total":0}
引用次数: 0

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。
本文章由计算机程序翻译,如有差异,请以英文原文为准。
求助全文
约1分钟内获得全文 求助全文
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.
×
引用
GB/T 7714-2015
复制
MLA
复制
APA
复制
导出至
BibTeX EndNote RefMan NoteFirst NoteExpress
×
提示
您的信息不完整,为了账户安全,请先补充。
现在去补充
×
提示
您因"违规操作"
具体请查看互助需知
我知道了
×
提示
确定
请完成安全验证×
copy
已复制链接
快去分享给好友吧!
我知道了
右上角分享
点击右上角分享
0
联系我们:info@booksci.cn Book学术提供免费学术资源搜索服务,方便国内外学者检索中英文文献。致力于提供最便捷和优质的服务体验。 Copyright © 2023 布克学术 All rights reserved.
京ICP备2023020795号-1
ghs 京公网安备 11010802042870号
Book学术文献互助
Book学术文献互助群
群 号:481959085
Book学术官方微信