UNLABELLED: The intracellular parasite Cardinium influences the bacterial microbiome composition of arthropod hosts; however, the mechanisms involved remain poorly understood. We sought to evaluate the interactions between Cardinium (cTPut) and SOL in Tyrophagus putrescentiae cultures based on relative abundance and gene expression data. First, we assembled the genome of Candidatus Krakonobacterium acarorum (formerly the Soliltalea-like symbiont SOL), a novel lineage of the Bacteroidota symbiont of mites. The assemblage SOL genome (1.2 Mb) contained complete pathways for the biosynthesis of lipoic acids, pantothenate, and menaquinone from futalosine. SOL is considered a facultative inhabitant (with prevalences ranging from 36% to 80% among individuals) of the gut (from 102 to 104 copies/mite) that is not detected in eggs, suggesting an extracellular location in the gut of mites. Second, gene expression was analyzed in SOL-inhabited cultures, including two cultures with cTPut and two cultures without cTPut. Correlation-based evidence for competition between cTPut and SOL was found mainly in the expression of transporter proteins. The presence of cTPut decreased interactions between SOL and the mite host; however, SOL is under greater control by mites in the presence of cTPut than in the absence of cTPut. Mite KEGG gene expression levels in the peroxisome, autophagy, sphingolipid, apoptosis, PI3K-Akt, and lysozyme pathways were more strongly correlated with SOL gene expression in cultures without cTPut than in those with cTPut. In contrast, mite KEGG gene expression levels in the proteasome, NF-κB, TNF, calcium, and Rap1 signaling pathways were more strongly correlated with SOL in the presence of cTPut. The explanation for these results is that cTPut mostly interacts with the mite host, resulting in changes in the host's immunity-related/regulatory pathways, indirectly affecting the symbiont SOL. IMPORTANCE: Here, we describe the novel Bacteroidetes symbiont (SOL) of mites. The analysis of gene expression in meta-transcriptomic samples from cultures with and without the intracellular parasite Cardinium revealed the effect of Cardinium on SOL as a model facultative symbiont of mites. Our findings suggest that there is competition between these two symbionts for nutrients. In addition, Cardinium can influence other bacterial symbionts via mite host immunity-related and regulatory pathways. Tyrophagus putrescentiae is a cosmopolitan pest mite that contaminates the home environment, including stored food and feed, with allergens. The interactions between intracellular bacteria and other members of the microbiome influence host physiology and indirectly affect allergen production.

• Klíčová slova
• Bacteroidetes, Bacteroidota, Cardinium, gene expression, interaction, mite, symbionts,
• MeSH
• Acaridae * mikrobiologie   MeSH
• Bacteroidetes * genetika   fyziologie   klasifikace   MeSH
• fylogeneze MeSH
• genom bakteriální MeSH
• roztoči * mikrobiologie   MeSH
• stanovení celkové genové exprese MeSH
• symbióza * MeSH
• zvířata MeSH
• Check Tag
• zvířata MeSH
• Publikační typ
• časopisecké články MeSH

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.

• Klíčová slova
• Cardinium, Erwiniaceae, Sodalis, Tyrophagus putrescentiae, Wolbachia, allergens, bacterial symbionts, gene expression, stored product mite,
• MeSH
• Acaridae * mikrobiologie   MeSH
• Bacteroidetes * genetika   fyziologie   MeSH
• regulace genové exprese u bakterií * MeSH
• roztoči * mikrobiologie   MeSH
• střevní mikroflóra * MeSH
• symbióza * MeSH
• Wolbachia genetika   fyziologie   MeSH
• zvířata MeSH
• Check Tag
• zvířata MeSH
• Publikační typ
• časopisecké články MeSH