The findings show that tick vitellogenesis pathways contribute to Rb regulation during reproduction and identify the I. scapularis-Rb system as a useful model for studying host control of obligate endosymbionts.
Abstract
Obligate endosymbionts relying on transovarial transmission must coordinate with host reproduction, yet the regulatory mechanisms remain poorly understood. Here we show that the vitellogenesis pathway of the tick Ixodes scapularis regulates the transcriptional state of its endosymbiont Rickettsia buchneri (Rb), separately from its abundance. In males, Rb DNA remained detectable, but bacterial transcription was strongly reduced across all examined genes, with markedly lower RNA/DNA ratios. In females, Rb was restricted to ovarian tissues (developing oocytes and interstitial cells), with no detection in salivary glands or midgut by TEM, FISH, or PCR. After blood feeding, Rb density within size-matched early-stage oocytes was significantly reduced. We further characterized two gene families mediating vitellogenesis: vitellogenin synthesis genes (Vgs, n = 20) and vitellogenin receptor genes (Vgr, n = 15). Vgs proteins showed conserved domain organization, whereas Vgr paralogs showed greater structural diversification. RNAi silencing of Vgs20 or Vgr12 altered Rb transcriptional profiles in both tick cells and ticks, although changes in bacterial load were not consistent between the two systems. Antibiotic depletion of Rb increased expression of both host genes. Together, these findings show that tick vitellogenesis pathways contribute to Rb regulation during reproduction and identify the I. scapularis-Rb system as a useful model for studying host control of obligate endosymbionts. IMPORTANCE Maternally inherited bacterial symbionts are commonly characterized by bacterial abundance. This study shows that bacterial abundance alone does not necessarily reflect symbiont functional state. In the blacklegged tick, the inherited symbiont Rickettsia buchneri persists in males but exhibits little transcriptional activity. In females, the host reproductive pathway determines whether the symbiont is active: silencing one component of this pathway changed bacterial gene expression without changing bacterial abundance. Hosts therefore regulate not only the abundance of inherited symbionts, but also their functional state. The same bacterial abundance can correspond to very different functional states. Understanding inherited symbioses therefore requires considering bacterial function alongside bacterial abundance.
Findings elucidate the important function of Vgs in ovary development and provide insights into the association between insect Vg genes and the ovarian bacteria, thereby establishing a groundwork for subsequent investigations on the molecular mechanisms underlying their interaction.
Cuikang Xu, Qingxiu Xie, Xiaozhen Li et al.· Journal of Economic Entomolo...· 0 citations
DmaxVgR gene silencing disrupted follicular architecture and reduced vitellogenin uptake by the oocytes, resulting in increased vitellogenin levels in the hemolymph suggest a feedback mechanism regulating YPP production.
F. O. Ramos, Jimena Leyria, M. Nouzová et al.· Insect Biochemistry and Mole...· 0 citations
Rumen flukes, particularly the trematode Calicophoron daubneyi, are emerging parasites of livestock in Europe, yet transcriptomic insights into their environmental and intermediate host stages remain limited. Here, we present a comprehensive transcriptomic analysis of eggs at three distinct developmental stages (freshly excreted, early developmental and eye-spot stages), as well as rediae and cercariae, of C. daubneyi. High-quality RNA-sequencing (RNA-seq) datasets revealed both shared and stage-specific transcriptional profiles with each developmental stage exhibiting its own distinct expression pattern. Subsequent GO-Term enrichment analyses revealed that fully embryonated eggs in eye-spot-stage especially upregulated genes related to cilia assembly, movement and motility, reflecting preparation for miracidial hatching and host-seeking behavior. Rediae showed enhanced transcription of genes involved in diverse metabolic and biosynthetic processes, supporting rapid asexual proliferation within the snail intermediate host. Cercariae exhibited predominant upregulation of genes associated with signal transduction and energy metabolism, indicating the adaptation to its changing environmental conditions. These findings provide the first transcriptomic insights into the biology of C. daubneyi outside the definitive host, reveal molecular mechanisms underlying development, transmission and adaptation to a changing environment and identify stage-specific genes as potential targets for interventions aimed at disrupting the parasites life cycle and controlling rumen flukes in the future.
Leah R. Knöpfle, Raúl O. Cosentino, Markus R. Schmidt et al.· BMC Genomics· 0 citations
The cattle tick Rhipicephalus microplus may rely on an alternative polyamine biosynthesis pathway mediated by arginine decarboxylase activity. This hematophagous ectoparasite is a major constraint to livestock production in tropical and subtropical regions, and its control is increasingly compromised by the rapid emergence of acaricide resistance, highlighting the need for new molecular targets. Previous RNA-seq analyses of ovaries, whole males, and female carcasses identified two sex-enriched transcripts, odc1 and odc2, initially annotated as ornithine decarboxylases (ODCs), enzymes that catalyze the rate-limiting step in polyamine biosynthesis. Polyamines are essential for nucleic acid stabilization, cell growth, stress responses, and gametogenesis. Here, we validated using qPCR that expression of both genes is sexually dimorphic. Phylogenetic analysis across Animalia revealed that R. microplus Odc1 and Odc2 form two divergent tick-specific clades, distinct from canonical ODCs described in mammals and insects. Biochemical characterization of recombinant proteins showed that Odc2 lacked detectable activity under the conditions tested, whereas Odc1 exhibited moderate ornithine decarboxylase activity and robust arginine decarboxylase activity. These results suggests that R. microplus may produce putrescine through an alternative route involving agmatine, thereby bypassing the canonical ornithine decarboxylation pathway. To our knowledge, this represents the first biochemical evidence consistent with arginine decarboxylase activity in an animal enzyme. Together, these findings support the existence of a previously unrecognized branch of polyamine metabolism in ticks and identify Odc1 as a promising candidate target for the development of selective acaricides.
R. Cossío-Bayúgar, E. Miranda-Miranda, Michael F. Dunn et al.· Scientific Reports· 1 citation
Theileria equi is an etiological agent of equine piroplasmosis, a tick-borne disease that significantly affects equine health and the global equine industry. In Brazil, Rhipicephalus microplus is the only tick species with confirmed vector competence for T. equi. However, the immunological mechanisms underlying pathogen-vector interactions remain poorly understood. This study aimed to evaluate the differential expression of key genes involved in major immune signaling pathways in the larval and nymphal stages, as well as in the gut and salivary glands of engorged female ticks, following T. equi infection. Our results showed that in infected ticks, the Toll receptor and its associated transcription factor (Dorsal) were upregulated in the gut and salivary glands. The gene encoding the IMD pathway receptor (PGRP) was upregulated in the infected gut, whereas the transcription factor Relish was upregulated in the salivary glands, suggesting tissue-specific activation and alternative regulation of this pathway. Additionally, genes encoding the antimicrobial peptides Microplusin and Defensin were upregulated in both tissues in response to infection. In contrast, the JAK/STAT pathway was downregulated in the infected gut, which may explain the lack of significant differential expression of the Ixodidin gene in this tissue. In the larval and nymphal stages, the transcriptional response was more restricted, with significant downregulation of PGRP in larvae and JAK in nymphs. These findings expand current knowledge of the R. microplus-T. equi immunological interface and highlight potential molecular targets for the development of novel biotechnological strategies for the control and prevention of equine piroplasmosis.
Carla Alves Rabello, K. Galdino, P. Paulino et al.· Acta Tropica· 0 citations
The results support algae-to-host HGT in P. bursaria and suggest that some transferred genes may contribute to metabolic integration during endosymbiosis.
Lei Yang, De-Yu Wei, Yuan Li et al.· Molecular Phylogenetics and...· 0 citations
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