Dataset Information

Daily rhythms and enrichment patterns in the transcriptome of the behavior-manipulating parasite Ophiocordyceps kimflemingiae.

ABSTRACT: Various parasite-host interactions that involve adaptive manipulation of host behavior display time-of-day synchronization of certain events. One example is the manipulated biting behavior observed in Carpenter ants infected with Ophiocordyceps unilateralis sensu lato. We hypothesized that biological clocks play an important role in this and other parasite-host interactions. In order to identify candidate molecular clock components, we used two general strategies: bioinformatics and transcriptional profiling. The bioinformatics approach was used to identify putative homologs of known clock genes. For transcriptional profiling, RNA-Seq was performed on 48 h time courses of Ophiocordyceps kimflemingiae (a recently named species of the O. unilateralis complex), whose genome has recently been sequenced. Fungal blastospores were entrained in liquid media under 24 h light-dark (LD) cycles and were harvested at 4 h intervals either under LD or continuous darkness. Of all O. kimflemingiae genes, 5.3% had rhythmic mRNAs under these conditions (JTK Cycle, ? 0.057 statistical cutoff). Our data further indicates that a significant number of transcription factors have a peaked activity during the light phase (day time). The expression levels of a significant number of secreted enzymes, proteases, toxins and small bioactive compounds peaked during the dark phase or subjective night. These findings support a model whereby this fungal parasite uses its biological clock for phase-specific activity. We further suggest that this may be a general mechanism involved in parasite-host interactions.

SUBMITTER: de Bekker C

PROVIDER: S-EPMC5669440 | biostudies-literature | 2017

REPOSITORIES: biostudies-literature

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Daily rhythms and enrichment patterns in the transcriptome of the behavior-manipulating parasite Ophiocordyceps kimflemingiae.

de Bekker Charissa C Will Ian I Hughes David P DP Brachmann Andreas A Merrow Martha M

PloS one 20171103 11

Various parasite-host interactions that involve adaptive manipulation of host behavior display time-of-day synchronization of certain events. One example is the manipulated biting behavior observed in Carpenter ants infected with Ophiocordyceps unilateralis sensu lato. We hypothesized that biological clocks play an important role in this and other parasite-host interactions. In order to identify candidate molecular clock components, we used two general strategies: bioinformatics and transcriptio ...[more]

PMID: 29099875

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Project description:BackgroundThe consequences of the earth's daily rotation have led to 24-h biological rhythms in most organisms. Even some parasites are known to have daily rhythms, which, when in synchrony with host rhythms, can optimise their fitness. Understanding these rhythms may enable the development of control strategies that take advantage of rhythmic vulnerabilities. Recent work on protozoan parasites has revealed 24-h rhythms in gene expression, drug sensitivity and the presence of an intrinsic circadian clock; however, similar studies on metazoan parasites are lacking. To address this, we investigated if a metazoan parasite has daily molecular oscillations, whether they reveal how these longer-lived organisms can survive host daily cycles over a lifespan of many years and if animal circadian clock genes are present and rhythmic. We addressed these questions using the human blood fluke Schistosoma mansoni that lives in the vasculature for decades and causes the tropical disease schistosomiasis.ResultsUsing round-the-clock transcriptomics of male and female adult worms collected from experimentally infected mice, we discovered that ~ 2% of its genes followed a daily pattern of expression. Rhythmic processes included a stress response during the host's active phase and a 'peak in metabolic activity' during the host's resting phase. Transcriptional profiles in the female reproductive system were mirrored by daily patterns in egg laying (eggs are the main drivers of the host pathology). Genes cycling with the highest amplitudes include predicted drug targets and a vaccine candidate. These 24-h rhythms may be driven by host rhythms and/or generated by a circadian clock; however, orthologs of core clock genes are missing and secondary clock genes show no 24-h rhythmicity.ConclusionsThere are daily rhythms in the transcriptomes of adult S. mansoni, but they appear less pronounced than in other organisms. The rhythms reveal temporally compartmentalised internal processes and host interactions relevant to within-host survival and between-host transmission. Our findings suggest that if these daily rhythms are generated by an intrinsic circadian clock then the oscillatory mechanism must be distinct from that in other animals. We have shown which transcripts oscillate at this temporal scale and this will benefit the development and delivery of treatments against schistosomiasis.

Project description:Background and objectivesCircadian rhythms contribute to treatment efficacy in several non-communicable diseases. However, chronotherapy (administering drugs at a particular time-of-day) against infectious diseases has been overlooked. Yet, the daily rhythms of both hosts and disease-causing agents can impact the efficacy of drug treatment. We use the rodent malaria parasite Plasmodium chabaudi, to test whether the daily rhythms of hosts, parasites and their interactions affect sensitivity to the key antimalarial, artemisinin.MethodologyAsexual malaria parasites develop rhythmically in the host's blood, in a manner timed to coordinate with host daily rhythms. Our experiments coupled or decoupled the timing of parasite and host rhythms, and we administered artemisinin at different times of day to coincide with when parasites were either at an early (ring) or later (trophozoite) developmental stage. We quantified the impacts of parasite developmental stage, and alignment of parasite and host rhythms, on drug sensitivity.ResultsWe find that rings were less sensitive to artemisinin than trophozoites, and this difference was exacerbated when parasite and host rhythms were misaligned, with little direct contribution of host time-of-day on its own. Furthermore, the blood concentration of haem at the point of treatment correlated positively with artemisinin efficacy but only when parasite and host rhythms were aligned.Conclusions and implicationsParasite rhythms influence drug sensitivity in vivo. The hitherto unknown modulation by alignment between parasite and host daily rhythms suggests that disrupting the timing of parasite development could be a novel chronotherapeutic approach.Lay summaryWe reveal that chronotherapy (providing medicines at a particular time-of-day) could improve treatment for malaria infections. Specifically, parasites' developmental stage at the time of treatment and the coordination of timing between parasite and host both affect how well antimalarial drug treatment works.

Project description:BackgroundDaily rhythmicity has been observed for a number of hormonal and behavioral variables in mammals. It can be entrained by several external factors, such as light-dark cycle and scheduled feeding. In dromedary camels, daily rhythmicity has been documented only for melatonin secretion and body temperature. In this study, the daily rhythmicity of behavioral repertoire, cortisol and testosterone levels was investigated in captive male camels.MethodsSix clinically healthy male dromedary camels (Camelus dromedarius) were used. The animals were housed in single boxes for 24 h daily and fed twice a day. Over a period of 48 h, behavioral observations were made and blood samples taken every two hours. The data were analyzed using diurnality index, conisor analysis and PROC mixed procedure.ResultsThe diurnality index for rumination and lying down was close to 0 (respectively, 0.09 and 0.19), while the indices for stereotypy, standing, feeding and walking were close to 1 (respectively, 0.74, 0.84, 0.92 and 0.85). Cosinor analysis revealed daily rhythmicity for all behaviors and for cortisol levels (acrophase at 12:57) but not for testosterone. Rumination and lying down (inactive behaviors) reached a peak during the scotophase, whereas feeding, walking and stereotypy (active behaviors) reached a peak during the photophase around midday. Cortisol level and expression of stereotypies peaked before and after food distribution and were negatively correlated (r = - 0.287, P = 0.005). Testosterone levels and expression of sexual behaviors were stimulated by the visual and olfactory contacts with the females and were positively correlated (r = 0.164, P = 0.040). Testosterone was also negatively correlated with cortisol (r = - 0.297; P = 0.003).DiscussionThese preliminary results provided new knowledge about the daily rhythm of behaviors in camels housed in boxes, suggesting that camels exhibit diurnal behavior pattern in the maintenance conditions outlined in the study. Daily rhythmicity seemed to be entrained not only by the light-dark cycle but also by scheduled feeding. The rise in stereotypy after food distribution could be due to the persistence of feeding motivation and frustration after the ingestion of food. Therefore, feeding practices should be improved to satisfy the foraging and feeding motivation of these camels. Behavioral and hormonal daily patterns in camels should be taken in consideration to adapt the management system, giving the animals more freedom during the light period and a diet richer in fiber, so as to improve reproductive performance, health and welfare.

Dataset Information

Daily rhythms and enrichment patterns in the transcriptome of the behavior-manipulating parasite Ophiocordyceps kimflemingiae.

Publications

Daily rhythms and enrichment patterns in the transcriptome of the behavior-manipulating parasite Ophiocordyceps kimflemingiae.

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