Daily rhythms in gene expression of the human parasite Schistosoma mansoni

Abstract Background The 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 developmen...

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Autores principales:	Kate A. Rawlinson, Adam J. Reid, Zhigang Lu, Patrick Driguez, Anna Wawer, Avril Coghlan, Geetha Sankaranarayanan, Sarah K. Buddenborg, Carmen Diaz Soria, Catherine McCarthy, Nancy Holroyd, Mandy Sanders, Karl F. Hoffmann, David Wilcockson, Gabriel Rinaldi, Matthew Berriman
Formato:	article
Lenguaje:	EN
Publicado:	BMC 2021
Materias:	Daily rhythms Transcriptomics RNA-seq Adult Schistosoma mansoni Animal circadian clock genes Biology (General) QH301-705.5
Acceso en línea:	https://doaj.org/article/9c514beb10074835b2b16a2af319d0f5
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spelling	oai:doaj.org-article:9c514beb10074835b2b16a2af319d0f52021-12-05T12:25:55ZDaily rhythms in gene expression of the human parasite Schistosoma mansoni10.1186/s12915-021-01189-91741-7007https://doaj.org/article/9c514beb10074835b2b16a2af319d0f52021-12-01T00:00:00Zhttps://doi.org/10.1186/s12915-021-01189-9https://doaj.org/toc/1741-7007Abstract Background The 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. Results Using 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. Conclusions There 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.Kate A. RawlinsonAdam J. ReidZhigang LuPatrick DriguezAnna WawerAvril CoghlanGeetha SankaranarayananSarah K. BuddenborgCarmen Diaz SoriaCatherine McCarthyNancy HolroydMandy SandersKarl F. HoffmannDavid WilcocksonGabriel RinaldiMatthew BerrimanBMCarticleDaily rhythmsTranscriptomicsRNA-seqAdult Schistosoma mansoniAnimal circadian clock genesBiology (General)QH301-705.5ENBMC Biology, Vol 19, Iss 1, Pp 1-21 (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	Daily rhythms Transcriptomics RNA-seq Adult Schistosoma mansoni Animal circadian clock genes Biology (General) QH301-705.5
spellingShingle	Daily rhythms Transcriptomics RNA-seq Adult Schistosoma mansoni Animal circadian clock genes Biology (General) QH301-705.5 Kate A. Rawlinson Adam J. Reid Zhigang Lu Patrick Driguez Anna Wawer Avril Coghlan Geetha Sankaranarayanan Sarah K. Buddenborg Carmen Diaz Soria Catherine McCarthy Nancy Holroyd Mandy Sanders Karl F. Hoffmann David Wilcockson Gabriel Rinaldi Matthew Berriman Daily rhythms in gene expression of the human parasite Schistosoma mansoni
description	Abstract Background The 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. Results Using 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. Conclusions There 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.
format	article
author	Kate A. Rawlinson Adam J. Reid Zhigang Lu Patrick Driguez Anna Wawer Avril Coghlan Geetha Sankaranarayanan Sarah K. Buddenborg Carmen Diaz Soria Catherine McCarthy Nancy Holroyd Mandy Sanders Karl F. Hoffmann David Wilcockson Gabriel Rinaldi Matthew Berriman
author_facet	Kate A. Rawlinson Adam J. Reid Zhigang Lu Patrick Driguez Anna Wawer Avril Coghlan Geetha Sankaranarayanan Sarah K. Buddenborg Carmen Diaz Soria Catherine McCarthy Nancy Holroyd Mandy Sanders Karl F. Hoffmann David Wilcockson Gabriel Rinaldi Matthew Berriman
author_sort	Kate A. Rawlinson
title	Daily rhythms in gene expression of the human parasite Schistosoma mansoni
title_short	Daily rhythms in gene expression of the human parasite Schistosoma mansoni
title_full	Daily rhythms in gene expression of the human parasite Schistosoma mansoni
title_fullStr	Daily rhythms in gene expression of the human parasite Schistosoma mansoni
title_full_unstemmed	Daily rhythms in gene expression of the human parasite Schistosoma mansoni
title_sort	daily rhythms in gene expression of the human parasite schistosoma mansoni
publisher	BMC
publishDate	2021
url	https://doaj.org/article/9c514beb10074835b2b16a2af319d0f5
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Daily rhythms in gene expression of the human parasite Schistosoma mansoni

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