Timing of host feeding drives rhythms in parasite replication

Handle URI:
http://hdl.handle.net/10754/627216
Title:
Timing of host feeding drives rhythms in parasite replication
Authors:
Prior, Kimberley F. ( 0000-0001-7069-3605 ) ; van der Veen, Daan R. ( 0000-0001-8037-1407 ) ; O’Donnell, Aidan J. ( 0000-0003-3503-094X ) ; Cumnock, Katherine; Schneider, David; Pain, Arnab ( 0000-0002-1755-2819 ) ; Subudhi, Amit; Ramaprasad, Abhinay ( 0000-0001-9372-5526 ) ; Rund, Samuel S. C. ( 0000-0002-1701-7787 ) ; Savill, Nicholas J.; Reece, Sarah E. ( 0000-0001-6716-6732 )
Abstract:
Circadian rhythms enable organisms to synchronise the processes underpinning survival and reproduction to anticipate daily changes in the external environment. Recent work shows that daily (circadian) rhythms also enable parasites to maximise fitness in the context of ecological interactions with their hosts. Because parasite rhythms matter for their fitness, understanding how they are regulated could lead to innovative ways to reduce the severity and spread of diseases. Here, we examine how host circadian rhythms influence rhythms in the asexual replication of malaria parasites. Asexual replication is responsible for the severity of malaria and fuels transmission of the disease, yet, how parasite rhythms are driven remains a mystery. We perturbed feeding rhythms of hosts by 12 hours (i.e. diurnal feeding in nocturnal mice) to desynchronise the host’s peripheral oscillators from the central, light-entrained oscillator in the brain and their rhythmic outputs. We demonstrate that the rhythms of rodent malaria parasites in day-fed hosts become inverted relative to the rhythms of parasites in night-fed hosts. Our results reveal that the host’s peripheral rhythms (associated with the timing of feeding and metabolism), but not rhythms driven by the central, light-entrained circadian oscillator in the brain, determine the timing (phase) of parasite rhythms. Further investigation reveals that parasite rhythms correlate closely with blood glucose rhythms. In addition, we show that parasite rhythms resynchronise to the altered host feeding rhythms when food availability is shifted, which is not mediated through rhythms in the host immune system. Our observations suggest that parasites actively control their developmental rhythms. Finally, counter to expectation, the severity of disease symptoms expressed by hosts was not affected by desynchronisation of their central and peripheral rhythms. Our study at the intersection of disease ecology and chronobiology opens up a new arena for studying host-parasite-vector coevolution and has broad implications for applied bioscience.
KAUST Department:
Biological and Environmental Sciences and Engineering (BESE) Division; Bioscience Program
Citation:
Prior KF, van der Veen DR, O’Donnell AJ, Cumnock K, Schneider D, et al. (2018) Timing of host feeding drives rhythms in parasite replication. PLOS Pathogens 14: e1006900. Available: http://dx.doi.org/10.1371/journal.ppat.1006900.
Publisher:
Public Library of Science (PLoS)
Journal:
PLOS Pathogens
KAUST Grant Number:
BAS/1/1020-01-01
Issue Date:
26-Feb-2018
DOI:
10.1101/229674; 10.1371/journal.ppat.1006900
Type:
Article
ISSN:
1553-7374
Sponsors:
This study was funded by the Human Frontiers Science Program (KFP, AJOD, NJS, SER), grant RPG0046/2013 (www.hfsp.org), the Royal Society (SER), grant UF110155 (https://royalsociety.org) and the Wellcome Trust (KFP, AJOD, SSCR, SER), grant 202769/Z/16/Z (https://wellcome.ac.uk). The project was also supported by a National Institutes of Health Directors Pioneer Award (KC, DS), 5DP1At007753 (https://commonfund.nih.gov/pioneer/description) and a faculty baseline funding by King Abdullah University of Science and Technology (KAUST) (AS, AR, AP), BAS/1/1020-01-01. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Additional Links:
https://www.biorxiv.org/content/early/2017/12/06/229674; http://journals.plos.org/plospathogens/article?id=10.1371/journal.ppat.1006900
Appears in Collections:
Articles; Bioscience Program; Biological and Environmental Sciences and Engineering (BESE) Division

Full metadata record

DC FieldValue Language
dc.contributor.authorPrior, Kimberley F.en
dc.contributor.authorvan der Veen, Daan R.en
dc.contributor.authorO’Donnell, Aidan J.en
dc.contributor.authorCumnock, Katherineen
dc.contributor.authorSchneider, Daviden
dc.contributor.authorPain, Arnaben
dc.contributor.authorSubudhi, Amiten
dc.contributor.authorRamaprasad, Abhinayen
dc.contributor.authorRund, Samuel S. C.en
dc.contributor.authorSavill, Nicholas J.en
dc.contributor.authorReece, Sarah E.en
dc.date.accessioned2018-04-25T12:52:46Z-
dc.date.available2018-02-28T12:53:38Z-
dc.date.available2018-04-25T12:52:46Z-
dc.date.issued2018-02-26en
dc.identifier.citationPrior KF, van der Veen DR, O’Donnell AJ, Cumnock K, Schneider D, et al. (2018) Timing of host feeding drives rhythms in parasite replication. PLOS Pathogens 14: e1006900. Available: http://dx.doi.org/10.1371/journal.ppat.1006900.en
dc.identifier.issn1553-7374en
dc.identifier.doi10.1101/229674-
dc.identifier.doi10.1371/journal.ppat.1006900-
dc.identifier.urihttp://hdl.handle.net/10754/627216-
dc.description.abstractCircadian rhythms enable organisms to synchronise the processes underpinning survival and reproduction to anticipate daily changes in the external environment. Recent work shows that daily (circadian) rhythms also enable parasites to maximise fitness in the context of ecological interactions with their hosts. Because parasite rhythms matter for their fitness, understanding how they are regulated could lead to innovative ways to reduce the severity and spread of diseases. Here, we examine how host circadian rhythms influence rhythms in the asexual replication of malaria parasites. Asexual replication is responsible for the severity of malaria and fuels transmission of the disease, yet, how parasite rhythms are driven remains a mystery. We perturbed feeding rhythms of hosts by 12 hours (i.e. diurnal feeding in nocturnal mice) to desynchronise the host’s peripheral oscillators from the central, light-entrained oscillator in the brain and their rhythmic outputs. We demonstrate that the rhythms of rodent malaria parasites in day-fed hosts become inverted relative to the rhythms of parasites in night-fed hosts. Our results reveal that the host’s peripheral rhythms (associated with the timing of feeding and metabolism), but not rhythms driven by the central, light-entrained circadian oscillator in the brain, determine the timing (phase) of parasite rhythms. Further investigation reveals that parasite rhythms correlate closely with blood glucose rhythms. In addition, we show that parasite rhythms resynchronise to the altered host feeding rhythms when food availability is shifted, which is not mediated through rhythms in the host immune system. Our observations suggest that parasites actively control their developmental rhythms. Finally, counter to expectation, the severity of disease symptoms expressed by hosts was not affected by desynchronisation of their central and peripheral rhythms. Our study at the intersection of disease ecology and chronobiology opens up a new arena for studying host-parasite-vector coevolution and has broad implications for applied bioscience.en
dc.description.sponsorshipThis study was funded by the Human Frontiers Science Program (KFP, AJOD, NJS, SER), grant RPG0046/2013 (www.hfsp.org), the Royal Society (SER), grant UF110155 (https://royalsociety.org) and the Wellcome Trust (KFP, AJOD, SSCR, SER), grant 202769/Z/16/Z (https://wellcome.ac.uk). The project was also supported by a National Institutes of Health Directors Pioneer Award (KC, DS), 5DP1At007753 (https://commonfund.nih.gov/pioneer/description) and a faculty baseline funding by King Abdullah University of Science and Technology (KAUST) (AS, AR, AP), BAS/1/1020-01-01. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.en
dc.language.isoenen
dc.publisherPublic Library of Science (PLoS)en
dc.relation.urlhttps://www.biorxiv.org/content/early/2017/12/06/229674en
dc.relation.urlhttp://journals.plos.org/plospathogens/article?id=10.1371/journal.ppat.1006900-
dc.rightsThis is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.en
dc.rights.urihttp://creativecommons.org/licenses/by/4.0/en
dc.titleTiming of host feeding drives rhythms in parasite replicationen
dc.typeArticleen
dc.contributor.departmentBiological and Environmental Sciences and Engineering (BESE) Divisionen
dc.contributor.departmentBioscience Programen
dc.identifier.journalPLOS Pathogensen
dc.eprint.versionPost-printen
dc.contributor.institutionInstitutes of Evolution, Immunology and Infection Research, University of Edinburgh, Edinburgh, United Kingdomen
dc.contributor.institutionFaculty of Health and Medical Sciences, University of Surrey, Guildford, United Kingdomen
dc.contributor.institutionDepartment of Microbiology and Immunology, Stanford University, Stanford, California, United States of Americaen
dc.contributor.institutionCentre for Immunity, Infection and Evolution, University of Edinburgh, Edinburgh, United Kingdomen
kaust.authorPain, Arnaben
kaust.authorSubudhi, Amiten
kaust.authorRamaprasad, Abhinayen
kaust.grant.numberBAS/1/1020-01-01en

Version History

VersionItem Editor Date Summary
2 10754/627216wangh0e2018-04-25 08:19:12.2Published with DOI
1 10754/627216.1grenzdm2018-02-28 12:53:38.0
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