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Timing of host feeding drives rhythms in parasite replication

Prior, Kimberley F., Van Der Veen, Daniel, O'Donnell, Aidan J., Cumnock, Katherine, Schneider, David, Pain, Arnab, Subudhi, Amit, Ramaprasad, Abhinay, Rund, Samuel S.C., Savill, Nicholas J. and Reece, Sarah E. (2018) Timing of host feeding drives rhythms in parasite replication PLOS Pathogens, 14 (2), e1006900.

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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 hosts' 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 hosts' 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.

Item Type: Article
Divisions : Faculty of Health and Medical Sciences > School of Biosciences and Medicine
Authors :
NameEmailORCID
Prior, Kimberley F.
Van Der Veen, DanielD.Vanderveen@surrey.ac.uk
O'Donnell, Aidan J.
Cumnock, Katherine
Schneider, David
Pain, Arnab
Subudhi, Amit
Ramaprasad, Abhinay
Rund, Samuel S.C.
Savill, Nicholas J.
Reece, Sarah E.
Date : 26 February 2018
Identification Number : 10.1371/journal.ppat.1006900
Copyright Disclaimer : © 2018 Prior et al. This 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.
Additional Information : Data Availability: All relevant data files are available from the Dryad Digital Repository database under the doi: 10.5061/dryad.jt224.
Depositing User : Clive Harris
Date Deposited : 22 Feb 2018 15:47
Last Modified : 13 Mar 2018 15:46
URI: http://epubs.surrey.ac.uk/id/eprint/845883

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