AuthorsPrior, Kimberley F.
van der Veen, Daan R.
O’Donnell, Aidan J.
Rund, Samuel S. C.
Savill, Nicholas J.
Reece, Sarah E.
KAUST DepartmentBiological and Environmental Sciences and Engineering (BESE) Division
KAUST Grant NumberBAS/1/1020-01-01
MetadataShow full item record
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.
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.
SponsorsThis 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.
PublisherPublic Library of Science (PLoS)
Except where otherwise noted, this item's license is described as 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.