Osmolality as a novel mechanism explaining diet effects on the outcome of infection with a blood parasite

Kenneth Wilson*, Robert Holdbrook, Catherine E. Reavey, Joanna L. Randall, Yamini Tummala, Fleur Ponton, Stephen J. Simpson, Judith A. Smith, Sheena C. Cotter

*Corresponding author for this work

Research output: Contribution to journalArticle

Abstract

Recent research has suggested that the outcome of host-parasite interactions is dependent on the diet of the host, but most previous studies have focused on "top-down" mechanisms, i.e., how the host's diet improves the host immune response to drive down the parasite population and improve host fitness. In contrast, the direct impacts of host nutrition on parasite fitness and the mechanisms underpinning these effects are relatively unexplored. Here, using a model host-pathogen system (Spodoptera littoralis caterpillars and Xenorhabdus nematophila, an extracellular bacterial blood parasite), we explore the effects of host dietary macronutrient balance on pathogen growth rates both in vivo and in vitro, allowing us to compare pathogen growth rates both in the presence and absence of the host immune response. In vivo, high dietary protein resulted in lower rates of bacterial establishment, slower bacterial growth, higher host survival, and slower speed of host death; in contrast, the energy content and amount of carbohydrate in the diet explained little variation in any measure of pathogen or host fitness. In vitro, we show that these effects are largely driven by the impact of host dietary protein on host hemolymph (blood) osmolality (i.e., its concentration of solutes), with bacterial growth being slower in protein-rich, high-osmolality hemolymphs, highlighting a novel "bottom-up" mechanism by which host diet can impact both pathogen and host fitness.

Original languageEnglish
Pages (from-to)2459-2467
Number of pages12
JournalCurrent Biology
Volume30
Issue number13
Early online date19 May 2020
DOIs
Publication statusPublished - 6 Jul 2020

Bibliographical note

Copyright the Author(s) 2020. Version archived for private and non-commercial use with the permission of the author/s and according to publisher conditions. For further rights please contact the publisher.

Keywords

  • bacteria
  • blood parasite
  • geometric framework
  • macronutrients
  • osmolality
  • osmotic stress
  • pathogen
  • resistance
  • Spodoptera
  • Xenorhabdus

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  • Cite this

    Wilson, K., Holdbrook, R., Reavey, C. E., Randall, J. L., Tummala, Y., Ponton, F., ... Cotter, S. C. (2020). Osmolality as a novel mechanism explaining diet effects on the outcome of infection with a blood parasite. Current Biology, 30(13), 2459-2467. https://doi.org/10.1016/j.cub.2020.04.058