A brain-infecting parasite impacts host metabolism both during exposure and after infection is established

Authors

Lauren E. Nadler, Scripps Institution of Oceanography, Norwegian University of Life Sciences, Nova Southeastern UniversityFollow
Erik Bengston, Scripps Institution of OceanographyFollow
Erika J. Eliason, University of California, Santa BarbaraFollow
Cameron Hassibi, Scripps Institution of OceanographyFollow
Siri H. Helland-Riise, Norwegian University of Life SciencesFollow
Ida B. JohansenFollow
Garfield T. Kwan, Scripps Institution of OceanographyFollow
Martin Tresguerres, Scripps Institution of OceanographyFollow
Andrew V. Turner, Scripps Institution of Oceanography
Kelly L. Weinersmith, Rice UniversityFollow
Øyvind Øverli, Norwegian University of Life SciencesFollow
Ryan F. Hechinger, Scripps Institution of OceanographyFollow

Document Type

Article

Publication Date

10-2-2020

Publication Title

Functional Ecology

Keywords

aerobic scope, citrate synthase, host–parasite relationship, lactate dehydrogenase, Na+/K+-ATPase, standard metabolic rate

ISSN

1365-2435

Volume

2020

Issue/No.

00

First Page

1

Last Page

12

Abstract

1. Metabolic costs associated with parasites should not be limited to established infections. Even during initial exposure to questing and attacking parasites, hosts can enact behavioural and physiological responses that could also incur metabolic costs. However, few studies have measured these costs directly. Hence, little is known about metabolic costs arising from parasite exposure.
2. Furthermore, no one has yet measured whether and how previous infection history modulates metabolic responses to parasite exposure.
3. Here, using the California killifish Fundulus parvipinnis and its brain‐infecting parasite Euhaplorchis californiensis, we quantified how killifish metabolism, behaviour and osmoregulatory phenotype changed upon acute exposure to parasite infectious stages (i.e. cercariae), and with long‐term infection.
4. Exposure to cercariae caused both naïve and long‐term infected killifish to acutely increase their metabolic rate and activity, indicating detection and response to parasite infectious stages. Additionally, these metabolic and behavioural effects were moderately stronger in long‐term infected hosts than naïve killifish, suggesting that hosts may develop learned behavioural responses, nociceptor sensitization and/or acute immune mechanisms to limit new infections.
5. Although established infection altered the metabolic response to parasite exposure, established infection did not alter standard metabolic rate, routine metabolic rate, maximum metabolic rate, aerobic scope or citrate synthase enzyme activity.
6. Unexpectedly, established infection reduced lactate dehydrogenase enzyme activity in killifish brains and relative Na+/K+‐ATPase abundance in gills, suggesting novel mechanisms by which E. californiensis may alter its hosts' behaviour and osmoregulation.
7. Thus, we provide empirical evidence that parasites can disrupt the metabolism of their host both during parasite exposure and after infection is established. This response may be modulated by previous infection history, with probable knock‐on effects for host performance, brain energy metabolism, osmoregulation and ecology.

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Comments

Funding information

Norges Forskningsråd, Grant/Award

Number: 250048/F20

Creative Commons License

This work is licensed under a Creative Commons Attribution 4.0 International License.

NSUWorks Citation

Lauren E. Nadler, Erik Bengston, Erika J. Eliason, Cameron Hassibi, Siri H. Helland-Riise, Ida B. Johansen, Garfield T. Kwan, Martin Tresguerres, Andrew V. Turner, Kelly L. Weinersmith, Øyvind Øverli, and Ryan F. Hechinger. 2020. A brain-infecting parasite impacts host metabolism both during exposure and after infection is established .Functional Ecology , (00) : 1 -12. https://nsuworks.nova.edu/occ_facarticles/1134.

ORCID ID

0000-0001-8225-8344

DOI

10.1111/1365-2435.13695