The University of Southampton
University of Southampton Institutional Repository

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

A brain‐infecting parasite impacts host metabolism both during exposure and after infection is established
A brain‐infecting parasite impacts host metabolism both during exposure and after infection is established
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.
Furthermore, no one has yet measured whether and how previous infection history modulates metabolic responses to parasite exposure.
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.
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.
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.
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.
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.
0269-8463
Nadler, Lauren E.
1d1f8e6a-e951-41f5-888c-cfcb4b4b19dc
Bengston, Erik
96d3bf34-949f-48f8-80ce-9b0d1d6fc8bc
Eliason, Erika J.
7e8d8789-3bee-4c9c-9909-c0447584989b
Hassibi, Cameron
4dd6922c-05a4-4401-b35a-9dad40125146
Helland‐Riise, Siri H.
47ed8efb-184a-411b-ac2e-638db33ab555
Johansen, Ida B.
f4d4c1af-1119-4df2-b3ff-a47a9637917b
Kwan, Garfield T.
6461488f-7e4f-4dcb-83d6-c19b149e149d
Tresguerres, Martin
36bc0bb4-5c93-4250-b3ec-61be4e7e0b5f
Turner, Andrew V.
bd45d4dc-12a8-4ae0-bae3-3d0770458b6b
Weinersmith, Kelly L.
c51f6356-2d1c-41be-880a-efdab1468df4
Øverli, Øyvind
d14da174-a655-4fe9-bc44-7216b9c774e3
Hechinger, Ryan F.
c9509090-149f-4ba2-bc9d-6279dada5d3f
Barribeau, Seth
f877a501-5bb6-4704-9de7-28b7a3cf8361
Nadler, Lauren E.
1d1f8e6a-e951-41f5-888c-cfcb4b4b19dc
Bengston, Erik
96d3bf34-949f-48f8-80ce-9b0d1d6fc8bc
Eliason, Erika J.
7e8d8789-3bee-4c9c-9909-c0447584989b
Hassibi, Cameron
4dd6922c-05a4-4401-b35a-9dad40125146
Helland‐Riise, Siri H.
47ed8efb-184a-411b-ac2e-638db33ab555
Johansen, Ida B.
f4d4c1af-1119-4df2-b3ff-a47a9637917b
Kwan, Garfield T.
6461488f-7e4f-4dcb-83d6-c19b149e149d
Tresguerres, Martin
36bc0bb4-5c93-4250-b3ec-61be4e7e0b5f
Turner, Andrew V.
bd45d4dc-12a8-4ae0-bae3-3d0770458b6b
Weinersmith, Kelly L.
c51f6356-2d1c-41be-880a-efdab1468df4
Øverli, Øyvind
d14da174-a655-4fe9-bc44-7216b9c774e3
Hechinger, Ryan F.
c9509090-149f-4ba2-bc9d-6279dada5d3f
Barribeau, Seth
f877a501-5bb6-4704-9de7-28b7a3cf8361

Nadler, Lauren E., Bengston, Erik, Eliason, Erika J., Hassibi, Cameron, Helland‐Riise, Siri H., Johansen, Ida B., Kwan, Garfield T., Tresguerres, Martin, Turner, Andrew V., Weinersmith, Kelly L., Øverli, Øyvind and Hechinger, Ryan F. , Barribeau, Seth (ed.) (2021) A brain‐infecting parasite impacts host metabolism both during exposure and after infection is established. Functional Ecology. (doi:10.1111/1365-2435.13695).

Record type: Article

Abstract

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.
Furthermore, no one has yet measured whether and how previous infection history modulates metabolic responses to parasite exposure.
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.
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.
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.
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.
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.

Text
Functional Ecology - 2020 - Nadler - A brain‐infecting parasite impacts host metabolism both during exposure and after - Version of Record
Available under License Creative Commons Attribution.
Download (989kB)

More information

e-pub ahead of print date: 8 October 2020
Published date: 25 January 2021

Identifiers

Local EPrints ID: 471672
URI: http://eprints.soton.ac.uk/id/eprint/471672
ISSN: 0269-8463
PURE UUID: b04361ab-764b-4123-b51f-f83585ee0a62
ORCID for Lauren E. Nadler: ORCID iD orcid.org/0000-0001-8225-8344

Catalogue record

Date deposited: 16 Nov 2022 17:37
Last modified: 17 Mar 2024 04:16

Export record

Altmetrics

Contributors

Author: Lauren E. Nadler ORCID iD
Author: Erik Bengston
Author: Erika J. Eliason
Author: Cameron Hassibi
Author: Siri H. Helland‐Riise
Author: Ida B. Johansen
Author: Garfield T. Kwan
Author: Martin Tresguerres
Author: Andrew V. Turner
Author: Kelly L. Weinersmith
Author: Øyvind Øverli
Author: Ryan F. Hechinger
Editor: Seth Barribeau

Download statistics

Downloads from ePrints over the past year. Other digital versions may also be available to download e.g. from the publisher's website.

View more statistics

Atom RSS 1.0 RSS 2.0

Contact ePrints Soton: eprints@soton.ac.uk

ePrints Soton supports OAI 2.0 with a base URL of http://eprints.soton.ac.uk/cgi/oai2

This repository has been built using EPrints software, developed at the University of Southampton, but available to everyone to use.

We use cookies to ensure that we give you the best experience on our website. If you continue without changing your settings, we will assume that you are happy to receive cookies on the University of Southampton website.

×