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

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. This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

Rapid blood acid–base regulation by European sea bass (Dicentrarchus labrax) in response to sudden exposure to high environmental CO2

“…NKA was immunodetected using α5, a mouse monoclonal antibody against the α-subunit of chicken NKA (a5, Developmental Studies Hybridoma Bank, Iowa City, IA, USA; Lebovitz et al, 1989 ). This antibody universally recognises NKA in teleost fishes including yellowfin tuna ( Thunnus albacares ; Kwan et al, 2019 ), Pacific chub mackerel ( Scomber japonicus ; Kwan et al, 2020 ) and California killifish ( Fundulus parvipinnis ; Nadler et al, 2021 ). Rabbit anti-NHE3 polyclonal antibodies were generously donated by Dr Junya Hiroi (St Marianna University School of Medicine, Kawaski, Japan); they target two epitope regions within rainbow trout ( Oncorhynchus mykiss ) NHE3b (GDEDFEFSEGDSASG and PSQRAQLRLPWTPSNLRRLAPL), and recognise NHE3 of multiple teleost species including European sea bass ( D. labrax ; Blondeau-Bidet et al, 2019 ).…”

Rapid blood acid-base regulation by European sea bass (Dicentrarchus labrax) in response to sudden exposure to high environmental CO2

“…It is The copyright holder for this preprint this version posted April 23, 2021. ; https://doi.org/10. 1101/2021 In comparison, sea bass exposed to hypercapnia in low alkalinity sea water (TA ~200 µM) showed no ability to accumulate HCO3 -, to compensate for respiratory acidosis, and did not experience a decrease in plasma [Cl -]. At face value, these results may support potential direct uptake of HCO3from seawater in exchange for blood Clthrough HCO3 -/Clexchange across the gills (Esbaugh et al, 2012;Perry and Gilmour, 2006;Tovey and Brauner, 2018).…”

“…It is The copyright holder for this preprint this version posted April 23, 2021. ; https://doi.org/10.1101/2021.04.22.441026 doi: bioRxiv preprint NKA was immunodetected using α5, a mouse monoclonal antibody against the α-subunit of chicken NKA ( a5, Developmental Studies Hybridoma Bank, Iowa City, IA, USA; Lebovitz et al, 1989). This antibody universally recognizes NKA in teleost fishes including yellowfin tuna (Thunnus albacares; Kwan et al, 2019), Pacific chub mackerel (Scomber japonicus; Kwan et al, 2020), and California killifish (Fundulus parvipinnis; Nadler et al, 2021). Rabbit anti-NHE3 polyclonal antibodies were generously donated by Dr Junya Hiroi (St. Marianna University School of Medicine, Kawaski, Japan); they target two epitope regions within rainbow trout (Oncorhynchus mykiss) NHE3b (GDEDFEFSEGDSASG and PSQRAQLRLPWTPSNLRRLAPL), and recognize NHE3 of multiple teleost species including European sea bass (D. labrax;Blondeau-Bidet et al, 2019).…”

“…). This antibody universally recognizes NKA in teleost fishes including yellowfin tuna (Thunnus albacares;Kwan et al, 2019), Pacific chub mackerel (Scomber japonicus;Kwan et al, 2020), and California killifish (Fundulus parvipinnis;Nadler et al, 2021). Rabbit anti-NHE3 polyclonal antibodies were generously donated by Dr Junya Hiroi (St. Marianna University…”

Risk-Induced Trait Responses and Non-consumptive Effects in Plants and Animals in Response to Their Invertebrate Herbivore and Parasite Natural Enemies

“…For instance, the simple presence of parasites in the vicinity has been reported to alter metabolic activity in potential hosts. Drosophila exposed to parasite mites separated by a screen (i.e., no contact possible) increased their metabolic rate (Luong et al, 2017), and this was also seen in fish exposed to motile trematode infectious stages (Nadler et al, 2021). Conversely, larval amphibians with non-contact exposure to trematodes did not exhibit changes in hormones associated with a stress response (Marino et al, 2014).…”