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\u27 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. A free Plain Language Summary can be found within the Supporting Information of this article

Activity of Energy Metabolic Enzymes in Different Coral Species and Populations Provides Evidence for Local Adaptation

Anthropogenic alterations to the Earth system threaten the persistence of coral reef ecosystems, yet pervasive knowledge gaps in basic coral biology prevent accurate measures of coral health prior to mortality. The goal of this thesis is to characterize the metabolic signatures of spatially distinct coral populations adapted to the light regimes of their microenvironments using pathway-specific enzymatic assays. Shallow (3 meters) and deep (5-8 meters) Acropora cervicornis and Porites astreoides populations were sampled at two distinct reef sites: Punta Caracol—a turbid lagoon habitat with large influxes of terrestrial sediments—and Eric Reef—a comparatively pristine open-ocean habitat characterized by greater water column clarity. Coral tissues collected from Bocas del Toro, Panama were homogenized and prepared for analysis at Scripps Institution of Oceanography (San Diego). Malate dehydrogenase (MDH), lactate dehydrogenase (LDH), strombine dehydrogenase (SDH), alanopine dehydrogenase (ADH), and citrate synthase (CS) enzymatic assays were employed to represent maximum fermentative and aerobic metabolic capacities by measuring changes in peak absorbance readings via spectrophotometry. Maximum changes in absorbance were standardized against actual protein concentrations in a novel methodology developed for this thesis. Calculated maximum enzymatic activities indicate that the energy metabolic pathways of A. cervicornis and P. astreoides are tuned to local environmental conditions that, generally, favor fermentation in Punta Caracol as suggested by the higher activities of the various opine dehydrogenases

Activity of Energy Metabolic Enzymes in Different Coral Species and Populations Provides Evidence for Local Adaptation

Anthropogenic alterations to the Earth system threaten the persistence of coral reef ecosystems, yet pervasive knowledge gaps in basic coral biology prevent accurate measures of coral health prior to mortality. The goal of this thesis is to characterize the metabolic signatures of spatially distinct coral populations adapted to the light regimes of their microenvironments using pathway-specific enzymatic assays. Shallow (3 meters) and deep (5-8 meters) Acropora cervicornis and Porites astreoides populations were sampled at two distinct reef sites: Punta Caracol—a turbid lagoon habitat with large influxes of terrestrial sediments—and Eric Reef—a comparatively pristine open-ocean habitat characterized by greater water column clarity. Coral tissues collected from Bocas del Toro, Panama were homogenized and prepared for analysis at Scripps Institution of Oceanography (San Diego). Malate dehydrogenase (MDH), lactate dehydrogenase (LDH), strombine dehydrogenase (SDH), alanopine dehydrogenase (ADH), and citrate synthase (CS) enzymatic assays were employed to represent maximum fermentative and aerobic metabolic capacities by measuring changes in peak absorbance readings via spectrophotometry. Maximum changes in absorbance were standardized against actual protein concentrations in a novel methodology developed for this thesis. Calculated maximum enzymatic activities indicate that the energy metabolic pathways of A. cervicornis and P. astreoides are tuned to local environmental conditions that, generally, favor fermentation in Punta Caracol as suggested by the higher activities of the various opine dehydrogenases

How a Brain-Infecting Parasite Alters Energy Metabolism in a Shoaling Fish: Implications for Conditioned Fear Responses and Mechanisms of Behaviour Modification

Parasites are increasingly being recognised as important players affecting individuals, populations, communities, and even ecosystems. Some parasites change their host’s behaviour to aid transmission to the next host in their life cycle. Parasite-induced behaviour modification may both drive and be driven by changes in host energy metabolism. Here, we examined the gregarious estuarine fish species, the California killifish (Fundulus parvipinnis) and its brain-infecting, behaviour-manipulating trematode parasite (Euhaplorchis californiensis). Killifish were reared in shoals from hatching in either a control (uninfected) or twice-weekly infection (infected) treatment for 12 months. Standard metabolic rate (SMR), maximum metabolic rate (MMR), and acute metabolic response to infectious propagules (MRacute) were then measured using respirometry chambers that allowed these social fish to smell and see their shoal-mates to prevent isolation stress. Brain, gill, and white muscle samples were extracted to assess the way infection influences citrate synthase (CS) and lactate dehydrogenase (LDH) enzymatic activities as indicators of aerobic and anaerobic metabolism, respectively. While SMR and MMR were unaffected by infection status, both uninfected and infected fish exhibited spikes in MRacute. Intriguingly, infected fish mounted a stronger response to exposure than naïve (control) hosts, implying a learned ‘fear’ response to parasite exposure. Measures of enzyme activity suggested that only the brain (the site of the infection) was impacted by the parasites, with infected individuals exhibiting lower LDH activity than uninfected fish. Given the importance of lactate in brain function, these results could suggest a mechanism for parasiteinduced behavioural modification

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