Immune-Challenged Fish Up-Regulate Their Metabolic Scope to Support Locomotion

Abstract

Energy-based trade-offs occur when investment in one fitness-related trait diverts energy away from other traits. The extent to which such trade-offs are shaped by limits on the rate of conversion of energy ingested in food (e.g. carbohydrates) into chemical energy (ATP) by oxidative metabolism rather than by the amount of food ingested in the first place is, however, unclear. Here we tested whether the ATP required for mounting an immune response will lead to a trade-off with ATP available for physical activity in mosquitofish (Gambusia holbrooki). To this end, we challenged fish either with lipopolysaccharide (LPS) from E. coli or with Sheep Red Blood Cells (SRBC), and measured oxygen consumption at rest and during swimming at maximum speed 24h, 48h and 7 days post-challenge in order to estimate metabolic rates. Relative to saline-injected controls, only LPS-injected fish showed a significantly greater resting metabolic rate two days post-challenge and significantly higher maximal metabolic rates two and seven days post-challenge. This resulted in a significantly greater metabolic scope two days post-challenge, with LPS-fish transiently overcompensating by increasing maximal ATP production more than would be required for swimming in the absence of an immune challenge. LPS-challenged fish therefore increased their production of ATP to compensate physiologically for the energetic requirements of immune functioning. This response would avoid ATP shortages and allow fish to engage in an aerobically-challenging activity (swimming) even when simultaneously mounting an immune response. Nevertheless, relative to controls, both LPS- and SRBC-fish displayed reduced body mass gain one week post-injection, and LPS-fish actually lost mass. The concomitant increase in metabolic scope and reduced body mass gain of LPS-challenged fish indicates that immune-associated trade-offs are not likely to be shaped by limited oxidative metabolic capacities, but may instead result from limitations in the acquisition, assimilation or efficient use of resources.

LPS Modulates the Expression of Iron-Related Immune Genes in Two Antarctic Notothenoids

“…It is therefore also possible that an effect in Fe 2+ plasma concentrations may have been missed in our time-frame and dosage, which followed previous studies on temperate fish (Nayak et al, 2011;Guzman-Villanueva et al, 2014;Seppola et al, 2015;Chen et al, 2016) but may less adequate in these Antarctic species. In the present study fish were injected twice, at 0 and 48 h, and sampled at 120 h after the last injection, a design chosen taken in consideration that low temperature habitats may contribute to a slower innate immune system response, as it has been described in cold-water fish when compared to temperate fish (Tort et al, 2003;MacKenzie et al, 2008;Magnoni et al, 2015;Bonneaud et al, 2016;Chen et al, 2016;Abram et al, 2017;Martínez et al, 2017a). The overall gene expression response, albeit not as vigorous as in other vertebrates (Collins, 2008;Johnson and Wessling-Resnick, 2012;Bethke et al, 2016), also suggests that an iron related immune response is active, much alike what it was seen in the sub-Antarctic Notothenioid Eleginops maclovinus (Martínez et al, 2017a), the Senegalese sole, Solea senegalensis (Prieto-Álamo et al, 2009) or the roughskin sculpin, Trachidermus fasciatus (Liu et al, 2012), among other fish species.…”

Effects of MP Polyethylene Microparticles on Microbiome and Inflammatory Response of Larval Zebrafish

“…In order to assess the effect of MP ingestion at the whole organism level, we monitored larval oxygen consumption in a closed respirometry system. Indeed, changes in oxygen consumption could provide an indication of changes in the metabolic status of the animal, including changes in immunological activity and physiological stress [ 70 , 71 ]. Overall, larval oxygen consumption rates were in line with previous studies, with an evident increase in oxygen consumption as the larvae ages [ 48 ].…”

Dose‐ and time‐dependent effects of an immune challenge on fish across biological levels

“…Several consequences are expected, such as a depletion of energy reserves in the liver and muscle (Wang et al, 2012), with potentially detrimental effects on body mass and whole‐body condition (Bonneaud et al, 2003). For instance, immune challenges can deplete liver glycogen in coho salmon ( Oncorhynchus kisutch ) and rainbow trout ( Oncorhynchus mykiss ) (Wedemeyer et al, 1969) and cause a significant body mass loss in mosquitofish ( Gambusia holbrooki ) (Bonneaud et al, 2016). The immune response itself and the associated increase of metabolic activity can lead to an overproduction of reactive oxygen species (ROS), which may exceed the amount of antioxidant molecules and result in deleterious consequences on cell and tissue integrity (Cherry & Piantadosi, 2015; Costantini & Møller, 2009; Finkel & Holbrook, 2000; Jaeschke et al, 2002; Preynat‐Seauve et al, 2003).…”