• Energy Research

Abstract Background Progressive CO2-induced ocean acidification (OA) impacts marine life in ways that are difficult to predict but are likely to become exacerbated over generations. Although marine fishes can balance acid–base homeostasis efficiently, indirect ionic regulation that alter neurosensory systems can result in behavioural abnormalities. In marine invertebrates, OA can also affect immune system function, but whether this is the case in marine fishes is not fully understood. Farmed fish are highly susceptible to disease outbreak, yet strategies for overcoming such threats in the wake of OA are wanting. Here, we exposed two generations of the European sea bass (Dicentrarchus labrax) to end-of-century predicted pH levels (IPCC RCP8.5), with parents (F1) being exposed for four years and their offspring (F2) for 18 months. Our design included a transcriptomic analysis of the olfactory rosette (collected from the F2) and a viral challenge (exposing F2 to betanodavirus) where we assessed survival rates. Results We discovered transcriptomic trade-offs in both sensory and immune systems after long-term transgenerational exposure to OA. Specifically, RNA-Seq analysis of the olfactory rosette, the peripheral olfactory organ, from 18-months-old F2 revealed extensive regulation in genes involved in ion transport and neuronal signalling, including GABAergic signalling. We also detected OA-induced up-regulation of genes associated with odour transduction, synaptic plasticity, neuron excitability and wiring and down-regulation of genes involved in energy metabolism. Furthermore, OA-exposure induced up-regulation of genes involved in innate antiviral immunity (pathogen recognition receptors and interferon-stimulated genes) in combination with down-regulation of the protein biosynthetic machinery. Consistently, OA-exposed F2 challenged with betanodavirus, which causes damage to the nervous system of marine fish, had acquired improved resistance. Conclusion F2 exposed to long-term transgenerational OA acclimation showed superior viral resistance, though as their metabolic and odour transduction programs were altered, odour-mediated behaviours might be consequently impacted. Although it is difficult to unveil how long-term OA impacts propagated between generations, our results reveal that, across generations, trade-offs in plastic responses is a core feature of the olfactory epithelium transcriptome in OA-exposed F2 offspring, and will have important consequences for how cultured and wild fish interacts with its environment.

Abstract Background Progressive CO2-induced ocean acidification (OA) impacts marine life in ways that are difficult to predict but are likely to become exacerbated over generations. Although marine fishes can balance acid–base homeostasis efficiently, indirect ionic regulation that alter neurosensory systems can result in behavioural abnormalities. In marine invertebrates, OA can also affect immune system function, but whether this is the case in marine fishes is not fully understood. Farmed fish are highly susceptible to disease outbreak, yet strategies for overcoming such threats in the wake of OA are wanting. Here, we exposed two generations of the European sea bass (Dicentrarchus labrax) to end-of-century predicted pH levels (IPCC RCP8.5), with parents (F1) being exposed for four years and their offspring (F2) for 18 months. Our design included a transcriptomic analysis of the olfactory rosette (collected from the F2) and a viral challenge (exposing F2 to betanodavirus) where we assessed survival rates. Results We discovered transcriptomic trade-offs in both sensory and immune systems after long-term transgenerational exposure to OA. Specifically, RNA-Seq analysis of the olfactory rosette, the peripheral olfactory organ, from 18-months-old F2 revealed extensive regulation in genes involved in ion transport and neuronal signalling, including GABAergic signalling. We also detected OA-induced up-regulation of genes associated with odour transduction, synaptic plasticity, neuron excitability and wiring and down-regulation of genes involved in energy metabolism. Furthermore, OA-exposure induced up-regulation of genes involved in innate antiviral immunity (pathogen recognition receptors and interferon-stimulated genes) in combination with down-regulation of the protein biosynthetic machinery. Consistently, OA-exposed F2 challenged with betanodavirus, which causes damage to the nervous system of marine fish, had acquired improved resistance. Conclusion F2 exposed to long-term transgenerational OA acclimation showed superior viral resistance, though as their metabolic and odour transduction programs were altered, odour-mediated behaviours might be consequently impacted. Although it is difficult to unveil how long-term OA impacts propagated between generations, our results reveal that, across generations, trade-offs in plastic responses is a core feature of the olfactory epithelium transcriptome in OA-exposed F2 offspring, and will have important consequences for how cultured and wild fish interacts with its environment.

An individual's environmental history may have delayed effects on its physiology and life history at later stages in life because of irreversible plastic responses of early ontogenesis to environmental conditions. We chose a marine fish, the common sole, as a model species to study these effects, because it inhabits shallow marine areas highly exposed to environmental changes. We tested whether temperature and trophic conditions experienced during the larval stage had delayed effects on life-history traits and resistance to hypoxia at the juvenile stage. We thus examined the combined effect of global warming and hypoxia in coastal waters, which are potential stressors to many estuarine and coastal marine fishes. Elevated temperature and better trophic conditions had a positive effect on larval growth and developmental rates; warmer larval temperature had a delayed positive effect on body mass and resistance to hypoxia at the juvenile stage. The latter suggests a lower oxygen demand of individuals that had experienced elevated temperatures during larval stages. We hypothesize that an irreversible plastic response to temperature occurred during early ontogeny that allowed adaptive regulation of metabolic rates and/or oxygen demand with long-lasting effects. These results could deeply affect predictions about impacts of global warming and eutrophication on marine organisms.

An individual's environmental history may have delayed effects on its physiology and life history at later stages in life because of irreversible plastic responses of early ontogenesis to environmental conditions. We chose a marine fish, the common sole, as a model species to study these effects, because it inhabits shallow marine areas highly exposed to environmental changes. We tested whether temperature and trophic conditions experienced during the larval stage had delayed effects on life-history traits and resistance to hypoxia at the juvenile stage. We thus examined the combined effect of global warming and hypoxia in coastal waters, which are potential stressors to many estuarine and coastal marine fishes. Elevated temperature and better trophic conditions had a positive effect on larval growth and developmental rates; warmer larval temperature had a delayed positive effect on body mass and resistance to hypoxia at the juvenile stage. The latter suggests a lower oxygen demand of individuals that had experienced elevated temperatures during larval stages. We hypothesize that an irreversible plastic response to temperature occurred during early ontogeny that allowed adaptive regulation of metabolic rates and/or oxygen demand with long-lasting effects. These results could deeply affect predictions about impacts of global warming and eutrophication on marine organisms.

Abstract Background Progressive climate-induced ocean acidification (OA) impacts marine life in ways that are difficult to predict but are likely to become exacerbated over generations. Although marine fishes can balance internal acid-base homeostasis efficiently, indirect ionic regulation effects that alter neurosensory systems can result in behavioural abnormalities. In marine invertebrates, OA can also affect immune system function, but whether this is the case in marine fishes of ecological and commercial importance is not yet understood. Farmed fish are highly susceptible to disease outbreak yet strategies for overcoming such threats in the wake of OA are wanting. Here, we exposed two generations of the European sea bass (Dicentrarchus labrax) to end-of-century predicted CO2 levels (IPCC RCP8.5), with parents being exposed for four years and their offspring for two years. Our design included a transcriptomic analysis of the olfactory rosette (collected from the F1 offspring) and a viral challenge (exposing F1 offspring to betanodavirus) where we assessed survival rates. Results We discovered long-term intergenerational molecular trade-offs in both sensory and immune systems. Specifically, RNA-Seq analysis of the olfactory rosette, the peripheral olfactory organ, from two-year-old F1 offspring revealed extensive regulation in genes involved in ion transport and neuronal signalling, including GABAergic signalling. We also detected extensive OA-induced intergenerational up-regulation of genes associated with odour transduction, synaptic plasticity, neuron excitability and wiring and down-regulation of genes involved in energy metabolism. In addition, intergenerational exposure to OA induced up-regulation of genes involved in innate antiviral immunity (pathogen recognition receptors and interferon-stimulated genes) in combination with down-regulation of the protein biosynthetic machinery. Consistently, OA-exposed F1 fish challenged with betanodavirus, which causes damage to the nervous system of marine fish, had acquired improved resistance. Conclusion F1 exposed to OA-intergenerational acclimation showed superior viral resistance, though as their metabolic and odour transduction programs were altered, odour-mediated behaviours might be consequently altered. Our results reveal that trade-offs in adaptive plastic responses is a core feature of the olfactory epithelium transcriptome in OA-exposed fish, suggesting that intergenerational plasticity propagate with progressive exposure to OA and will have important consequences for how cultured and wild fish interacts with its environment.

Abstract Background Progressive climate-induced ocean acidification (OA) impacts marine life in ways that are difficult to predict but are likely to become exacerbated over generations. Although marine fishes can balance internal acid-base homeostasis efficiently, indirect ionic regulation effects that alter neurosensory systems can result in behavioural abnormalities. In marine invertebrates, OA can also affect immune system function, but whether this is the case in marine fishes of ecological and commercial importance is not yet understood. Farmed fish are highly susceptible to disease outbreak yet strategies for overcoming such threats in the wake of OA are wanting. Here, we exposed two generations of the European sea bass (Dicentrarchus labrax) to end-of-century predicted CO2 levels (IPCC RCP8.5), with parents being exposed for four years and their offspring for two years. Our design included a transcriptomic analysis of the olfactory rosette (collected from the F1 offspring) and a viral challenge (exposing F1 offspring to betanodavirus) where we assessed survival rates. Results We discovered long-term intergenerational molecular trade-offs in both sensory and immune systems. Specifically, RNA-Seq analysis of the olfactory rosette, the peripheral olfactory organ, from two-year-old F1 offspring revealed extensive regulation in genes involved in ion transport and neuronal signalling, including GABAergic signalling. We also detected extensive OA-induced intergenerational up-regulation of genes associated with odour transduction, synaptic plasticity, neuron excitability and wiring and down-regulation of genes involved in energy metabolism. In addition, intergenerational exposure to OA induced up-regulation of genes involved in innate antiviral immunity (pathogen recognition receptors and interferon-stimulated genes) in combination with down-regulation of the protein biosynthetic machinery. Consistently, OA-exposed F1 fish challenged with betanodavirus, which causes damage to the nervous system of marine fish, had acquired improved resistance. Conclusion F1 exposed to OA-intergenerational acclimation showed superior viral resistance, though as their metabolic and odour transduction programs were altered, odour-mediated behaviours might be consequently altered. Our results reveal that trade-offs in adaptive plastic responses is a core feature of the olfactory epithelium transcriptome in OA-exposed fish, suggesting that intergenerational plasticity propagate with progressive exposure to OA and will have important consequences for how cultured and wild fish interacts with its environment.