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result(s) for
"Nilsson, Göran E"
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Molecular signatures of transgenerational response to ocean acidification in a species of reef fish
Ocean acidification impairs reef fish behaviour. This study shows offspring of spiny damselfish sensitive to high CO
2
levels have different brain molecular responses to those of tolerant individuals, suggesting individual variation may allow adaptation.
The impact of ocean acidification on marine ecosystems will depend on species capacity to adapt
1
,
2
. Recent studies show that the behaviour of reef fishes is impaired at projected CO
2
levels
3
,
4
; however, individual variation exists that might promote adaptation. Here, we show a clear signature of parental sensitivity to high CO
2
in the brain molecular phenotype of juvenile spiny damselfish,
Acanthochromis polyacanthus
, primarily driven by circadian rhythm genes. Offspring of CO
2
-tolerant and CO
2
-sensitive parents were reared at near-future CO
2
(754 μatm) or present-day control levels (414 μatm). By integrating 33 brain transcriptomes and proteomes with a
de novo
assembled genome we investigate the molecular responses of the fish brain to increased CO
2
and the expression of parental tolerance to high CO
2
in the offspring molecular phenotype. Exposure to high CO
2
resulted in differential regulation of 173 and 62 genes and 109 and 68 proteins in the tolerant and sensitive groups, respectively. Importantly, the majority of differences between offspring of tolerant and sensitive parents occurred in high CO
2
conditions. This transgenerational molecular signature suggests that individual variation in CO
2
sensitivity could facilitate adaptation of fish populations to ocean acidification.
Journal Article
Near-future carbon dioxide levels alter fish behaviour by interfering with neurotransmitter function
A study of two species of coral reef fish demonstrates that the anticipated increase in atmospheric carbon dioxide directly interferes with neurotransmitter function in their larvae, a hitherto unrecognized problem for marine fishes.
Predicted future CO
2
levels have been found to alter sensory responses and behaviour of marine fishes. Changes include increased boldness and activity, loss of behavioural lateralization, altered auditory preferences and impaired olfactory function
1
,
2
,
3
,
4
,
5
. Impaired olfactory function makes larval fish attracted to odours they normally avoid, including ones from predators and unfavourable habitats
1
,
3
. These behavioural alterations have significant effects on mortality that may have far-reaching implications for population replenishment, community structure and ecosystem function
2
,
6
. However, the underlying mechanism linking high CO
2
to these diverse responses has been unknown. Here we show that abnormal olfactory preferences and loss of behavioural lateralization exhibited by two species of larval coral reef fish exposed to high CO
2
can be rapidly and effectively reversed by treatment with an antagonist of the GABA-A receptor. GABA-A is a major neurotransmitter receptor in the vertebrate brain. Thus, our results indicate that high CO
2
interferes with neurotransmitter function, a hitherto unrecognized threat to marine populations and ecosystems. Given the ubiquity and conserved function of GABA-A receptors, we predict that rising CO
2
levels could cause sensory and behavioural impairment in a wide range of marine species, especially those that tightly control their acid–base balance through regulatory changes in HCO
3
−
and Cl
−
levels.
Journal Article
Marine mollusc predator-escape behaviour altered by near-future carbon dioxide levels
Ocean acidification poses a range of threats to marine invertebrates; however, the potential effects of rising carbon dioxide (CO2) on marine invertebrate behaviour are largely unknown. Marine gastropod conch snails have a modified foot and operculum allowing them to leap backwards rapidly when faced with a predator, such as a venomous cone shell. Here, we show that projected near-future seawater CO2 levels (961 µatm) impair this escape behaviour during a predator–prey interaction. Elevated-CO2 halved the number of snails that jumped from the predator, increased their latency to jump and altered their escape trajectory. Physical ability to jump was not affected by elevated-CO2 indicating instead that decision-making was impaired. Antipredator behaviour was fully restored by treatment with gabazine, a GABA antagonist of some invertebrate nervous systems, indicating potential interference of neurotransmitter receptor function by elevated-CO2, as previously observed in marine fishes. Altered behaviour of marine invertebrates at projected future CO2 levels could have potentially far-reaching implications for marine ecosystems.
Journal Article
Extreme anoxia tolerance in crucian carp and goldfish through neofunctionalization of duplicated genes creating a new ethanol-producing pyruvate decarboxylase pathway
Without oxygen, most vertebrates die within minutes as they cannot meet cellular energy demands with anaerobic metabolism. However, fish of the genus
Carassius
(crucian carp and goldfish) have evolved a specialized metabolic system that allows them to survive prolonged periods without oxygen by producing ethanol as their metabolic end-product. Here we show that this has been made possible by the evolution of a pyruvate decarboxylase, analogous to that in brewer’s yeast and the first described in vertebrates, in addition to a specialized alcohol dehydrogenase. Whole-genome duplication events have provided additional gene copies of the pyruvate dehydrogenase multienzyme complex that have evolved into a pyruvate decarboxylase, while other copies retained the essential function of the parent enzymes. We reveal the key molecular substitution in duplicated pyruvate dehydrogenase genes that underpins one of the most extreme hypoxic survival strategies among vertebrates and that is highly deleterious in humans.
Journal Article
Atlantic salmon show capability for cardiac acclimation to warm temperatures
Increases in environmental temperature predicted to result from global warming have direct effects on performance of ectotherms. Moreover, cardiac function has been observed to limit the tolerance to high temperatures. Here we show that two wild populations of Atlantic salmon originating from northern and southern extremes of its European distribution have strikingly similar cardiac responses to acute warming when acclimated to common temperatures, despite different local environments. Although cardiac collapse starts at 21–23 °C with a maximum heart rate of ~\\n150 beats per min (bpm) for 12 °C-acclimated fish, acclimation to 20 °C considerably raises this temperature (27.5 °C) and maximum heart rate (~\\n200 bpm). Only minor population differences exist and these are consistent with the warmer habitat of the southern population. We demonstrate that the considerable cardiac plasticity discovered for Atlantic salmon is largely independent of natural habitat, and we propose that observed cardiac plasticity may aid salmon to cope with global warming.
Cardiac function can limit high-temperature tolerance in fish. Here, Antilla
et al.
show similar cardiac responses to warming for two wild Atlantic salmon populations with different environmental temperatures, which suggests that cardiac plasticity is independent of natural habitat.
Journal Article
Counter-Gradient Variation in Respiratory Performance of Coral Reef Fishes at Elevated Temperatures
The response of species to global warming depends on how different populations are affected by increasing temperature throughout the species' geographic range. Local adaptation to thermal gradients could cause populations in different parts of the range to respond differently. In aquatic systems, keeping pace with increased oxygen demand is the key parameter affecting species' response to higher temperatures. Therefore, respiratory performance is expected to vary between populations at different latitudes because they experience different thermal environments. We tested for geographical variation in respiratory performance of tropical marine fishes by comparing thermal effects on resting and maximum rates of oxygen uptake for six species of coral reef fish at two locations on the Great Barrier Reef (GBR), Australia. The two locations, Heron Island and Lizard Island, are separated by approximately 1200 km along a latitudinal gradient. We found strong counter-gradient variation in aerobic scope between locations in four species from two families (Pomacentridae and Apogonidae). High-latitude populations (Heron Island, southern GBR) performed significantly better than low-latitude populations (Lizard Island, northern GBR) at temperatures up to 5°C above average summer surface-water temperature. The other two species showed no difference in aerobic scope between locations. Latitudinal variation in aerobic scope was primarily driven by up to 80% higher maximum rates of oxygen uptake in the higher latitude populations. Our findings suggest that compensatory mechanisms in high-latitude populations enhance their performance at extreme temperatures, and consequently, that high-latitude populations of reef fishes will be less impacted by ocean warming than will low-latitude populations.
Journal Article
Surviving without oxygen involves major tissue specific changes in the proteome of crucian carp ( Carassius carassius )
The crucian carp ( Carassius carassius ) can survive complete oxygen depletion (anoxia) for several months at low temperatures, making it an excellent model for studying molecular adaptations to anoxia. Still, little is known about how its global proteome responds to anoxia and reoxygenation. By applying mass spectrometry-based proteome analyses on brain, heart and liver tissue from crucian carp exposed to normoxia, five days anoxia, and reoxygenation, we found major changes in particularly cardiac and hepatic protein levels in response to anoxia and reoxygenation. These included tissue-specific differences in mitochondrial proteins involved in aerobic respiration and mitochondrial membrane integrity. Enzymes in the electron transport system (ETS) decreased in heart and increased massively in liver during anoxia and reoxygenation but did not change in the brain. Importantly, the data support a special role for the liver in succinate handling upon reoxygenation, as suggested by a drastic increase of components of the ETS and uncoupling protein 2, which could allow for succinate metabolism without excessive formation of reactive oxygen species (ROS). Also during reoxygenation, the levels of proteins involved in the cristae junction organization of the mitochondria changed in the heart, possibly functioning to suppress ROS formation. Furthermore, proteins involved in immune (complement) system activation changed in the anoxic heart compared to normoxic controls. The results emphasize that responses to anoxia are highly tissue-specific and related to organ function.
Journal Article
The Metabolomic Response of Crucian Carp (Carassius carassius) to Anoxia and Reoxygenation Differs between Tissues and Hints at Uncharacterized Survival Strategies
The anoxia-tolerant crucian carp (Carassius carassius) has been studied in detail for numerous years, with particular focus on unravelling the underlying physiological mechanisms of anoxia tolerance. However, relatively little work has been focused on what occurs beyond anoxia, and often the focus is a single organ or tissue type. In this study, we quantified more than 100 metabolites by capillary electrophoresis-mass spectrometry (CE-MS) in brain, heart, liver, and blood plasma from four experimental groups, being normoxic (control) fish, anoxia-exposed fish, and two groups that had been exposed to anoxia followed by reoxygenation for either 3 h or 24 h. The heart, which maintains cardiac output during anoxia, unexpectedly, was slower to recover compared to the brain and liver, mainly due to a slower return to control concentrations of the energy-carrying compounds ATP, GTP, and phosphocreatine. Crucian carp accumulated amino acids in most tissues, and also surprisingly high levels of succinate in all tissues investigated during anoxia. Purine catabolism was enhanced, leading to accumulation of uric acid during anoxia and increasing urea formation that continued into 24 h of reoxygenation. These tissue-specific differences in accumulation and distribution of the metabolites may indicate an intricate system of transport between tissues, opening for new avenues of investigation of possible mechanisms aimed at reducing the generation of reactive oxygen species (ROS) and resultant tissue damage during reoxygenation.
Journal Article