Journal of Experimental Biology最新文献

Natural and anthropogenic stressors are dramatically altering environments, impacting key animal physiological traits, including cardiac performance. Animals require energy and nutrients from their diet to support cardiac performance and plasticity; however, the nutritional landscape is changing in response to environmental perturbations. Diet quantity, quality and options vary in space and time across heterogeneous environments, over the lifetime of an organism and in response to environmental stressors. Variation in dietary energy and nutrients (e.g. lipids, amino acids, vitamins, minerals) impact the heart's structure and performance, and thus whole-animal resilience to environmental change. Notably, many animals can alter their diet in response to environmental cues, depending on the context. Yet, most studies feed animals ad libitum using a fixed diet, thus underestimating the role of food in impacting cardiac performance and resilience. By applying an ecological lens to the study of cardiac plasticity, this Commentary aims to further our understanding of cardiac function in the context of environmental change.

Although a mechanism accounting for hyperthermic death at critical temperatures remains elusive, the mitochondria of crucial active excitable tissues (i.e. heart and brain) may well be key to this process. Mitochondria produce ∼90% of the ATP required by cells to maintain cellular integrity and function. They also integrate into biosynthetic pathways that support metabolism as a whole, allow communication within the cell, and regulate cellular health and death pathways. We have previously shown that cardiac and brain mitochondria demonstrate decreases in the efficiency of, and absolute capacity for ATP synthesis as temperatures rise, until ultimately there is too little ATP to support cellular demands, and organ failure follows. Importantly, substantial decreases in ATP synthesis occur at temperatures immediately below the temperature of heart failure, and this suggests a causal role of mitochondria in hyperthermic death. However, what causes mitochondria to fail? Here, we consider the answers to this question. Mitochondrial dysfunction at high temperature has classically been attributed to elevated leak respiration suspected to result from increased movement of protons (H+) through the inner mitochondrial membrane (IMM), thereby bypassing the ATP synthases. In this Commentary, we introduce some alternative explanations for elevated leak respiration. We first consider respiratory complex I and then propose that a loss of IMM structure occurs as temperatures rise. The loss of the cristae folds of the IMM may affect the efficiency of H+ transport, increasing H+ conductance either through the IMM or into the bulk water phases of mitochondria. In either case, O2 consumption increases while ATP synthesis decreases.

The hearts of salmonids display remarkable plasticity, adapting to various environmental factors that influence cardiac function and demand. For instance, in response to cold temperature, the salmonid heart undergoes growth and remodeling to counterbalance the reduced contractile function associated with dropping temperatures. Alongside heart size, the distinct pyramidal shape of the wild salmonid heart is essential for optimal cardiac performance, yet the environmental drivers behind this optimal cardiac morphology remain to be fully understood. Intriguingly, farmed salmonids often have rounded, asymmetrical ventricles and misaligned bulbi from an early age. These deformities are noteworthy given that farmed salmon are often not exposed to natural cues, such as a gradual temperature increase and changing day lengths, during critical developmental stages. In this study, we investigated whether natural environmental conditions during early life stages are pivotal for proper cardiac morphology. Atlantic salmon were raised under simulated natural conditions (low temperature with a natural photoperiod; SimNat) and compared with those reared under simulated farming conditions (SimFarm). Our findings reveal that the ventricle shape and bulbus alignment in SimNat fish closely resemble those of wild salmon, while functional analyses indicate significant differences between SimNat and SimFarm hearts, suggesting diastolic dysfunction and higher cardiac workload in SimFarm hearts. These findings highlight the profound influence of environmental factors such as water temperature and photoperiod on the structural development of the salmonid heart, underscoring the importance of early environmental conditions for cardiac health.

Very few vertebrates survive without oxygen (anoxia) for more than a few minutes. Crucian carp (Carassius carassius) are one example, surviving months of anoxia at low temperatures, and we hypothesised that they maintain mitochondrial membrane potential and function. Isolated crucian carp cardiomyocytes indeed maintained mitochondrial membrane potential after blocking complex IV of the electron transport system with cyanide, while those of anoxia-intolerant trout depolarised. When complexes I-III were inhibited, crucian carp mitochondria depolarised, indicating that these complexes need to function during anoxia. Mitochondrial membrane potential depended on reversal of ATP synthase in chemical anoxia, as blocking with cyanide combined with oligomycin to inhibit ATP synthase led to depolarisation. ATP synthase activity was reduced in the heart after 1 week of anoxia in crucian carp, together with a downregulation of ATP synthase subunit gene expression. However, the morphology of cardiac mitochondria was not affected by 1 week of anoxia, even with a large increase in mitofusin 2 mRNA expression. Cardiac citrate synthase activity was not affected by anoxia, while cytochrome c oxidase activity was increased. We show how mitochondria respond to anoxia. A mechanistic understanding of how mitochondrial function can be maintained in anoxia may provide new perspectives to reduce mitochondrial damage in anoxia-sensitive organisms.

Female Pacific salmon often experience higher mortality than males during their once-in-a-lifetime up-river spawning migration, particularly when exposed to secondary stressors (e.g. high temperatures). However, the underlying mechanisms remain unknown. One hypothesis is that female Pacific salmon hearts are more oxygen-limited than those of males and are less able to supply oxygen to the body's tissues during this demanding migration. Notably, female hearts have higher coronary blood flow, which could indicate a greater reliance on this oxygen source. Oxygen limitations can develop from naturally occurring coronary blockages (i.e. coronary arteriosclerosis) found in mature salmon hearts. If female hearts rely more heavily on coronary blood flow but experience similar arteriosclerosis levels as males, they will have disproportionately impaired aerobic performance. To test this hypothesis, we measured resting (RMR) and maximum metabolic rate (MMR), aerobic scope (AS) and acute upper thermal tolerance in coho salmon (Oncorhynchus kisutch) with an intact or artificially blocked coronary oxygen supply. We also assessed venous blood oxygen and chemistry (cortisol, ions and metabolite concentrations) at different time intervals during recovery from exhaustive exercise. We found that coronary blockage impaired MMR, AS and the partial pressure of oxygen in venous blood (PvO2) during exercise recovery but did not differ between sexes. Coronary ligation lowered acute upper thermal tolerance by 1.1°C. Although we did not find evidence of enhanced female reliance on coronary supply, our findings highlight the importance of coronary blood supply for mature wild salmon, where migration success may be linked to cardiac performance, particularly during warm water conditions.

The ventricle of the vertebrate heart is the main segment of the cardiac outflow region. Compared with other cardiac components, it shows remarkable histomorphological variation among different animal groups. This variation is especially apparent in the myocardium, which is generally classified into three main types: trabeculated, compact and mixed. The trabeculated or 'spongy' myocardium is characterized by the existence of trabeculae and deep recesses or intertrabecular spaces, lined by the endocardium. The compact type is composed of condensed myocardial fibers, with almost no trabeculated layer. The mixed type consists of an outer compact layer and an inner trabeculated layer. Among vertebrates, fishes show a great diversity of myocardial types. On this basis, the ventricular myoarchitecture has been categorized into four groups of varying complexity. This classification is made according to (i) the proportion of the two types of myocardium, trabeculated versus compact, and (ii) the vascularization of the heart wall. Here, we review the morphogenetic mechanisms that give rise to the different ventricular myoarchitecture in gnathostomes (i.e. jawed vertebrates) with special emphasis on the diversity of the ventricular myocardium throughout the phylogeny of ancient actinopterygians and teleosts. Finally, we propose that the classification of the ventricular myoarchitecture should be reconsidered, given that the degrees of myocardial compactness on which the current classification system is based do not constitute discrete states, but an anatomical continuum.

In bivalves and gastropods, ventricle contraction causes a negative pressure in the auricles and increases venous return from the afferent oblique vein (AOV): the constant-volume (CV) mechanism. The flow in the AOV should be a pulsative flow synchronized with the ventricular contraction. The flow in the heart and adjacent vessels of Mytilus galloprovincialis were measured by magnetic resonance imaging to confirm this hypothesis. Under a regular heartbeat, pulsative flows in the AOV and branchial vessels (BVs) were almost completely synchronized with the flow in the aorta, while filling of the ventricle was in the opposite phase. Flows in the BVs were directed to the posterior direction, and a pair of BVs in the gill axes (the efferent BVs) were connected to the AOV. Based on the images of the whole pathway of the AOV in an oblique slice, we confirmed that haemolymph flow was evoked from the efferent BVs and flow into the ventricle via the auricle was completed in a single heartbeat. Therefore, the walls of the AOV and BVs could resist negative transmural pressure caused by the ventricular contraction. In conclusion, the auricle, the AOV and the BVs, including the gill filaments, act as a suction pump. The pulsative venous return is driven by the negative pressure of the AOV as in the CV mechanism, and the negative pressure in the efferent BVs could draw haemolymph from the sinus via the gill and the afferent BVs. Therefore, Mytilus can start and stop its heartbeat as necessary.

Heart failure is among the first major consequences of heat stress in aquatic ectotherms. Mitochondria produce most of the ATP used by the heart and represent almost half of the volume in cardiac cells. It has therefore been hypothesized that mitochondrial dysfunction may be a major cause of heart failure associated with heat stress. The present study aims to investigate if CTmax is linked to the thermal sensitivity of cardiac mitochondria in the three-spined stickleback (Gasterosteus aculeatus), and if it is influenced by heart fatty acid composition and age. To do so, we measured the CTmax of 30 fish. The cardiac mitochondrial oxygen consumption was measured by high resolution respirometry at three temperatures and heart lipid profiles were obtained by gas chromatography (GC) coupled with a flame ionization detector (FID). Fish age was estimated via otolith readings. Fatty acid profiles showed no correlation with CTmax, but EPA levels were higher in older individuals. Mitochondrial respiration was measured in 35 fish using high-resolution respirometry. It was strongly affected by temperature and showed a drastic drop in OXPHOS respiration fed by complex I and complex I+complex II, while uncoupled respiration plateaued at CTmax temperature. Our results suggest that complex I is an important modulator of the impact of temperature on mitochondrial respiration at high temperatures but is not the main limiting factor in physiological conditions (maximal OXPHOS). Mitochondrial respiration was also affected by fish age, showing a general decrease in older individuals.

A prevailing assumption in the cardiovascular field is that the metabolic rate of the heart is a constant proportion of a mammal's whole-body aerobic metabolic rate. In this Commentary, we assemble previously published cardiovascular, metabolic and body mass data from matched terrestrial mammalian species, at rest and during heavy exercise, and reveal scaling relationships that challenge this assumption. Our analyses indicate that the fractional metabolic cost of systemic perfusion compared with whole-body metabolic rate increases significantly with body size among resting mammals, from ∼2.5% in a mouse to ∼10% in an elephant. We propose that two significant body size-dependent effects contribute to this conclusion; namely, that larger species generate higher mean systemic arterial blood pressure and that their myocardium operates with lower external mechanical efficiencies compared with those of smaller species. We discuss potential physiological and mechanical explanations, including the additional energy needed to support the arterial blood column above the heart in larger species, especially those with long necks, as well as the possible sources of greater internal energy losses from the heart of larger species. Thus, we present an updated view of how increasing blood pressure and decreasing efficiency of the myocardium result in an increasing fractional metabolic cost of perfusion as body size increases among resting mammals.

A decrease in environmental temperature represents a challenge to the cardiovascular system of ectotherms. To gain insight into the cellular changes that occur during cold exposure and cold acclimation we characterized the cardiac phosphoproteome and proteome of zebrafish following 24 h or 1 week exposure to 20°C from 27°C; or at multiple points during 6 weeks of acclimation to 20°C from 27°C. Our results indicate that cold exposure causes an increase in mitogen-activated protein kinase signalling, the activation of stretch-sensitive pathways, cellular remodelling via ubiquitin-dependent pathways and changes to the phosphorylation state of proteins that regulate myofilament structure and function including desmin and troponin T. Cold acclimation (2-6 weeks) led to a decrease in multiple components of the electron transport chain through time, but an increase in proteins for lipid transport, lipid metabolism, the incorporation of polyunsaturated fatty acids into membranes and protein turnover. For example, there was an increase in the levels of apolipoprotein C, prostaglandin reductase-3 and surfeit locus protein 4, involved in lipid transport, lipid metabolism and lipid membrane remodelling. Gill opercular movements suggest that oxygen utilization during cold acclimation is reduced. Neither the amount of food consumed relative to body mass nor body condition was affected by acclimation. These results suggest that while oxygen uptake was reduced, energy homeostasis was maintained. This study highlights that the response of zebrafish to a decrease in temperature is dynamic through time and that investment in the proteomic response increases with the duration of exposure.