The anaerobic energy metabolism of goldfish determined by simultaneous direct and indirect calorimetry during anoxia and hypoxia

Waversveld, J. van; Addink, Albert D.F.; Thillart, G. van den

doi:10.1007/bf00691503

Cited by 52 publications

(22 citation statements)

References 8 publications

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“…The most accurate surrogate method for measuring ATP turnover (or total metabolic rate) is to monitor metabolic heat production because a decrease in heat production signifies a decrease in ATP turnover and metabolic rate. Decreases in heat production in response to hypoxia exposure have been measured in many fish species including goldfish (van Waversveld et al, 1989a;van Waversveld et al, 1989b;van Waversveld et al, 1988), crucian carp (Johansson et al, 1995), tilapia (Oreochromis mossambiscus) (van Ginneken et al, 1999;van Ginneken et al, 1997) and European eel (Anguilla anguilla) (van Ginneken et al, 2001), and in isolated liver cells from rainbow trout (Oncorhynchus mykiss) (Rissanen et al, 2006). Interestingly, across this very broad range of fish species that includes species considered to be extremely hypoxia tolerant (crucian carp, goldfish, and tilapia) and tissues from fish considered to be very hypoxia sensitive (rainbow trout), all species show the capacity to decrease metabolic rate in response to hypoxia exposure.…”

Section: The Metabolic Challenge Of Surviving O 2 Tensions Below P Critmentioning

confidence: 99%

Physiological, behavioral and biochemical adaptations of intertidal fishes to hypoxia

Richards

2011

Journal of Experimental Biology

262

202

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SummaryHypoxia survival in fish requires a well-coordinated response to either secure more O 2 from the hypoxic environment or to limit the metabolic consequences of an O 2 restriction at the mitochondria. Although there is a considerable amount of information available on the physiological, behavioral, biochemical and molecular responses of fish to hypoxia, very little research has attempted to determine the adaptive value of these responses. This article will review current attempts to use the phylogenetically corrected comparative method to define physiological and behavioral adaptations to hypoxia in intertidal fish and further identify putatively adaptive biochemical traits that should be investigated in the future. In a group of marine fishes known as sculpins, from the family Cottidae, variation in hypoxia tolerance, measured as a critical O 2 tension (P crit ), is primarily explained by variation in mass-specific gill surface area, red blood cell hemoglobin-O 2 binding affinity, and to a lesser extent variation in routine O 2 consumption rate (M O2 ). The most hypoxia-tolerant sculpins consistently show aquatic surface respiration (ASR) and aerial emergence behavior during hypoxia exposure, but no phylogenetically independent relationship has been found between the thresholds for initiating these behaviors and P crit . At O 2 levels below P crit , hypoxia survival requires a rapid reorganization of cellular metabolism to suppress ATP consumption to match the limited capacity for O 2 -independent ATP production. Thus, it is reasonable to speculate that the degree of metabolic rate suppression and the quantity of stored fermentable fuel is strongly selected for in hypoxia-tolerant fishes; however, these assertions have not been tested in a phylogenetic comparative model.

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Section: The Metabolic Challenge Of Surviving O 2 Tensions Below P Critmentioning

confidence: 99%

Physiological, behavioral and biochemical adaptations of intertidal fishes to hypoxia

Richards

2011

Journal of Experimental Biology

262

202

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“…This oxygen level is below their critical O 2 concentration (~1.0·mg·l -1 at 8°C for crucian carp) (Nilsson, 1992), which represents the P O 2 at which oxygen delivery to the tissues becomes seriously compromised and fish can no longer fulfil their energy requirements by aerobic metabolism alone. Consequently adaptive responses, including activation of anaerobic energy production and remodelling of gill epithelia to enhance oxygen uptake, are turned on (Vanwaversveld et al, 1989;Sollid et al, 2003).…”

Section: Temperature Affects Hypoxic Regulation Of Hif-1mentioning

confidence: 99%

Temperature regulates hypoxia-inducible factor-1 (HIF-1) in a poikilothermic vertebrate, crucian carp (Carassius carassius)

Rissanen

Tranberg

Sollid

et al. 2006

Journal of Experimental Biology

146

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SUMMARY Hypoxia-inducible transcription factor-1 (HIF-1) is a master regulator of hypoxia-induced gene responses. To find out whether HIF-1 function is involved in gene expression changes associated with temperature acclimation as well as in hypoxia adaptation in poikilotherms, we studied HIF-1 DNA binding activity and HIF-1α expression in normoxia and during hypoxia (0.7 mg l–1 O2) in crucian carp at temperatures of 26, 18 and 8°C. Temperature had a marked influence on HIF-1 in normoxia. Although HIF-1α mRNA levels remained unaltered, cold acclimation (8°C)increased HIF-1α protein amounts in the liver, gills and heart and HIF-1 DNA binding activity in the heart, gills and kidney of crucian carp by two- to threefold compared to warm acclimated fish (26°C). In the heart and kidney HIF-1 activity was already significantly increased in the 18°C acclimated fish. Temperature also affected hypoxic regulation of HIF-1. Although hypoxia initially increased amounts of HIF-1α protein in all studied tissues at every temperature, except for liver at 18°C, HIF-1 activity increased only in the heart of 8°C acclimated and in the gills of 18°C acclimated fish. At 8°C HIF-1α mRNA levels increased transiently in the gills after 6 h of hypoxia and in the kidney after 48 h of hypoxia. In the gills at 26°C HIF-1α mRNA levels increased after 6 h of hypoxia and remained above normoxic levels for up to 48 h of hypoxia. These results show that HIF-1 is involved in controlling gene responses to both oxygen and temperature in crucian carp. No overall transcriptional control mechanism has been described for low temperature acclimation in poikilotherms, but the present results suggest that HIF-1 could have a role in such regulation. Moreover, this study highlights interaction of the two prime factors defining metabolism,temperature and oxygen, in the transcriptional control of metabolic homeostasis in animals.

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“…To assess the effects of hypoxia and gill remodeling on Cl Ϫ efflux (JOUTCl Ϫ ), fish were lightly anesthetized and injected intraperitoneally with 40 Ci kg Ϫ1 of 36 Cl (American Radiolabeled Chemicals, St. Louis, MO) and allowed to recover for 12 h. Fish were anesthetized (ethyl-P-aminobenzoate, 2.4 ϫ 10 Ϫ4 mol/l), and their vents were sutured shut and glued to eliminate urinary excretion for 7 h (the fish were too small to be fitted with urinary catheters). The fish were placed in their chambers, and after 3 h water flow was stopped and 10 ml samples were collected for 4 h at hourly intervals to determine the appearance of 36 Cl. After 4 h, the fish were euthanized with anesthetic, and blood samples (ϳ300 l) were collected by caudal puncture into heparinized syringes.…”

Section: Fig 2 Effects Of Exposure To Hypoxia For 7 Days On Branchimentioning

confidence: 99%

Physiological consequences of gill remodeling in goldfish (Carassius auratus) during exposure to long-term hypoxia

Mitrovic¹,

Dymowska²,

Nilsson³

et al. 2009

American Journal of Physiology-Regulatory, Integrative and Comp

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Mitrovic D, Dymowska A, Nilsson GE, Perry SF. Physiological consequences of gill remodeling in goldfish (Carassius auratus) during exposure to long-term hypoxia. Am J Physiol Regul Integr Comp Physiol 297: R224 -R234, 2009. First published May 20, 2009 doi:10.1152/ajpregu.00189.2009 acclimated to 7°C and exposed to hypoxia (ϳ10 mmHg) for 7 days exhibited a pronounced remodeling of the gill consisting of the removal of an interlamellar cell mass (ILCM). Subsequent experiments were designed to assess the impact of gill remodeling and the associated increase in functional lamellar surface area on the distribution of branchial ionocytes and Cl Ϫ flux across the gill. Despite the increased functional lamellar surface area during hypoxia, there was no corresponding increase in Cl Ϫ loss or efflux of the extracellular marker polyethylene glycol (PEG 4000). However, when hypoxic fish were returned to normoxic water for 12 h, rates of Cl Ϫ and PEG efflux were markedly stimulated in keeping with an increased surface area for solute movement. Similarly, the rate of branchial Cl Ϫ uptake was reduced (105 Ϯ 22 vs. 45 Ϯ 8 mol ⅐ kg Ϫ1 ⅐ h Ϫ1 ) in normoxic and hypoxic fish, respectively, but then stimulated (345 mol ⅐ kg Ϫ1 ⅐ h Ϫ1 ) upon reestablishment of normoxic conditions. Hypoxia (7 days) was accompanied by a significant decrease in the total cross-sectional area of branchial ionocytes owing to a decrease in their numbers and individual sizes. Thus, despite experiencing an increase in functional lamellar surface area, hypoxic goldfish limit branchial Cl Ϫ loss likely by a hypoxia-mediated decrease in paracellular permeability. In normoxic fish, the ionocytes were largely confined to the outer edges of the ILCM. During hypoxia, preexisting ionocytes migrated with the shrinking ILCM, while a smaller proportion of newly differentiated cells appeared below the surface of the ILCM. The capacity to maintain a population of ionocytes in contact with the water is an appropriate strategy to retain ionoregulatory capabilities regardless of whether the lamellae are uncovered or covered.

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The anaerobic energy metabolism of goldfish determined by simultaneous direct and indirect calorimetry during anoxia and hypoxia

Cited by 52 publications

References 8 publications

Physiological, behavioral and biochemical adaptations of intertidal fishes to hypoxia

Physiological, behavioral and biochemical adaptations of intertidal fishes to hypoxia

Temperature regulates hypoxia-inducible factor-1 (HIF-1) in a poikilothermic vertebrate, crucian carp (Carassius carassius)

Physiological consequences of gill remodeling in goldfish (Carassius auratus) during exposure to long-term hypoxia

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