Abstract
Organismal metabolic rate, a fundamental metric in biology, demonstrates an allometric scaling relationship with body size. Fractal-like vascular distribution networks of biological systems are proposed to underlie metabolic rate allometric scaling laws from individual organisms to cells, mitochondria, and enzymes. Tissue-specific metabolic scaling is notably absent from this paradigm. In the current study, metabolic scaling relationships of hearts and brains with body size were examined by improving on a high-throughput whole-organ oxygen consumption rate (OCR) analysis method in five biomedically and environmentally relevant teleost model species. Tissue-specific metabolic scaling was compared with organismal routine metabolism (RMO2), which was measured using whole organismal respirometry. Basal heart OCR and organismal RMO2 scaled identically with body mass in a species-specific fashion across all five species tested. However, organismal maximum metabolic rates (MMO2) and pharmacologically-induced maximum cardiac metabolic rates in zebrafish Danio rerio did not show a similar relationship with body mass. Brain metabolic rates did not scale with body size. The identical allometric scaling of heart and organismal metabolic rates with body size suggests that hearts, the power generator of an organism’s vascular distribution network, might be crucial in determining teleost metabolic rate scaling under routine conditions. Furthermore, these findings indicate the possibility of measuring heart OCR utilizing the high-throughput approach presented here as a proxy for organismal metabolic rate—a useful metric in characterizing organismal fitness. In addition to heart and brain OCR, the current approach was also used to measure whole liver OCR, partition cardiac mitochondrial bioenergetic parameters using pharmacological agents, and estimate heart and brain glycolytic rates. This high-throughput whole-organ bioenergetic analysis method has important applications in toxicology, evolutionary physiology, and biomedical sciences, particularly in the context of investigating pathogenesis of mitochondrial diseases.
Highlights
The metabolic rate, often characterized as the rate of oxygen consumption, is a fundamental metric in physiological, ecological and evolutionary analyses of organismal survival and fitness
We improved on a method developed by Little and Seebacher [10] to examine ex vivo heart-specific oxygen consumption rate (OCR) using the XFe24 Extracellular Flux Analyzer (Seahorse Bioscience, Billerica, MA) to explore (i) metabolic rate scaling of heart and brain tissues with organ size and body size and (ii) how these scaling relationships compare with whole organismal metabolic rates in five biomedically and environmentally relevant teleost model species— zebrafish (Danio rerio), Atlantic killifish (Fundulus heteroclitus), mosquito fish (Gambusia holbrooki), Japanese medaka (Oryzias latipes), and fathead minnow (Pimephales promelas)
The methods we describe here provide a rapid and relatively simple high-throughput approach to estimate mitochondrial bioenergetics ex vivo with intact hearts of small (~
Summary
The metabolic rate, often characterized as the rate of oxygen consumption, is a fundamental metric in physiological, ecological and evolutionary analyses of organismal survival and fitness. The metabolic rate of an organism demonstrates an allometric scaling relationship with body mass according to the equation Y = a Mb, where Y is metabolic rate, M is body mass, a is the species-specific scaling constant, and b is the scaling exponent [1,2,3,4]. We improved on a method developed by Little and Seebacher [10] to examine ex vivo heart-specific oxygen consumption rate (OCR) using the XFe24 Extracellular Flux Analyzer (Seahorse Bioscience, Billerica, MA) to explore (i) metabolic rate scaling of heart and brain tissues with organ size and body size and (ii) how these scaling relationships compare with whole organismal metabolic rates in five biomedically and environmentally relevant teleost model species— zebrafish (Danio rerio), Atlantic killifish (Fundulus heteroclitus), mosquito fish (Gambusia holbrooki), Japanese medaka (Oryzias latipes), and fathead minnow (Pimephales promelas). To investigate the metabolic scaling relationship between basal tissue-specific OCR and routine whole organismal metabolic rate (RMO2), we quantified whole organismal respiration rates for each fish prior to heart and brain measurements in all five species
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