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Scaling with body mass of mitochondrial respiration from the white muscle of three phylogenetically, morphologically and behaviorally disparate teleost fishes

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Abstract

White muscle (WM) fibers in many fishes often increase in size from <50 μm in juveniles to >250 μm in adults. This leads to increases in intracellular diffusion distances that may impact the scaling with body mass of muscle metabolism. We have previously found similar negative scaling of aerobic capacity (mitochondrial volume density, V mt) and the rate of an aerobic process (post-contractile phosphocreatine recovery) in fish WM. In the present study, we examined the scaling with body mass of oxygen consumption rates of isolated mitochondria (VO2mt) from WM in three species from different families that vary in morphology and behavior: an active, pelagic species (bluefish, Pomatomus saltatrix), a relatively inactive demersal species (black sea bass, Centropristis striata), and a sedentary, benthic species (southern flounder, Paralichthys lethostigma). In contrast to our prior studies, the measurement of respiration in isolated mitochondria is not influenced by the diffusion of oxygen or metabolites. V mt was measured in WM and in high-density isolates used for VO2mt measurements. WM V mt was significantly higher in the bluefish than in the other two species and VO2mt was independent of body mass when expressed per milligram protein or per milliliter mitochondria. The size-independence of VO2mt indicates that differences in WM aerobic function result from variation in V mt and not to changes in VO2mt. This is consistent with our prior work that indicated that while diffusion constraints influence mitochondrial distribution, the negative scaling of aerobic processes like post-contractile PCr recovery can largely be attributed to the body size dependence of V mt.

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Abbreviations

VO2max:

Maximal rate of oxygen consumption

V mt :

Mitochondrial volume density

VO2mt:

Rate of mitochondrial oxygen consumption

RM:

Red muscle

WM:

White muscle

TEM:

Transmission electron microscopy

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Acknowledgments

This research was supported by a National Science Foundation Grant to S.T.K. and R.M.D. (IOS-0719123) and a National Institute of Arthritis and Musculoskeletal and Skin Diseases Grant to S.T.K. (R15-AR052708). We also thank Mark Gay for assistance with microscopy, Dr. Heather Koopman for constructive comments on the manuscript, and Dr. Christopher D. Moyes for helpful suggestions on experimental procedures.

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Authors and Affiliations

  1. Department of Biology and Marine Biology, University of North Carolina Wilmington, 601 S. College Rd., Wilmington, NC, 28403-5915, USA

    Jessica L. Burpee, Elise L. Bardsley, Richard M. Dillaman & Stephen T. Kinsey

  2. Center for Marine Science, University of North Carolina Wilmington, 601 S. College Rd., Wilmington, NC, 28403-5927, USA

    Wade O. Watanabe

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  1. Jessica L. Burpee
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  2. Elise L. Bardsley
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  5. Stephen T. Kinsey
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Correspondence to Stephen T. Kinsey.

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Communicated by G. Heldmaier.

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Burpee, J.L., Bardsley, E.L., Dillaman, R.M. et al. Scaling with body mass of mitochondrial respiration from the white muscle of three phylogenetically, morphologically and behaviorally disparate teleost fishes. J Comp Physiol B 180, 967–977 (2010). https://doi.org/10.1007/s00360-010-0474-x

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