Variation in metabolic rate among individuals is related to tissue-specific differences in mitochondrial leak respiration

Salin, K., Auer, S. K., Rudolf, A. M., Anderson, G. J., Selman, C. and Metcalfe, N. B. (2016) Variation in metabolic rate among individuals is related to tissue-specific differences in mitochondrial leak respiration. Physiological and Biochemical Zoology, 89(6), pp. 511-523. (doi: 10.1086/688769) (PMID:27792536)

Abstract

Standard metabolic rate (SMR) and maximum metabolic rate (MMR) typically vary two- or threefold among conspecifics, with both traits assumed to significantly impact fitness. However, the underlying mechanisms that determine such intraspecific variation are not well understood. We examined the influence of mitochondrial properties on intraspecific variation in SMR and MMR and hypothesized that if SMR supports the cost of maintaining the metabolic machinery required for MMR, then the mitochondrial properties underlying these traits should be shared. Mitochondrial respiratory capacity (leak and phosphorylating respiration) and mitochondrial content (cytochrome c oxidase activity) were determined in the liver and white muscle of brown trout Salmo trutta of similar age and maintenance conditions. SMR and MMR were uncorrelated across individuals and were not associated with the same mitochondrial properties, suggesting that they are under the control of separate physiological processes. Moreover, tissue-specific relationships between mitochondrial properties and whole-organism metabolic traits were observed. Specifically, SMR was positively associated with leak respiration in liver mitochondria, while MMR was positively associated with muscle mitochondrial leak respiration and mitochondrial content. These results suggest that a high SMR or MMR, rather than signaling a higher ability for respiration-driven ATP synthesis, may actually reflect greater dissipation of energy, driven by proton leak across the mitochondrial inner membrane. Knowledge of these links should aid interpretation of the potential fitness consequences of such variation in metabolism, given the importance of mitochondria in the utilization of resources and their allocation to performance.

• Item Type: Articles
• Additional Information: This research was supported by a European Research Council Advanced Grant (number 322784) to N.B.M.
• Keywords: Brown trout, fish, liver, oxygen consumption, white muscle.
• Status: Published
• Refereed: Yes
• Glasgow Author(s) Enlighten ID: Anderson, Mr Graeme and Auer, Dr Sonya and Selman, Professor Colin and Rudolf, Ms Agata Marta and Metcalfe, Professor Neil and Salin, Dr Karine
• Authors: Salin, K., Auer, S. K., Rudolf, A. M., Anderson, G. J., Selman, C., and Metcalfe, N. B.
• Subjects: Q Science > QL Zoology
• College/School: College of Medical Veterinary and Life Sciences > School of Biodiversity, One Health & Veterinary Medicine
• Journal Name: Physiological and Biochemical Zoology
• Publisher: University of Chicago Press
• ISSN: 1522-2152
• ISSN (Online): 1537-5293
• Published Online: 27 September 2016
• Copyright Holders: Copyright © 2016 The University of Chicago
• First Published: First published in Physiological and Biochemical Zoology 89(6): 511-523
• Publisher Policy: Reproduced in accordance with the publisher copyright policy