Mitochondrial biogenesis in cold-bodied fishes

Abstract

SummaryMitochondrial biogenesis is induced in response to cold temperature in many organisms. The effect is particularly pronounced in ectotherms such as fishes, where acclimation to cold temperature increases mitochondrial density. Some polar fishes also have exceptionally high densities of mitochondria. The net effect of increasing mitochondrial density is threefold. First, it increases the concentration of aerobic metabolic enzymes per gram of tissue, maintaining ATP production. Second, it elevates the density of mitochondrial membrane phospholipids, enhancing rates of intracellular oxygen diffusion. Third, it reduces the diffusion distance for oxygen and metabolites between capillaries and mitochondria. Although cold-induced mitochondrial biogenesis has been well documented in fishes, little is known about the molecular pathway governing it. In mammals, the co-transcriptional activator peroxisome proliferator-activated receptor gamma coactivator 1 alpha (PGC-1) is thought to coordinate the three components of mitochondrial biogenesis: the synthesis of mitochondrial proteins, the synthesis of phospholipids and the replication of mitochondrial DNA. Some components of the mitochondrial biogenic pathway are conserved between fishes and mammals, yet the pathway appears more versatile in fishes. In some tissues of cold-acclimated fishes, the synthesis of mitochondrial proteins increases in the absence of an increase in phospholipids, whereas in some polar fishes, densities of mitochondrial phospholipids increase in the absence of an increase in proteins. The ability of cold-bodied fishes to fine-tune the mitochondrial biogenic pathway may allow them to modify mitochondrial characteristics to meet the specific needs of the cell, whether it is to increase ATP production or enhance oxygen diffusion.

Mechanisms and costs of mitochondrial thermal acclimation in a eurythermal killifish (Fundulus heteroclitus)

“…For example, previous studies have demonstrated low-temperature acclimation effects on mitochondrial enzyme function (Fangue et al, 2009;Kraffe et al, 2007), inner mitochondrial membrane (IMM) composition (for review see : Guderley, 2004;Grim et al, 2010;Kraffe et al, 2007), and mitochondrial volume density (Dhillon and Schulte, 2011;Egginton and Johnston, 1984; for review see: O'Brien, 2011). Although beneficial at the acclimation temperature, changes in mitochondrial physiology associated with thermal acclimation may result in dysfunction during acute thermal shifts (to previously unstressful temperatures), which may be a potential mechanism underlying shifts in thermal limits.…”

Intraspecific variation in the thermal plasticity of mitochondria in killifish

“…Mitochondria are of particular significance in the study of cold temperature acclimation, as lower temperatures reduce the mitochondria's ability to produce ATP via oxidative phosphorylation, both directly at the level of the mitochondrion and indirectly through limitations on oxygen transport. Thus, acclimation or adaptation to cold temperature requires organisms to counter a potential ATP deficit by enhancing processes involved in oxygen delivery and oxidative capacity (O'Brien, 2011).…”

“…For example, cold-induced angiogenesis, particularly in the mitochondria-rich red muscle of fishes, can offset reduced diffusion, in addition to providing other benefits such as improved waste removal (Hoppeler et al, 1981;Johnston, 1982;Egginton and Cordiner, 1997;Egginton et al, 2000;Mathieu-Costello et al, 2005;O'Brien, 2011). Another common response during cold temperature acclimation is the proliferation and catabolization of lipids (Jones and Sidell, 1982;Egginton and Sidell, 1989;Sidell and Moerland, 1989;O'Brien, 2011). Lipid droplets in the muscle fibers increase the solubility coefficient of oxygen at low temperatures (Egginton and Sidell, 1989;Sidell, 1998) and provide a preferred fuel substrate.…”

Temperature during embryonic development has persistent effects on metabolic enzymes in the muscle of zebrafish

“…Johnston and Maitland, 1980;Egginton and Sidell, 1989;McClelland et al, 2006;Orczewska et al, 2010). This response is thought to improve cellular function by counteracting the kinetic effects of temperature on the catalytic rates of mitochondrial enzymes or on the rates of oxygen/metabolite diffusion (Hubley et al, 1997;Guderley, 2004;Kinsey et al, 2011;O'Brien, 2011). However, the presence and magnitude of metabolic temperature acclimation in adult fish depends on the magnitude of temperature change and can vary between populations and species Dhillon and Schulte, 2011).…”