High mitochondrial densities in the hearts of Antarctic icefishes are maintained by an increase in mitochondrial size rather than mitochondrial biogenesis

Abstract

SUMMARYWe investigated the molecular mechanisms regulating differences in mitochondrial volume density between heart ventricles of Antarctic notothenioids that vary in the expression of hemoglobin (Hb) and myoglobin (Mb). In mammals, peroxisome proliferatoractivated receptor γ coactivator-1α (PGC-1α) and nuclear respiratory factor 1 (NRF-1) stimulate mitochondrial biogenesis and maintain mitochondrial density in muscle tissues. We hypothesized that these factors would also maintain mitochondrial density in the hearts of Antarctic notothenioids. The percent cell volume occupied by mitochondria is significantly lower in hearts of the red-blooded notothenioid Notothenia coriiceps (18.18±0.69%) in comparison with those of the icefish Chaenocephalus aceratus (36.53±2.07%), which lacks both Hb and cardiac Mb. Mitochondrial densities are not different between hearts of N. coriiceps and Chionodraco rastrospinosus, which lacks Hb, but whose heart expresses Mb. Despite differences in mitochondrial volume density between hearts of N. coriiceps and C. aceratus, the levels of transcripts of the genes encoding PGC-1α, NRF-1 and citrate synthase, and the copy number of mitochondrial DNA do not differ. Our results indicate that the high mitochondrial densities in hearts of C. aceratus may result from an increase in organelle size. The surface-to-volume ratio of mitochondria from N. coriiceps is 1.9-fold greater than that of mitochondria from C. aceratus. In addition, the levels of PGC-1α correlate with mitochondrial density in muscle tissues of notothenioids possessing mitochondria of similar size and morphology. Finally, the levels of PGC-1α are 4.6-fold higher in the aerobic pectoral adductor muscle in comparison with the glycolytic skeletal muscle of N. coriiceps. The potential physiological significance of an increase in mitochondrial size in hearts of Antarctic icefishes is discussed.

Warm-preconditioning protects against acute heat-induced respiratory dysfunction and delays bleaching in a symbiotic sea anemone

“…Assay linearity was tested across a range of sample protein concentrations (0.1-2.0 mg ml −1 ) and specificity of the SDH and CCO assays was confirmed by using the specific inhibitors malonate (10 mmol l −1 ) and KCN (300 μmol l −1 ), respectively. Changes in tissue aerobic capacity can stem from changes in mitochondrial size and/or density as well as altered function of individual mitochondria (Somero and Hochachka, 2002;Urschel and O'Brien, 2008). Thus, in addition to calculating biomassnormalised (specific) enzyme activity, we normalised all mETC complex activities to that of CS, a reliable enzymatic indicator of mitochondrial density (Holloszy et al, 1970;Spinazzi et al, 2012;Vigelsø et al, 2014).…”

“…With the TCA cycle acting as the 'hub' of cellular aerobic metabolism (Somero and Hochachka, 2002), biomass-normalised activity of its gate-keeper enzyme citrate synthase (CS) is a useful marker of tissue mitochondrial density and aerobic capacity (e.g. Srere, 1969;Urschel and O'Brien, 2008;Vigelsø et al, 2014;Hawkins et al, 2016a). TCA cyclederived NADH and FADH 2 drive oxidative phosphorylation at the mETC, which comprises several multi-protein complexes embedded in the inner mitochondrial membrane (IMM; see Fig.…”

Exposure to critical thermal maxima causes oxidative stress in hearts of white- but not red-blooded Antarctic notothenioid fishes

“…Degenerate nucleotides are indicated by N, R and Y (NA or C or G or T; RA or G; YC or T). Degenerate and gene-specific primers for EF-1 were published previously (Urschel and OʼBrien, 2008). …”

Phenylhydrazine-induced anemia causes nitric-oxide-mediated upregulation of the angiogenic pathway in Notothenia coriiceps

“…Tissues of hemoglobinless icefishes display both dramatically greater mitochondrial densities (O'Brien and Sidell, 2000) and vascular densities (Wujcik et al, 2006) than those of their red-blooded relatives. Yet, despite the apparently higher level of NO in icefish, there is no significant difference in expression of mitochondrial biogenesis genes in ventricles and angiogenesis genes in retinae between red-and white-blooded adult notothenioids (Urschel and O'Brien, 2008;Beers et al, 2010). Feedback inhibition could be responsible for lack of upregulation in the genes, once stable well-oxygenated phenotypes are attained.…”