Cardiac adaptations to low temperature in non-polar teleost fish

SUMMARYIn the eurythermal cuttlefish Sepia officinalis, performance depends on hearts that ensure systemic oxygen supply over a broad range of temperatures. We therefore aimed to identify adjustments in energetic cardiac capacity and underlying mitochondrial function supporting thermal acclimation and adaptation that could be crucial for the cuttlefishʼs competitive success in variable environments. Two genetically distinct cuttlefish populations were acclimated to 11, 16 and 21°C. Subsequently, skinned and permeabilised heart fibres were used to assess mitochondrial functioning by means of high-resolution respirometry and a substrate-inhibitor protocol, followed by measurements of cardiac citrate synthase and cytosolic enzyme activities. Temperate English Channel cuttlefish had lower mitochondrial capacities but larger hearts than subtropical Adriatic cuttlefish. Warm acclimation to 21°C decreased mitochondrial complex I activity in Adriatic cuttlefish and increased complex IV activity in English Channel cuttlefish. However, compensation of mitochondrial capacities did not occur during cold acclimation to 11°C. In systemic hearts, the thermal sensitivity of mitochondrial substrate oxidation was high for proline and pyruvate but low for succinate. Oxygen efficiency of catabolism rose as temperature changed from 11 to 21°C via shifts to oxygen-conserving oxidation of proline and pyruvate and via reduced relative proton leak. The changes observed for substrate oxidation, mitochondrial complexes, relative proton leak and heart mass improve energetic efficiency and essentially seem to extend tolerance to high temperatures and reduce associated tissue hypoxia. We conclude that cuttlefish sustain cardiac performance and, thus, systemic oxygen delivery over short-and long-term changes of temperature and environmental conditions by multiple adjustments in cellular and mitochondrial energetics. Supplementary material available online at

Section: Discussion Evolutionary Adaptationmentioning

confidence: 99%

Section: Discussion Evolutionary Adaptationmentioning

confidence: 99%

Mitochondrial dynamics underlying thermal plasticity of cuttlefish (Sepia officinalis) hearts

Oellermann

Pörtner

Mark

2012

“…Cardiac hypertrophy is often associated with cold-acclimation/ adaptation (Driedzic et al, 1996;Farrell, 1996;Axelsson et al, 1998;Aho and Vornanen, 2001), and has been previously reported to occur in Atlantic cod. Foster et al (Foster et al, 1993) showed that the RVM of juvenile cod acclimated to 5°C for 43days was 24% greater than for 15°C-acclimated fish.…”

Section: Temperature Effects On Cardiac Functionmentioning

confidence: 92%

Atlantic cod (Gadus morhua L.) in situ cardiac performance at cold temperatures: long-term acclimation, acute thermal challenge and the role of adrenaline

Lurman

Petersen

Gamperl

2012

SUMMARYThe resting and maximum in situ cardiac performance of Newfoundland Atlantic cod (Gadus morhua) acclimated to 10, 4 and 0°C were measured at their respective acclimation temperatures, and when acutely exposed to temperature changes: i.e. hearts from 10°C fish cooled to 4°C, and hearts from 4°C fish measured at 10 and 0°C. Intrinsic heart rate (f H ) decreased from 41beatsmin -1 at 10°C to 33beatsmin -1 at 4°C and 25beatsmin -1 at 0°C. However, this degree of thermal dependency was not reflected in maximal cardiac output (Q max values were ~44, ~37 and ~34mlmin -1 kg -1 at 10, 4 and 0°C, respectively). Further, cardiac scope showed a slight positive compensation between 4 and 0°C (Q 10 1.7), and full, if not a slight over compensation between 10 and 4°C (Q 10 0.9). The maximal performance of hearts exposed to an acute decrease in temperature (i.e. from 10 to 4°C and 4 to 0°C) was comparable to that measured for hearts from 4°C-and 0°C-acclimated fish, respectively. In contrast, 4°C-acclimated hearts significantly out-performed 10°C-acclimated hearts when tested at a common temperature of 10°C (in terms of both Q max and power output). Only minimal differences in cardiac function were seen between hearts stimulated with basal (5nmoll ) levels of adrenaline, the effects of which were not temperature dependent. These results: (1) show that maximum performance of the isolated cod heart is not compromised by exposure to cold temperatures; and (2) support data from other studies, which show that, in contrast to salmonids, cod cardiac performance/myocardial contractility is not dependent upon humoral adrenergic stimulation.

“…This indicates that acclimation to 4°C did not cause cardiac hypertrophy. Although several studies describe hypertrophy in trout cardiac muscle in response to cold acclimation (Graham and Farrell, 1989;Klaiman et al, 2011;Vornanen et al, 2005), this phenomenon is not universally reported (Driedzic et al, 1996;Gamperl and Farrell, 2004). It has been proposed that other factors may be involved in triggering the hypertrophic response, including seasonal changes in photoperiod and thyroid hormones (Tiitu and Vornanen, 2003;Gamperl and Farrell, 2004).…”

Section: Variation In Morphological Remodellingmentioning

confidence: 99%

Cold acclimation increases cardiac myofilament function and ventricular pressure generation in trout

Klaiman

Pyle

Gillis

2014

Reducing temperature below the optimum of most vertebrate hearts impairs contractility and reduces organ function. However, a number of fish species, including the rainbow trout, can seasonally acclimate to low temperature. Such ability requires modification of physiological systems to compensate for the thermodynamic effects of temperature on biological processes. The current study tested the hypothesis that rainbow trout compensate for the direct effect of cold temperature by increasing cardiac contractility during cold acclimation. We examined cardiac contractility, following thermal acclimation (4, 11 and 17°C), by measuring the Ca 2+ sensitivity of force generation by chemically skinned cardiac trabeculae as well as ventricular pressure generation using a modified Langendorff preparation. We demonstrate, for the first time, that the Ca 2+ sensitivity of force generation was significantly higher in cardiac trabeculae from 4°C-acclimated trout compared with those acclimated to 11 or 17°C, and that this functional change occurred in parallel with a decrease in the level of cardiac troponin T phosphorylation. In addition, we show that the magnitude and rate of ventricular pressure generation was greater in hearts from trout acclimated to 4°C compared with those from animals acclimated to 11 or 17°C. Taken together, these results suggest that enhanced myofilament function, caused by modification of existing contractile proteins, is at least partially responsible for the observed increase in pressure generation after acclimation to 4°C. In addition, by examining the phenotypic plasticity of a comparative model we have identified a strategy, used in vivo, by which the force-generating capacity of cardiac muscle can be increased.