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

Abstract

Global warming is intensifying interest in the physiological consequences of temperature change in ectotherms, but we still have a relatively poor understanding of the effects of temperature on early life stages. This study determined how embryonic temperature (T E ) affects development and the activity of metabolic enzymes in the swimming muscle of zebrafish. Embryos developed successfully to hatching (survival ≥88%) from 22 to 32°C, but suffered sharp increases in mortality outside of this range. Embryos that were incubated until hatching at a control T E (27°C) or near the extremes for successful development (22 or 32°C) were next raised to adulthood under control conditions at 27°C. Growth trajectories after hatching were altered in the 22°C and 32°C T E groups compared with 27°C T E controls, but growth slowed after 3 months of age in all groups. Maximal enzyme activities of cytochrome c oxidase (COX), citrate synthase (CS), hydroxyacyl-coA dehydrogenase (HOAD), pyruvate kinase (PK) and lactate dehydrogenase (LDH) were measured across a range of assay temperatures (22, 27, 32 and 36°C) in adults from each T E group that were acclimated to 27 or 32°C. Substrate affinities (K m ) were also determined for COX and LDH. In adult fish acclimated to 27°C, COX and PK activities were higher in 22°C and 32°C T E groups than in 27°C T E controls, and the temperature optimum for COX activity was higher in the 32°C T E group than in the 22°C T E group. Warm acclimation reduced COX, CS and/or PK activities in the 22 and 32°C T E groups, possibly to compensate for thermal effects on molecular activity. This response did not occur in the 27°C T E controls, which instead increased LDH and HOAD activities. Warm acclimation also increased thermal sensitivity (Q 10 ) of HOAD to cool temperatures across all T E groups. We conclude that the temperature experienced during early development can have a persistent impact on energy metabolism pathways and acclimation capacity in later life.

Phenotypic plasticity induced using high ambient temperature during embryogenesis in domesticated zebrafish, Danio rerio

“…High and low temperatures (32°C and 22°C compared to the control at 27°C) during embryonic development in zebrafish have an influence on the acclimation response, which has an influence on energy metabolism and swimming performance in later life stages, which is controlled by expression of several metabolic genes (Scott & Johnston, ) in swimming muscle (Schnurr, Yin, & Scott, ). In the study of Schnurr et al (), temperature treatment during early life in zebrafish resulted in a reduction in body mass and standard length until 12 weeks of age. However, in the high‐temperature group, a significant growth rate was observed beyond this age and the body length was higher than the control group (Schnurr et al, ), which is in agreement with our study.…”

Distinct physiological strategies are used to cope with constant hypoxia and intermittent hypoxia in killifish (Fundulus heteroclitus)

“…The maximal activities of several enzymes were assayed using standard methods (Bears et al, 2006;Schnurr et al, 2014). The frozen muscle, liver, heart and brain samples were weighed and homogenized on ice in 20 volumes of homogenization buffer (20 mmol l −1 Hepes, 1 mmol l −1 sodium EDTA and 0.1% Triton X-100) at pH 7.0.…”

Physiological tradeoffs may underlie the evolution of hypoxia tolerance and exercise performance in sunfish (Centrarchidae)

“…We studied wildcaught fish that were well acclimated to common conditions in the lab, which eliminated the influence of reversible plasticity on our results, but this approach cannot eliminate the differences between species that are caused by irreversible developmental plasticity. Developmental plasticity can have a strong influence on adult physiology (West-Eberhard, 2003; Scott and Johnston, 2012; Schnurr et al, 2014), and developmental hypoxia in particular can have persistent effects on hypoxia tolerance, the gas-exchange organs, and the activities of metabolic enzymes in several tissues (Crocker et al, 2013;Blank and Burggren, 2014;Robertson et al, 2014). Exposure of parent zebrafish to hypoxia has also been shown to improve the hypoxia tolerance of their offspring (Ho and Burggren, 2012), suggesting that trans-generational effects could have also influenced some of our observations.…”

“…The maximal activities of several enzymes were assayed at 25°C using standard methods that have been previously described (Schnurr et al, 2014;Borowiec et al, 2015) with a SpectraMax Plus 384 microplate reader (Molecular Devices, Sunnyvale, CA, USA). Tissue was homogenized on ice in 20 volumes of homogenization buffer (20 mmol l −1 Hepes, 1 mmol l −1 EDTA and 0.1% Triton X-100) at pH 7.0.…”