Intraspecific variation and plasticity in mitochondrial oxygen binding affinity as a response to environmental temperature

Dillon J Chung,P R Morrison,C J Brauner,P M Schulte,H J Bryant,E Jung

doi:10.1038/s41598-017-16598-6

Dillon J Chung, P R Morrison + Show 4 more

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https://doi.org/10.1038/s41598-017-16598-6

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Journal: Scientific Reports	Publication Date: Nov 24, 2017
Citations: 24	License type: open-access

Affiliation: University of British Columbia

Abstract

Mitochondrial function has been suggested to underlie constraints on whole-organism aerobic performance and associated hypoxia and thermal tolerance limits, but most studies have focused on measures of maximum mitochondrial capacity. Here we investigated whether variation in mitochondrial oxygen kinetics could contribute to local adaptation and plasticity in response to temperature using two subspecies of the Atlantic killifish (Fundulus heteroclitus) acclimated to a range of temperatures (5, 15, and 33 °C). The southern subspecies of F. heteroclitus, which has superior thermal and hypoxia tolerances compared to the northern subspecies, exhibited lower mitochondrial O2 P50 (higher O2 affinity). Acclimation to thermal extremes (5 or 33 °C) altered mitochondrial O2 P50 in both subspecies consistent with the effects of thermal acclimation on whole-organism thermal tolerance limits. We also examined differences between subspecies and thermal acclimation effects on whole-blood Hb O2-P50 to assess whether variation in oxygen delivery is involved in these responses. In contrast to the clear differences between subspecies in mitochondrial O2-P50 there were no differences in whole-blood Hb-O2 P50 between subspecies. Taken together these findings support a general role for mitochondrial oxygen kinetics in differentiating whole-organism aerobic performance and thus in influencing species responses to environmental change.

Highlights

Both ambient temperature and O2 availability vary widely across the biosphere and this has profound implications for the geographic distributions of aquatic organisms[1,2]
These effects on Mito-P50 are consistent with intraspecific variation and the effects of thermal acclimation on whole-organism thermal and hypoxia tolerance[25]
We propose that variation in Mito-P50 partially underlies intraspecific variation in hypoxia tolerance (Fig. 125)

Summary

Introduction

Both ambient temperature and O2 availability vary widely across the biosphere and this has profound implications for the geographic distributions of aquatic organisms[1,2]. Given the relationship between ambient temperature and aerobic metabolism, prolonged thermal stress likely alters mitochondrial function and an investigation of temperature effects on Mito-P50 is necessary[3,4,6] To address this question, here we utilize F. heteroclitus, a eurythermal teleost found in estuarine salt marshes along a large latitudinal range that spans a steep thermal gradient [(Northern Florida, USA (mean monthly southern temperature range Sapelo Island, GA, USA: 11–30 °C22) to Nova Scotia, Canada (mean monthly northern temperature range 3–11 °C Wells Inlet, ME, USA22)]. Northern and southern F. heteroclitus subspecies exhibit variation in thermal and hypoxia tolerance that is consistent with apparent adaptation to their local environments[24,25] This species recruits a wide array of physiological responses to thermal stress, including altered mitochondrial function[12,15,25,26,27]. We assessed intraspecific variation and thermal acclimation effects on hemoglobin (Hb) O2-P50, as there is some evidence of intraspecific variation in this parameter in F. heteroclitus[28] and any variation in this parameter could result in changes in PO2 gradients between the circulatory system and the mitochondrion

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