Ethanol metabolism varies with hypoxia tolerance in ten cyprinid species

  • Rashpal S. Dhillon
  • Milica Mandic
  • Lili Yao
  • Zhen-Dong Cao
  • Shi-Jian Fu
  • Colin J. Brauner
  • Yuxiang S. Wang
  • Jeffrey G. Richards
Original Paper
  • 101 Downloads

Abstract

During periods of severe hypoxia or anoxia, Carassius spp. are known for their ability to produce ethanol as their anaerobic end product, which diffuses into the environment thereby reducing the osmotic and acidotic load associated with “anaerobic” glycolysis. However, the relationship between alcohol dehydrogenase (ADH) and acetaldehyde dehydrogenase (ALDH) activities, key ethanol metabolizing enzymes, and hypoxia tolerance among Carassius spp. and their closely related non-ethanol-producing cyprinids remains unclear. To address this, we quantified the activity levels of key anaerobic enzymes in liver and muscle in species of cyprinids over 48 h of severe hypoxia exposure (0.7 kPa). As predicted, muscle ADH activity was highest in the two most hypoxia-tolerant species (Carassius spp.), with very low levels present in the other species examined. However, liver ADH activities showed an inverse relationship with hypoxia tolerance, with the most hypoxia-tolerant fish having the lowest ADH activity. There was no correlation between hypoxia tolerance and ALDH and LDH activities in muscle or liver. All species produced lactate, reaching their highest levels after 8 h, but returning to near-baseline levels by 48 h of sustained exposure to hypoxia, suggesting lactate oxidation or depressed ATP demand. Liver glycogen content was not affected by 48 h hypoxia exposure in the most hypoxia-tolerant species, whereas the least tolerant species consumed the majority of the liver glycogen stores, which is probably due to the greater relative hypoxia exposure experienced by these species. Our findings that liver ADH activities were inversely related to hypoxia tolerance suggests that in all but Carassius spp., the ethanol metabolizing pathways in cyprinids is largely similar to that observed in other vertebrates and plays a role in the detoxification of ethanol. Furthermore, conservation of glycogen stores may be the result of metabolic-depressing pathways in the more tolerant species, regardless of the ability to produce ethanol, or adaptations that improve oxygen uptake to reduce metabolic demands due to hypoxia.

Keywords

Cyprinids Ethanol Aerobic Anaerobic metabolism Hypoxia Alcohol dehydrogenase Acetaldehyde dehydrogenase 

Notes

Acknowledgements

This study was funded by National Science Foundation of China (NSFC 31172096), the Key Project of the Chongqing Natural Science Foundation, and the Project of Chongqing Science and Technology Commission (CSTC, No. 2010CA1010; S.-J.F.). J.G.R. and Y.S.W. was supported by a Natural Science and Engineering Research Council (NSERC) Discovery Grants, and CJB was supported by a NSERC Discovery grant and Accelerator supplement. The authors would like to thank Matthew D. Regan and four anonymous referees for their comments during the preparation of this manuscript.

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Copyright information

© Springer-Verlag GmbH Germany 2017

Authors and Affiliations

  • Rashpal S. Dhillon
    • 1
    • 2
  • Milica Mandic
    • 3
  • Lili Yao
    • 1
  • Zhen-Dong Cao
    • 4
  • Shi-Jian Fu
    • 4
  • Colin J. Brauner
    • 2
  • Yuxiang S. Wang
    • 5
  • Jeffrey G. Richards
    • 2
  1. 1.Department of Biomolecular ChemistryUniversity of WisconsinMadisonUSA
  2. 2.Department of ZoologyUniversity of British ColumbiaVancouverCanada
  3. 3.Department of BiologyUniversity of OttawaOttawaCanada
  4. 4.Laboratory of Evolutionary Physiology and Behaviour, Chongqing Key Laboratory of Animal BiologyChongqing Normal UniversityChongqingChina
  5. 5.Department of BiologyQueen’s UniversityKingstonCanada

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