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Mitochondrial physiology of diapausing and developing embryos of the annual killifish Austrofundulus limnaeus: implications for extreme anoxia tolerance

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Abstract

Diapausing embryos of the annual killifish Austrofundulus limnaeus have the highest reported anoxia tolerance of any vertebrate and previous studies indicate modified mitochondrial physiology likely supports anoxic metabolism. Functional mitochondria isolated from diapausing and developing embryos of the annual killifish exhibited VO2, respiratory control ratios (RCR), and P:O ratios consistent with those obtained from other ectothermic vertebrate species. Reduced oxygen consumption associated with dormancy in whole animal respiration rates are correlated with maximal respiration rates of mitochondria isolated from diapausing versus developing embryos. P:O ratios for developing embryos were similar to those obtained from adult liver, but were diminished in mitochondria from diapausing embryos suggesting decreased oxidative efficiency. Proton leak in adult liver corresponded with that of developing embryos but was elevated in mitochondria isolated from diapausing embryos. In metabolically suppressed diapause II embryos, over 95% of the mitochondrial oxygen consumption is accounted for by proton leak across the inner mitochondrial membrane. Decreased activity of mitochondrial respiratory chain complexes correlates with diminished oxidative capacity of isolated mitochondria, especially during diapause. Respiratory complexes exhibited suppressed activity in mitochondria with the ATP synthase exhibiting the greatest inhibition during diapause II. Mitochondria isolated from diapause II embryos are not poised to produce ATP, but rather to shuttle carbon and electrons through the Kreb’s cycle while minimizing the generation of a proton motive force. This particular mitochondrial physiology is likely a mechanism to avoid production of reactive oxygen species during large-scale changes in flux through oxidative phosphorylation pathways associated with metabolic transitions into and out of dormancy and anoxia.

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Acknowledgments

This work was supported by National Science Foundation grant IOB-0344578 to JEP and a Faculty Research Development Grant from George Fox University to JMD. The authors also wish to thank S.S. Hillman for helpful discussions and technical advice.

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Authors and Affiliations

  1. Department of Biology, George Fox University, Newberg, OR, 97132, USA

    Jeffrey M. Duerr

  2. Department of Biology, Portland State University, P.O. Box 751, Portland, OR, 97207, USA

    Jason E. Podrabsky

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  1. Jeffrey M. Duerr
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Correspondence to Jeffrey M. Duerr.

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Communicated by H. V. Carey.

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Duerr, J.M., Podrabsky, J.E. Mitochondrial physiology of diapausing and developing embryos of the annual killifish Austrofundulus limnaeus: implications for extreme anoxia tolerance. J Comp Physiol B 180, 991–1003 (2010). https://doi.org/10.1007/s00360-010-0478-6

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