Mitochondrial physiology of diapausing and developing embryos of the annual killifish Austrofundulus limnaeus: implications for extreme anoxia tolerance.
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 VO(2), 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.
Duerr
Jeffrey M
JM
Department of Biology, George Fox University, Newberg, OR 97132, USA. jduerr@georgefox.edu
Podrabsky
Jason E
JE
D000222:Adaptation, Physiological; D000818:Animals; D002458:Cell Fractionation / Q000379:methods; D045222:Electron Transport Chain Complex Proteins / Q000378:metabolism; D004625:Embryo, Nonmammalian / Q000502:physiology*; D047108:Embryonic Development; D000860:Hypoxia / Q000503:physiopathology*; D007695:Killifishes / Q000196:embryology* / Q000254:growth & development / Q000502:physiology*; D008018:Life Cycle Stages / Q000502:physiology; D008928:Mitochondria / Q000378:metabolism*; D008930:Mitochondria, Liver / Q000378:metabolism; D010085:Oxidative Phosphorylation; D010101:Oxygen Consumption; D056152:Respiratory Rate; D013312:Stress, Physiological
D045222:Electron Transport Chain Complex Proteins
Biochim Biophys Acta. 2010 Mar;1800(3):205-12
19409964
Trends Biochem Sci. 2006 Jan;31(1):26-34
16337125
J Exp Biol. 2009 Jul;212(Pt 14):2248-53
19561214
Comp Biochem Physiol B Biochem Mol Biol. 2006 Nov-Dec;145(3-4):296-305
17070716
Am J Physiol Heart Circ Physiol. 2004 May;286(5):H1633-41
14693685
Biochem J. 1994 Jan 1;297 ( Pt 1):27-9
8280106
FEBS Lett. 1997 Oct 13;416(1):15-8
9369223
Biosci Rep. 1997 Feb;17(1):23-31
9171918
Proc Natl Acad Sci U S A. 2000 Jul 18;97(15):8670-4
10890886
J Exp Biol. 2006 Jul;209(Pt 14):2678-85
16809458
Methods Enzymol. 1974;32:392-406
4155469
Am J Physiol Regul Integr Comp Physiol. 2002 Feb;282(2):R372-82
11792646
Insect Biochem Mol Biol. 2008 Mar;38(3):367-73
18252250
Biochim Biophys Acta. 2003 Jun 5;1604(2):77-94
12765765
J Exp Biol. 2002 Aug;205(Pt 15):2287-96
12110662
Comp Biochem Physiol C Toxicol Pharmacol. 2003 Jan;134(1):79-90
12524020
Biochim Biophys Acta. 1975 Jan 31;376(1):13-26
123764
Biochem J. 2005 Dec 1;392(Pt 2):353-62
16076285
J Exp Zool. 1972 Dec;182(3):389-414
4674089
J Comp Physiol B. 2007 Oct;177(7):743-52
17576568
Clin Chem. 2007 Apr;53(4):729-34
17332151
Am J Physiol Regul Integr Comp Physiol. 2003 May;284(5):R1306-13
12676751
Biochem J. 2000 Oct 15;351 Pt 2:307-11
11023814
J Exp Biol. 2000 May;203(Pt 9):1469-76
10751162
J Exp Biol. 2007 Jul;210(Pt 13):2253-66
17575031
Comp Biochem Physiol B. 1993 Dec;106(4):889-93
8299351
Physiol Rev. 2004 Jan;84(1):277-359
14715917
Nature. 1955 Jun 25;175(4469):1120-1
14394122
J Biol Chem. 1982 Mar 25;257(6):2754-7
7061448
Eur J Biochem. 1990 Mar 10;188(2):313-9
2156698
Physiol Biochem Zool. 2004 May-Jun;77(3):366-77
15286911
Am J Physiol. 1996 Oct;271(4 Pt 1):C1380-9
8897845
Proc Natl Acad Sci U S A. 1997 Feb 18;94(4):1166-71
9037024
J Exp Biol. 2008 Jun;211(Pt 12):1911-8
18515721
J Exp Zool. 1972 Nov;182(2):143-67
5079083
Biochim Biophys Acta. 2008 Jul-Aug;1777(7-8):719-28
18455500
J Biol Chem. 1974 Mar 10;249(5):1417-22
4274152
Biochem Soc Trans. 2005 Nov;33(Pt 5):897-904
16246006
Am J Physiol Regul Integr Comp Physiol. 2007 Nov;293(5):R1833-45
17804585
Hypertension. 2009 Jun;53(6):885-92
19398655
J Exp Biol. 2000 Dec;203(Pt 23):3603-12
11060221
Free Radic Biol Med. 2005 Jan 1;38(1):12-23
15589367
J Exp Biol. 1999 Oct;202 (Pt 19):2567-80
10482717
Am J Physiol. 1998 Dec;275(6):R1977-82
9843887
Biochem J. 1980 Jan 15;186(1):21-33
7370008
Biochem J. 1987 Apr 15;243(2):499-505
2820383
J Exp Biol. 2009 Feb;212(Pt 4):514-22
19181899