Mitochondrial respiration and Ca2+ waves are linked during fertilization and meiosis completion

Abstract

Fertilization increases both cytosolic Ca2+ concentration and oxygen consumption in the egg but the relationship between these two phenomena remains largely obscure. We have measured mitochondrial oxygen consumption and the mitochondrial NADH concentration on single ascidian eggs and found that they increase in phase with each series of meiotic Ca2+ waves emitted by two pacemakers (PM1 and PM2). Oxygen consumption also increases in response to Ins(1,4,5)P3-induced Ca2+ transients. Using mitochondrial inhibitors we show that active mitochondria sequester cytosolic Ca2+ during sperm-triggered Ca2+ waves and that they are strictly necessary for triggering and sustaining the activity of the meiotic Ca2+ wave pacemaker PM2. Strikingly, the activity of the Ca2+ wave pacemaker PM2 can be restored or stimulated by flash photolysis of caged ATP. Taken together our observations provide the first evidence that, in addition to buffering cytosolic Ca2+, the egg's mitochondria are stimulated by Ins(1,4,5)P3-mediated Ca2+ signals. In turn, mitochondrial ATP production is required to sustain the activity of the meiotic Ca2+ wave pacemaker PM2.