All for one – changes in mitochondrial morphology and activity during syncytial oogenesis

Abstract The syncytial groups of germ cells (germ-line cysts) forming in ovaries of clitellate annelids are an attractive model to study mitochondrial stage-specific changes. Using transmission electron microscopy, serial block-face scanning electron microscopy, and fluorescent microscopy, we analyzed the mitochondria distribution and morphology and the state of membrane potential in female cysts in Enchytraeus albidus. We visualized in 3D at the ultrastructural level mitochondria in cysts at successive stages: 2-celled, 4-celled, 16-celled cysts, and cyst in advanced oogenesis. We found that mitochondria form extensive aggregates – they are fused and connected into large and branched mitochondrial networks. The most extensive networks are formed with up to 10,000 fused mitochondria, whereas individual organelles represent up to 2% of the total mitochondrial volume. We classify such morphology of mitochondria as a dynamic hyperfusion state, and suggest that it can maintain their high activity and intensifies the process of cellular respiration within the syncytial cysts. We found some individual mitochondria undergoing degradation, which implies that damaged mitochondria are removed from networks for their final elimination. As it was shown that growing oocytes possess less active mitochondria than the nurse cells, it suggests that the high activity of mitochondria in the nurse cells and their dynamic hyperfusion state serve the needs of the growing oocyte. Additionally, we measured by calorimetry the total antioxidant capacity of germ-line cysts in comparison to somatic tissue, and it suggests that antioxidative defense systems, together with mitochondrial networks, can effectively protect germ-line mitochondria from damage.