Cockroach bacteriocytes migrate into the ovaries for vertical transmission of the bacterial endosymbiont Blattabacterium

Abstract

Diverse insect groups are obligatorily associated with and dependent on specific microorganisms as essential mutualistic partners that are usually maintained in specialized cells or organs, called bacteriocytes or symbiotic organs. Many organisms with symbiotic microorganisms have developed elaborate vertical transmission mechanisms, which are thought to be important for the evolution of intimate symbiotic relationships with microorganisms. One such case is the cockroach-Blattabacterium endosymbiosis, in which the symbiotic bacteria have been evolutionarily conserved and co-speciated with the host insects with stable vertical symbiont transmission via ovarial passage. While classical histological descriptions and recent electron microscopic observations have reported the vertical symbiont transmission processes in some cockroach-Blattabacterium associations, the full picture of the infection dynamics has not been fully understood. In this study, we conducted detailed histological and cytological observations of the localization of the bacteriocytes and the symbiotic bacteria during the postembryonic development of the German cockroach Blattella germanica. We found that the symbiont-filled bacteriocytes migrate into and associate with nymphal ovaries and are subsequently eliminated from adult ovaries, suggesting that symbiont infection to the ovaries may only occur during nymphal stages. We also found that the symbiotic bacteria are localized in the space between each oocyte and surrounding follicle cells, the symbiont-localized space is interconnected between neighboring oocytes, and therefore the symbiotic bacteria can move across oocytes within the same ovariole, suggesting the possibility that the symbiont-infected oocytes may serve as the source of symbiont supply to developing young oocytes upstream in the same ovariole. Based on these observations, we provide a hypothesis as to how the postembryonic developmental dynamics of the bacteriocytes are integrated into the vertical symbiont transmission and functioning in the cockroach-Blattabacterium endosymbiosis.