Maternal Inheritance of a Single Somatic Animal Cell Displayed by the Bacteriocyte in the Whitefly Bemisia tabaci

Bacteriocytes are insect cells harboring symbiotic bacteria that are required by their insect host and are transmitted vertically via the female ovary [1]. In most insect groups, the bacteria are released from the bacteriocytes and transferred to the ovary [2, 3], but in whiteflies, maternal bacteriocytes migrate to each egg [4-6], where they have been reported to lyse, releasing the symbionts [1]. To investigate bacteriocyte inheritance in whiteflies further, we applied microsatellite genotyping and genomic analysis to a genetically diverse population of Bemisia tabaci, and we observed the fate of the bacteriocyte in embryos. Surprisingly, the microsatellite profile of the bacteriocytes was uniform, and insect cross experiments demonstrated that the bacteriocytes have a stable genotype that differs from the genotype of the insect head (which lacks bacteriocytes). Comparative genomic analysis indicates that genomes of the bacteriocyte and whitefly head are distinct. Interestingly, the bacterioyte genome contains the canonical arthropod telomere repeats TTAGG, and the bacteriocytes express telomere maintenance genes that may underlie cellular immortality in animal cells [7]. Microscopy observations confirmed that a single bacteriocyte transmitted to each egg is retained and divides once just before egg hatch, yielding two bacteriocytes in the neonate insect. These data demonstrate the maternal inheritance of an absolutely required somatic insect cell, violating the developmental separation of germline and soma [8, 9]. Future investigation on the mechanism and phylogenetic distribution of maternally inherited bacteriocytes will shed light on the developmental origins and evolutionary diversification of bacteriocytes [10] and the processes underlying cellular immortality [11].