Vertical transfer of bacterial symbionts via a placental analogue in the cyclostome bryozoan Patinella verrucaria (Stenolaemata): Ultrastructural and molecular evidence.

Symbiotic associations with prokaryotes are common among marine filter-feeding invertebrates. In the almost exclusively colonial phylum Bryozoa, however, such associations have only been recorded in some species of the order Cheilostomata (class Gymnolaemata). Here we describe for the first time symbiotic bacteria in the colonies, larvae and developing ancestrulae of the bryozoan Patinella verrucaria from the order Cyclostomata (class Stenolaemata) using transmission electron and fluorescent microscopy. Ultrastructural and molecular data suggest the existence of two distinct bacterial species, both from the family Rhodobacteraceae. The presence of bacteria in all three stages of the bryozoan life cycle indicates a vertical transfer of symbionts. Both intracellular and free bacteria were recorded in the colonies, being presumably transported by amoebocytes from autozooids to the colonial incubation chamber. The bacteria are accumulated in the placental analogue and in associated cells surrounding developing embryos and larvae, and are presumably transmitted to the mature ciliated larvae during rupture of the placenta facilitated by the movements of their cilia before and/or during larval release. Thus, the nourishing function of the placenta is complemented by the symbiont transfer, which can be regarded as an example of extension of functions. This is the first example of a placenta providing bacterial infection to the progeny in invertebrates.