Cellular mechanism for selective vertical transmission of an obligate insect symbiont at the bacteriocyte–embryo interface

Abstract

Many insects are associated with obligate symbiotic bacteria, which are localized in specialized cells called bacteriocytes, vertically transmitted through host generations via ovarial passage, and essential for growth and reproduction of their hosts. Although vertical transmission is pivotal for maintenance of such intimate host–symbiont associations, molecular and cellular mechanisms underlying the process are largely unknown. Here we report a cellular mechanism for vertical transmission of the obligate symbiont Buchnera in the pea aphid Acyrthosiphon pisum . In the aphid body, Buchnera cells are transmitted from maternal bacteriocytes to adjacent blastulae at the ovariole tips in a highly coordinated manner. By making use of symbiont-manipulated strains of A. pisum , we demonstrated that the facultative symbiont Serratia is, unlike Buchnera , not transmitted from maternal bacteriocytes to blastulae, suggesting a specific mechanism for Buchnera transmission. EM observations revealed a series of exo-/endocytotic processes operating at the bacteriocyte–blastula interface: Buchnera cells are exocytosed from the maternal bacteriocyte, temporarily released to the extracellular space, and endocytosed by the posterior syncytial cytoplasm of the blastula. These results suggest that the selective Buchnera transmission is likely attributable to Buchnera -specific exocytosis by the maternal bacteriocyte, whereas both Buchnera and Serratia are nonselectively incorporated by the endocytotic activity of the posterior region of the blastula. The sophisticated cellular mechanism for vertical transmission of Buchnera must have evolved to ensure the obligate host–symbiont association, whereas facultative symbionts like Serratia may coopt the endocytotic component of the mechanism for their entry into the host embryos.

A novel intracellular mutualistic bacterium in the invasive antCardiocondyla obscurior

“…Maternal transmission of Westeberhardia occurs through a different process than described for other endosymbionts (Koga et al, 2012;Balmand et al, 2013). In adult queens, Westeberhardia is localized in ovarial syncytial nurse cells, which originate from the same germline stem cell as the oocyte and are responsible for provisioning of the oocyte with metabolites.…”

Signatures of host/symbiont genome coevolution in insect nutritional endosymbioses

“…When aphids reproduce sexually, they are oviparous; when they reproduce asexually, they are viviparous. The ease of maintaining a continuous supply of asexual embryos vs. the difficulty of maintaining a steady supply of sexually produced embryos means that most recent work has focused on Buchnera transmission during asexual reproduction (53). That said, during both sexual and asexual reproduction in A. pisum it is clear that Buchnera do not localize to the germarium at any point in development and that each developing oocyte (in the case of sexual reproduction) or embryo (in the case of asexual reproduction) receive Buchnera from a single maternal bacteriocyte cell (13,(53)(54)(55).…”

Swapping symbionts in spittlebugs: evolutionary replacement of a reduced genome symbiont

“…Replacing an ancestral symbiont with a new one is a potential solution: symbiont services, such as essential amino-acid biosynthesis, are ubiquitous capabilities in bacteria. But, as a result of host-symbiont coadaptation, symbiont cells are intimately involved in host development (for example, Braendle et al, 2003;Koga et al, 2012) such that their sudden removal causes lethal developmental disruption. Nonetheless, several cases are known in which an insect host lineage has acquired a new symbiont, which has entirely replaced an ancestral one (for example, Lefèvre et al, 2004;Conord et al, 2008;Toenshoff et al, 2012;Toju et al, 2013) or has persisted along with the ancestral symbiont while assuming a subset of its functions (for example, Lamelas et al, 2011).…”