Wolbachia Utilizes Host Microtubules and Dynein for Anterior Localization in the Drosophila Oocyte

Abstract

To investigate the role of the host cytoskeleton in the maternal transmission of the endoparasitic bacteria Wolbachia, we have characterized their distribution in the female germ line of Drosophila melanogaster. In the germarium, Wolbachia are distributed to all germ cells of the cyst, establishing an early infection in the cell destined to become the oocyte. During mid-oogenesis, Wolbachia exhibit a distinct concentration between the anterior cortex and the nucleus in the oocyte, where many bacteria appear to contact the nuclear envelope. Following programmed rearrangement of the microtubule network, Wolbachia dissociate from this anterior position and become dispersed throughout the oocyte. This localization pattern is distinct from mitochondria and all known axis determinants. Manipulation of microtubules and cytoplasmic Dynein and Dynactin, but not Kinesin-1, disrupts anterior bacterial localization in the oocyte. In live egg chambers, Wolbachia exhibit movement in nurse cells but not in the oocyte, suggesting that the bacteria are anchored by host factors. In addition, we identify mid-oogenesis as a period in the life cycle of Wolbachia in which bacterial replication occurs. Total bacterial counts show that Wolbachia increase at a significantly higher rate in the oocyte than in the average nurse cell, and that normal Wolbachia levels in the oocyte depend on microtubules. These findings demonstrate that Wolbachia utilize the host microtubule network and associated proteins for their subcellular localization in the Drosophila oocyte. These interactions may also play a role in bacterial motility and replication, ultimately leading to the bacteria's efficient maternal transmission.

Wolbachia Associations with Insects: Winning or Losing Against a Master Manipulator

“…Wolbachia are known to preferentially localize within specific regions of the oocyte during oogenesis (Ferree et al, 2005;Frydman et al, 2006). Recent studies show that Wolbachia access the cytoplasm of the forming egg by two main routes.…”

Symmetric and asymmetric mitotic segregation patterns influence Wolbachia distribution in host somatic tissue

“…Work in the Drosophila oocyte has demonstrated that microtubule-dependent Wolbachia movement during mid-oogenesis relies on the minus-end motor protein dynein for proper anterior positioning (Ferree et al, 2005). This raises the possibility that the concentration at the centrosome might be achieved by Wolbachia continuously engaging dynein, a minusend-directed motor protein.…”

“…Either of these possibilities is likely, because studies of Wolbachia in oocytes have shown that the bacteria can engage different motor and cortical proteins during oocyte development (Ferree et al, 2005;Serbus and Sullivan, 2007).…”

Reliance of Wolbachia on High Rates of Host Proteolysis Revealed by a Genome-Wide RNAi Screen of Drosophila Cells

“…For example, in the Drosophila oocyte, Wolbachia rely on normal host microtubule organization and the Gurken dorsal signaling complex to maintain titer (Ferree et al 2005;Serbus et al 2011). Additional evidence for the influence of host factors on Wolbachia titer comes from the finding that the same Wolbachia strain in D. simulans and D. melanogaster exhibits dramatically different titers in the mature oocyte (Poinsot et al 1998;Serbus and Sullivan 2007).…”