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, 111 (20), 7433-7

Intrasperm Vertical Symbiont Transmission

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Intrasperm Vertical Symbiont Transmission

Kenji Watanabe et al. Proc Natl Acad Sci U S A.

Abstract

Symbiotic bacteria are commonly associated with cells and tissues of diverse animals and other organisms, which affect hosts' biology in a variety of ways. Most of these symbionts are present in the cytoplasm of host cells and maternally transmitted through host generations. The paucity of paternal symbiont transmission is likely relevant to the extremely streamlined sperm structure: the head consisting of condensed nucleus and the tail made of microtubule bundles, without the symbiont-harboring cytoplasm that is discarded in the process of spermatogenesis. Here, we report a previously unknown mechanism of paternal symbiont transmission via an intrasperm passage. In the leafhopper Nephotettix cincticeps, a facultative Rickettsia symbiont was found not only in the cytoplasm but also in the nucleus of host cells. In male insects, strikingly, most sperm heads contained multiple intranuclear Rickettsia cells. The Rickettsia infection scarcely affected the host fitness including normal sperm functioning. Mating experiments revealed both maternal and paternal transmission of the Rickettsia symbiont through host generations. When cultured with mosquito and silkworm cell lines, the Rickettsia symbiont was preferentially localized within the insect cell nuclei, indicating that the Rickettsia symbiont itself must have a mechanism for targeting nucleus. The mechanisms underlying the sperm head infection without disturbing sperm functioning are, although currently unknown, of both basic and applied interest.

Conflict of interest statement

The authors declare no conflict of interest.

Figures

Fig. 1.
Fig. 1.
The green rice leafhopper N. cincticeps and its Rickettsia symbiont. (A) An adult male of N. cincticeps. (B) Phylogenetic placement of the Rickettsia symbiont of N. cincticeps on the basis of 16S rRNA gene sequence. A Bayesian phylogeny inferred from 1,296 aligned nucleotide sites is shown. Posterior probabilities for the Bayesian phylogeny and bootstrap probabilities for the maximum likelihood phylogeny at 50% or higher are shown at the nodes, whereas asterisks indicate support values lower than 50%. Sequence accession numbers are shown in brackets. Major Rickettsia groups (40) are indicated on the right side.
Fig. 2.
Fig. 2.
Transmission electron microscopy of nuclear localization of the Rickettsia symbiont in tissues of N. cincticeps and cell lines of other insects. (A) Malphigian tubule cell of N. cincticeps. (B) Midgut cell of N. cincticeps. (C) Cell line aff3 derived from the silkworm B. mori. (D) Cell line AeAl-2 derived from the mosquito A. albopictus. (E) Cross-section of sperm heads in testis of N. cincticeps. (F) Longitudinal section of sperm heads in testis of N. cincticeps. (G) Magnified image of the sperm heads. (H) Spermatheca of Rickettsia-uninfected female of N. cincticeps after mating with Rickettsia-infected male. mv, microvilli on the epithelium of spermatheca; n, nucleus; sh, sperm head; st, sperm tail. Asterisk in H highlights an intrasperm Rickettsia cell.
Fig. 3.
Fig. 3.
In situ hybridization of the Rickettsia symbiont in mature sperm heads obtained from seminal vesicles of Rickettsia-infected males of N. cincticeps. (A) Red hybridization signals due to 16S rRNA of the Rickettsia symbiont. (B) Blue signals due to DNA staining of sperm heads. Note the unstained areas within the sperm heads, reflecting endonuclear localization of the Rickettsia symbiont cells. (C) Merged image. Note that a number of Rickettsia cells are arranged in a row within each sperm head.
Fig. 4.
Fig. 4.
Number of Rickettsia cells in mature sperm heads and vertical transmission rates of Rickettsia. (A) Number of Rickettsia per sperm head based on in situ hybridization images of 1,109 sperm heads obtained from seminal vesicles of four Rickettsia-infected adult males. (B) Vertical transmission rates of Rickettsia upon all mating combinations within and between the Rickettsia-infected and uninfected host strains. The numbers of parent pairs and those of total offspring are indicated above the columns.

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