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Proc Natl Acad Sci U S A. 2014 May 20;111(20):7433-7. doi: 10.1073/pnas.1402476111. Epub 2014 May 5.

Intrasperm vertical symbiont transmission.

Author information

1
National Institute of Agrobiololgical Sciences, Tsukuba 305-8634, Japan;
2
Graduate School of Life and Environmental Sciences, University of Tsukuba, Tsukuba 305-8577, Japan; andNational Institute of Advanced Industrial Science and Technology, Tsukuba 305-8566, Japan.
3
National Institute of Advanced Industrial Science and Technology, Tsukuba 305-8566, Japan.
4
National Institute of Agrobiololgical Sciences, Tsukuba 305-8634, Japan; hnada@affrc.go.jp.

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.

PMID:
24799707
PMCID:
PMC4034255
DOI:
10.1073/pnas.1402476111
[Indexed for MEDLINE]
Free PMC Article

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