Abstract
Virus-like particles (VLPs) have not been observed in Caenorhabditis germ cells, although nematode genomes contain low numbers of retrotransposon and retroviral sequences. We used electron microscopy to search for VLPs in various wild strains of Caenorhabditis, and observed very rare candidate VLPs in some strains, including the standard laboratory strain of C. elegans, N2. We identified the N2 VLPs as capsids produced by Cer1, a retrotransposon in the Gypsy/Ty3 family of retroviruses/retrotransposons. Cer1 expression is age and temperature dependent, with abundant expression at 15°C and no detectable expression at 25°C, explaining how VLPs escaped detection in previous studies. Similar age and temperature-dependent expression of Cer1 retrotransposons was observed for several other wild strains, indicating that these properties are common, if not integral, features of this retroelement. Retrotransposons, in contrast to DNA transposons, have a cytoplasmic stage in replication, and those that infect non-dividing cells must pass their genomic material through nuclear pores. In most C. elegans germ cells, nuclear pores are largely covered by germline-specific organelles called P granules. Our results suggest that Cer1 capsids target meiotic germ cells exiting pachytene, when free nuclear pores are added to the nuclear envelope and existing P granules begin to be removed. In pachytene germ cells, Cer1 capsids concentrate away from nuclei on a subset of microtubules that are exceptionally resistant to microtubule inhibitors; the capsids can aggregate these stable microtubules in older adults, which exhibit a temperature-dependent decrease in egg viability. When germ cells exit pachytene, the stable microtubules disappear and capsids redistribute close to nuclei that have P granule-free nuclear pores. This redistribution is microtubule dependent, suggesting that capsids that are released from stable microtubules transfer onto new, dynamic microtubules to track toward nuclei. These studies introduce C. elegans as a model to study the interplay between retroelements and germ cell biology.
Highlights
DNA transposons, retrotransposons, and retroviruses that are expressed in germ cells have tremendous potential to damage the genome by creating novel insertions that are transmitted vertically to host progeny
No viruslike particles have been observed in C. elegans germ cells
We show here that Cer1, an endogenous Gypsy/Ty3 class retrotransposon, is expressed at very high levels in C. elegans germ cells, but escaped detection in previous studies because its expression is both temperature and age dependent
Summary
DNA transposons, retrotransposons, and retroviruses that are expressed in germ cells have tremendous potential to damage the genome by creating novel insertions that are transmitted vertically to host progeny. Because DNA transposons replicate by an excision and reintegration mechanism (‘‘cut and paste’’), replication of an endogenous element does not necessarily increase copy number [1]. Retrotransposons, replicate by first transcribing genomic RNAs that are later reverse transcribed for integration (‘‘copy-and paste’’), and endogenous elements have the potential to increase their copy numbers exponentially if left unchecked [1,2]. Animal and plant genomes typically contain far more copies of retrotransposons than of DNA transposons. Retrotransposons constitute only 0.6% of the C. elegans genome, while DNA transposons make up about 12% [5,6,7]. C. elegans has long been considered an inadequate model organism to study natural virus-host interactions, recent studies have shown that it is possible to artificially infect nematodes or nematode cell lines with promiscuous viruses, and a natural virus that infects intestinal cells has been identified [11,12,13,14,15]
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