Male killing Spiroplasma preferentially disrupts neural development in the Drosophila melanogaster embryo.

Male killing bacteria such as Spiroplasma are widespread pathogens of numerous arthropods including Drosophila melanogaster. These maternally transmitted bacteria can bias host sex ratios toward the female sex in order to 'selfishly' enhance bacterial transmission. However, little is known...

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Autores principales: Jennifer Martin, Trisha Chong, Patrick M Ferree
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Publicado: Public Library of Science (PLoS) 2013
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spelling oai:doaj.org-article:afefe643e045434f9edc980ec9d622d32021-11-18T08:46:47ZMale killing Spiroplasma preferentially disrupts neural development in the Drosophila melanogaster embryo.1932-620310.1371/journal.pone.0079368https://doaj.org/article/afefe643e045434f9edc980ec9d622d32013-01-01T00:00:00Zhttps://www.ncbi.nlm.nih.gov/pmc/articles/pmid/24236124/?tool=EBIhttps://doaj.org/toc/1932-6203Male killing bacteria such as Spiroplasma are widespread pathogens of numerous arthropods including Drosophila melanogaster. These maternally transmitted bacteria can bias host sex ratios toward the female sex in order to 'selfishly' enhance bacterial transmission. However, little is known about the specific means by which these pathogens disrupt host development in order to kill males. Here we show that a male-killing Spiroplasma strain severely disrupts nervous tissue development in male but not female D. melanogaster embryos. The neuroblasts, or neuron progenitors, form properly and their daughter cells differentiate into neurons of the ventral nerve chord. However, the neurons fail to pack together properly and they produce highly abnormal axons. In contrast, non-neural tissue, such as mesoderm, and body segmentation appear normal during this time, although the entire male embryo becomes highly abnormal during later stages. Finally, we found that Spiroplasma is altogether absent from the neural tissue but localizes within the gut and the epithelium immediately surrounding the neural tissue, suggesting that the bacterium secretes a toxin that affects neural tissue development across tissue boundaries. Together these findings demonstrate the unique ability of this insect pathogen to preferentially affect development of a specific embryonic tissue to induce male killing.Jennifer MartinTrisha ChongPatrick M FerreePublic Library of Science (PLoS)articleMedicineRScienceQENPLoS ONE, Vol 8, Iss 11, p e79368 (2013)
institution DOAJ
collection DOAJ
language EN
topic Medicine
R
Science
Q
spellingShingle Medicine
R
Science
Q
Jennifer Martin
Trisha Chong
Patrick M Ferree
Male killing Spiroplasma preferentially disrupts neural development in the Drosophila melanogaster embryo.
description Male killing bacteria such as Spiroplasma are widespread pathogens of numerous arthropods including Drosophila melanogaster. These maternally transmitted bacteria can bias host sex ratios toward the female sex in order to 'selfishly' enhance bacterial transmission. However, little is known about the specific means by which these pathogens disrupt host development in order to kill males. Here we show that a male-killing Spiroplasma strain severely disrupts nervous tissue development in male but not female D. melanogaster embryos. The neuroblasts, or neuron progenitors, form properly and their daughter cells differentiate into neurons of the ventral nerve chord. However, the neurons fail to pack together properly and they produce highly abnormal axons. In contrast, non-neural tissue, such as mesoderm, and body segmentation appear normal during this time, although the entire male embryo becomes highly abnormal during later stages. Finally, we found that Spiroplasma is altogether absent from the neural tissue but localizes within the gut and the epithelium immediately surrounding the neural tissue, suggesting that the bacterium secretes a toxin that affects neural tissue development across tissue boundaries. Together these findings demonstrate the unique ability of this insect pathogen to preferentially affect development of a specific embryonic tissue to induce male killing.
format article
author Jennifer Martin
Trisha Chong
Patrick M Ferree
author_facet Jennifer Martin
Trisha Chong
Patrick M Ferree
author_sort Jennifer Martin
title Male killing Spiroplasma preferentially disrupts neural development in the Drosophila melanogaster embryo.
title_short Male killing Spiroplasma preferentially disrupts neural development in the Drosophila melanogaster embryo.
title_full Male killing Spiroplasma preferentially disrupts neural development in the Drosophila melanogaster embryo.
title_fullStr Male killing Spiroplasma preferentially disrupts neural development in the Drosophila melanogaster embryo.
title_full_unstemmed Male killing Spiroplasma preferentially disrupts neural development in the Drosophila melanogaster embryo.
title_sort male killing spiroplasma preferentially disrupts neural development in the drosophila melanogaster embryo.
publisher Public Library of Science (PLoS)
publishDate 2013
url https://doaj.org/article/afefe643e045434f9edc980ec9d622d3
work_keys_str_mv AT jennifermartin malekillingspiroplasmapreferentiallydisruptsneuraldevelopmentinthedrosophilamelanogasterembryo
AT trishachong malekillingspiroplasmapreferentiallydisruptsneuraldevelopmentinthedrosophilamelanogasterembryo
AT patrickmferree malekillingspiroplasmapreferentiallydisruptsneuraldevelopmentinthedrosophilamelanogasterembryo
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