Wolbachia interferes with ferritin expression and iron metabolism in insects.
Wolbachia is an intracellular bacterium generally described as being a facultative reproductive parasite. However, Wolbachia is necessary for oogenesis completion in the wasp Asobara tabida. This dependence has evolved recently as a result of interference with apoptosis during oogenesis. Through com...
| Main Authors: | , , , , , |
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| Format: | Article |
| Language: | English |
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Public Library of Science (PLoS)
2009-10-01
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| Series: | PLoS Pathogens |
| Online Access: | http://europepmc.org/articles/PMC2759286?pdf=render |
| _version_ | 1818827780234674176 |
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| author | Natacha Kremer Denis Voronin Delphine Charif Patrick Mavingui Bertrand Mollereau Fabrice Vavre |
| author_facet | Natacha Kremer Denis Voronin Delphine Charif Patrick Mavingui Bertrand Mollereau Fabrice Vavre |
| author_sort | Natacha Kremer |
| collection | DOAJ |
| description | Wolbachia is an intracellular bacterium generally described as being a facultative reproductive parasite. However, Wolbachia is necessary for oogenesis completion in the wasp Asobara tabida. This dependence has evolved recently as a result of interference with apoptosis during oogenesis. Through comparative transcriptomics between symbiotic and aposymbiotic individuals, we observed a differential expression of ferritin, which forms a complex involved in iron storage. Iron is an essential element that is in limited supply in the cell. However, it is also a highly toxic precursor of Reactive Oxygen Species (ROS). Ferritin has also been shown to play a key role in host-pathogen interactions. Measuring ferritin by quantitative RT-PCR, we confirmed that ferritin was upregulated in aposymbiotic compared to symbiotic individuals. Manipulating the iron content in the diet, we showed that iron overload markedly affected wasp development and induced apoptotic processes during oogenesis in A. tabida, suggesting that the regulation of iron homeostasis may also be related to the obligate dependence of the wasp. Finally, we demonstrated that iron metabolism is influenced by the presence of Wolbachia not only in the obligate mutualism with A. tabida, but also in facultative parasitism involving Drosophila simulans and in Aedes aegypti cells. In these latter cases, the expression of Wolbachia bacterioferritin was also increased in the presence of iron, showing that Wolbachia responds to the concentration of iron. Our results indicate that Wolbachia may generally interfere with iron metabolism. The high affinity of Wolbachia for iron might be due to physiological requirement of the bacterium, but it could also be what allows the symbiont to persist in the organism by reducing the labile iron concentration, thus protecting the cell from oxidative stress and apoptosis. These findings also reinforce the idea that pathogenic, parasitic and mutualistic intracellular bacteria all use the same molecular mechanisms to survive and replicate within host cells. By impacting the general physiology of the host, the presence of a symbiont may select for host compensatory mechanisms, which extends the possible consequences of persistent endosymbiont on the evolution of their hosts. |
| first_indexed | 2024-12-19T00:48:59Z |
| format | Article |
| id | doaj.art-b810a8bc420d4b1c9701d4081fb78b70 |
| institution | Directory Open Access Journal |
| issn | 1553-7366 1553-7374 |
| language | English |
| last_indexed | 2024-12-19T00:48:59Z |
| publishDate | 2009-10-01 |
| publisher | Public Library of Science (PLoS) |
| record_format | Article |
| series | PLoS Pathogens |
| spelling | doaj.art-b810a8bc420d4b1c9701d4081fb78b702022-12-21T20:44:08ZengPublic Library of Science (PLoS)PLoS Pathogens1553-73661553-73742009-10-01510e100063010.1371/journal.ppat.1000630Wolbachia interferes with ferritin expression and iron metabolism in insects.Natacha KremerDenis VoroninDelphine CharifPatrick MavinguiBertrand MollereauFabrice VavreWolbachia is an intracellular bacterium generally described as being a facultative reproductive parasite. However, Wolbachia is necessary for oogenesis completion in the wasp Asobara tabida. This dependence has evolved recently as a result of interference with apoptosis during oogenesis. Through comparative transcriptomics between symbiotic and aposymbiotic individuals, we observed a differential expression of ferritin, which forms a complex involved in iron storage. Iron is an essential element that is in limited supply in the cell. However, it is also a highly toxic precursor of Reactive Oxygen Species (ROS). Ferritin has also been shown to play a key role in host-pathogen interactions. Measuring ferritin by quantitative RT-PCR, we confirmed that ferritin was upregulated in aposymbiotic compared to symbiotic individuals. Manipulating the iron content in the diet, we showed that iron overload markedly affected wasp development and induced apoptotic processes during oogenesis in A. tabida, suggesting that the regulation of iron homeostasis may also be related to the obligate dependence of the wasp. Finally, we demonstrated that iron metabolism is influenced by the presence of Wolbachia not only in the obligate mutualism with A. tabida, but also in facultative parasitism involving Drosophila simulans and in Aedes aegypti cells. In these latter cases, the expression of Wolbachia bacterioferritin was also increased in the presence of iron, showing that Wolbachia responds to the concentration of iron. Our results indicate that Wolbachia may generally interfere with iron metabolism. The high affinity of Wolbachia for iron might be due to physiological requirement of the bacterium, but it could also be what allows the symbiont to persist in the organism by reducing the labile iron concentration, thus protecting the cell from oxidative stress and apoptosis. These findings also reinforce the idea that pathogenic, parasitic and mutualistic intracellular bacteria all use the same molecular mechanisms to survive and replicate within host cells. By impacting the general physiology of the host, the presence of a symbiont may select for host compensatory mechanisms, which extends the possible consequences of persistent endosymbiont on the evolution of their hosts.http://europepmc.org/articles/PMC2759286?pdf=render |
| spellingShingle | Natacha Kremer Denis Voronin Delphine Charif Patrick Mavingui Bertrand Mollereau Fabrice Vavre Wolbachia interferes with ferritin expression and iron metabolism in insects. PLoS Pathogens |
| title | Wolbachia interferes with ferritin expression and iron metabolism in insects. |
| title_full | Wolbachia interferes with ferritin expression and iron metabolism in insects. |
| title_fullStr | Wolbachia interferes with ferritin expression and iron metabolism in insects. |
| title_full_unstemmed | Wolbachia interferes with ferritin expression and iron metabolism in insects. |
| title_short | Wolbachia interferes with ferritin expression and iron metabolism in insects. |
| title_sort | wolbachia interferes with ferritin expression and iron metabolism in insects |
| url | http://europepmc.org/articles/PMC2759286?pdf=render |
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