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Genetic manipulation allows in vivo tracking of the life cycle of the son‐killer symbiont, Arsenophonus nasoniae, and reveals patterns of host invasion, tropism and pathology
Maternally heritable symbionts are common in arthropods and represent important partners and antagonists. A major impediment to understanding the mechanistic basis of these symbioses has been lack of genetic manipulation tools, for instance, those enabling transgenic GFP expression systems for in vi...
Autores principales: | , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
John Wiley & Sons, Inc.
2019
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6771839/ https://www.ncbi.nlm.nih.gov/pubmed/31237728 http://dx.doi.org/10.1111/1462-2920.14724 |
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author | Nadal‐Jimenez, Pol Griffin, Joanne S. Davies, Lianne Frost, Crystal L. Marcello, Marco Hurst, Gregory D. D. |
author_facet | Nadal‐Jimenez, Pol Griffin, Joanne S. Davies, Lianne Frost, Crystal L. Marcello, Marco Hurst, Gregory D. D. |
author_sort | Nadal‐Jimenez, Pol |
collection | PubMed |
description | Maternally heritable symbionts are common in arthropods and represent important partners and antagonists. A major impediment to understanding the mechanistic basis of these symbioses has been lack of genetic manipulation tools, for instance, those enabling transgenic GFP expression systems for in vivo visualization. Here, we transform the ‘son‐killer’ reproductive parasite Arsenophonus nasoniae that infects the parasitic wasp Nasonia vitripennis with the plasmid pOM1‐gfp, re‐introduce this strain to N. vitripennis and then used this system to track symbiont life history in vivo. These data revealed transfer of the symbiont into the fly pupa by N. vitripennis during oviposition and N. vitripennis larvae developing infection over time through feeding. A strong tropism of A. nasoniae to the N. vitripennis ovipositor developed during wasp pupation, which aids onward transmission. The symbiont was also visualized in diapause larvae. Occasional necrotic diapause larvae were observed which displayed intense systemic infection alongside widespread melanotic nodules indicative of an active but failed immune response. Our results provide the foundation for the study of this symbiosis through in vivo tracking of the fate of symbionts through host development, which is rarely achieved in heritable microbe/insect interactions. |
format | Online Article Text |
id | pubmed-6771839 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2019 |
publisher | John Wiley & Sons, Inc. |
record_format | MEDLINE/PubMed |
spelling | pubmed-67718392019-10-07 Genetic manipulation allows in vivo tracking of the life cycle of the son‐killer symbiont, Arsenophonus nasoniae, and reveals patterns of host invasion, tropism and pathology Nadal‐Jimenez, Pol Griffin, Joanne S. Davies, Lianne Frost, Crystal L. Marcello, Marco Hurst, Gregory D. D. Environ Microbiol Research Articles Maternally heritable symbionts are common in arthropods and represent important partners and antagonists. A major impediment to understanding the mechanistic basis of these symbioses has been lack of genetic manipulation tools, for instance, those enabling transgenic GFP expression systems for in vivo visualization. Here, we transform the ‘son‐killer’ reproductive parasite Arsenophonus nasoniae that infects the parasitic wasp Nasonia vitripennis with the plasmid pOM1‐gfp, re‐introduce this strain to N. vitripennis and then used this system to track symbiont life history in vivo. These data revealed transfer of the symbiont into the fly pupa by N. vitripennis during oviposition and N. vitripennis larvae developing infection over time through feeding. A strong tropism of A. nasoniae to the N. vitripennis ovipositor developed during wasp pupation, which aids onward transmission. The symbiont was also visualized in diapause larvae. Occasional necrotic diapause larvae were observed which displayed intense systemic infection alongside widespread melanotic nodules indicative of an active but failed immune response. Our results provide the foundation for the study of this symbiosis through in vivo tracking of the fate of symbionts through host development, which is rarely achieved in heritable microbe/insect interactions. John Wiley & Sons, Inc. 2019-07-11 2019-08 /pmc/articles/PMC6771839/ /pubmed/31237728 http://dx.doi.org/10.1111/1462-2920.14724 Text en © 2019 The Authors. Environmental Microbiology published by Society for Applied Microbiology and John Wiley & Sons Ltd. This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. |
spellingShingle | Research Articles Nadal‐Jimenez, Pol Griffin, Joanne S. Davies, Lianne Frost, Crystal L. Marcello, Marco Hurst, Gregory D. D. Genetic manipulation allows in vivo tracking of the life cycle of the son‐killer symbiont, Arsenophonus nasoniae, and reveals patterns of host invasion, tropism and pathology |
title | Genetic manipulation allows in vivo tracking of the life cycle of the son‐killer symbiont, Arsenophonus nasoniae, and reveals patterns of host invasion, tropism and pathology |
title_full | Genetic manipulation allows in vivo tracking of the life cycle of the son‐killer symbiont, Arsenophonus nasoniae, and reveals patterns of host invasion, tropism and pathology |
title_fullStr | Genetic manipulation allows in vivo tracking of the life cycle of the son‐killer symbiont, Arsenophonus nasoniae, and reveals patterns of host invasion, tropism and pathology |
title_full_unstemmed | Genetic manipulation allows in vivo tracking of the life cycle of the son‐killer symbiont, Arsenophonus nasoniae, and reveals patterns of host invasion, tropism and pathology |
title_short | Genetic manipulation allows in vivo tracking of the life cycle of the son‐killer symbiont, Arsenophonus nasoniae, and reveals patterns of host invasion, tropism and pathology |
title_sort | genetic manipulation allows in vivo tracking of the life cycle of the son‐killer symbiont, arsenophonus nasoniae, and reveals patterns of host invasion, tropism and pathology |
topic | Research Articles |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6771839/ https://www.ncbi.nlm.nih.gov/pubmed/31237728 http://dx.doi.org/10.1111/1462-2920.14724 |
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