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Vertical Transmission at the Pathogen-Symbiont Interface: Serratia symbiotica and Aphids
Many insects possess beneficial bacterial symbionts that occupy specialized host cells and are maternally transmitted. As a consequence of their host-restricted lifestyle, these symbionts often possess reduced genomes and cannot be cultured outside hosts, limiting their study. The bacterial species...
Autores principales: | , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
American Society for Microbiology
2021
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8092240/ https://www.ncbi.nlm.nih.gov/pubmed/33879583 http://dx.doi.org/10.1128/mBio.00359-21 |
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author | Perreau, Julie Patel, Devki J. Anderson, Hanna Maeda, Gerald P. Elston, Katherine M. Barrick, Jeffrey E. Moran, Nancy A. |
author_facet | Perreau, Julie Patel, Devki J. Anderson, Hanna Maeda, Gerald P. Elston, Katherine M. Barrick, Jeffrey E. Moran, Nancy A. |
author_sort | Perreau, Julie |
collection | PubMed |
description | Many insects possess beneficial bacterial symbionts that occupy specialized host cells and are maternally transmitted. As a consequence of their host-restricted lifestyle, these symbionts often possess reduced genomes and cannot be cultured outside hosts, limiting their study. The bacterial species Serratia symbiotica was originally characterized as noncultured strains that live as mutualistic symbionts of aphids and are vertically transmitted through transovarial endocytosis within the mother’s body. More recently, culturable strains of S. symbiotica were discovered that retain a larger set of ancestral Serratia genes, are gut pathogens in aphid hosts, and are principally transmitted via a fecal-oral route. We find that these culturable strains, when injected into pea aphids, replicate in the hemolymph and are pathogenic. Unexpectedly, they are also capable of maternal transmission via transovarial endocytosis: using green fluorescent protein (GFP)-tagged strains, we observe that pathogenic S. symbiotica strains, but not Escherichia coli, are endocytosed into early embryos. Furthermore, pathogenic S. symbiotica strains are compartmentalized into specialized aphid cells in a fashion similar to that of mutualistic S. symbiotica strains during later stages of embryonic development. However, infected embryos do not appear to develop properly, and offspring infected by a transovarial route are not observed. Thus, cultured pathogenic strains of S. symbiotica have the latent capacity to transition to lifestyles as mutualistic symbionts of aphid hosts, but persistent vertical transmission is blocked by their pathogenicity. To transition into stably inherited symbionts, culturable S. symbiotica strains may need to adapt to regulate their titer, limit their pathogenicity, and/or provide benefits to aphids that outweigh their cost. |
format | Online Article Text |
id | pubmed-8092240 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2021 |
publisher | American Society for Microbiology |
record_format | MEDLINE/PubMed |
spelling | pubmed-80922402021-05-04 Vertical Transmission at the Pathogen-Symbiont Interface: Serratia symbiotica and Aphids Perreau, Julie Patel, Devki J. Anderson, Hanna Maeda, Gerald P. Elston, Katherine M. Barrick, Jeffrey E. Moran, Nancy A. mBio Research Article Many insects possess beneficial bacterial symbionts that occupy specialized host cells and are maternally transmitted. As a consequence of their host-restricted lifestyle, these symbionts often possess reduced genomes and cannot be cultured outside hosts, limiting their study. The bacterial species Serratia symbiotica was originally characterized as noncultured strains that live as mutualistic symbionts of aphids and are vertically transmitted through transovarial endocytosis within the mother’s body. More recently, culturable strains of S. symbiotica were discovered that retain a larger set of ancestral Serratia genes, are gut pathogens in aphid hosts, and are principally transmitted via a fecal-oral route. We find that these culturable strains, when injected into pea aphids, replicate in the hemolymph and are pathogenic. Unexpectedly, they are also capable of maternal transmission via transovarial endocytosis: using green fluorescent protein (GFP)-tagged strains, we observe that pathogenic S. symbiotica strains, but not Escherichia coli, are endocytosed into early embryos. Furthermore, pathogenic S. symbiotica strains are compartmentalized into specialized aphid cells in a fashion similar to that of mutualistic S. symbiotica strains during later stages of embryonic development. However, infected embryos do not appear to develop properly, and offspring infected by a transovarial route are not observed. Thus, cultured pathogenic strains of S. symbiotica have the latent capacity to transition to lifestyles as mutualistic symbionts of aphid hosts, but persistent vertical transmission is blocked by their pathogenicity. To transition into stably inherited symbionts, culturable S. symbiotica strains may need to adapt to regulate their titer, limit their pathogenicity, and/or provide benefits to aphids that outweigh their cost. American Society for Microbiology 2021-04-20 /pmc/articles/PMC8092240/ /pubmed/33879583 http://dx.doi.org/10.1128/mBio.00359-21 Text en Copyright © 2021 Perreau et al. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) . |
spellingShingle | Research Article Perreau, Julie Patel, Devki J. Anderson, Hanna Maeda, Gerald P. Elston, Katherine M. Barrick, Jeffrey E. Moran, Nancy A. Vertical Transmission at the Pathogen-Symbiont Interface: Serratia symbiotica and Aphids |
title | Vertical Transmission at the Pathogen-Symbiont Interface: Serratia symbiotica and Aphids |
title_full | Vertical Transmission at the Pathogen-Symbiont Interface: Serratia symbiotica and Aphids |
title_fullStr | Vertical Transmission at the Pathogen-Symbiont Interface: Serratia symbiotica and Aphids |
title_full_unstemmed | Vertical Transmission at the Pathogen-Symbiont Interface: Serratia symbiotica and Aphids |
title_short | Vertical Transmission at the Pathogen-Symbiont Interface: Serratia symbiotica and Aphids |
title_sort | vertical transmission at the pathogen-symbiont interface: serratia symbiotica and aphids |
topic | Research Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8092240/ https://www.ncbi.nlm.nih.gov/pubmed/33879583 http://dx.doi.org/10.1128/mBio.00359-21 |
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