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Abundance and Localization of Symbiotic Bacterial Communities in the Fly Parasitoid Spalangia cameroni

Multicellular eukaryotes often host multiple microbial symbionts that may cooperate or compete for host resources, such as space and nutrients. Here, we studied the abundances and localization of four bacterial symbionts, Rickettsia, Wolbachia, Sodalis, and Arsenophonus, in the parasitic wasp Spalan...

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Autores principales: Rohkin Shalom, Sarit, Weiss, Benjamin, Lalzar, Maya, Kaltenpoth, Martin, Chiel, Elad
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9088259/
https://www.ncbi.nlm.nih.gov/pubmed/35420439
http://dx.doi.org/10.1128/aem.02549-21
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author Rohkin Shalom, Sarit
Weiss, Benjamin
Lalzar, Maya
Kaltenpoth, Martin
Chiel, Elad
author_facet Rohkin Shalom, Sarit
Weiss, Benjamin
Lalzar, Maya
Kaltenpoth, Martin
Chiel, Elad
author_sort Rohkin Shalom, Sarit
collection PubMed
description Multicellular eukaryotes often host multiple microbial symbionts that may cooperate or compete for host resources, such as space and nutrients. Here, we studied the abundances and localization of four bacterial symbionts, Rickettsia, Wolbachia, Sodalis, and Arsenophonus, in the parasitic wasp Spalangia cameroni. Using quantitative PCR (qPCR), we measured the symbionts’ titers in wasps that harbor different combinations of these symbionts. We found that the titer of each symbiont decreased as the number of symbiont species in the community increased. Symbionts' titers were higher in females than in males. Rickettsia was the most abundant symbiont in all the communities, followed by Sodalis and Wolbachia. The titers of these three symbionts were positively correlated in some of the colonies. Fluorescence in situ hybridization was in line with the qPCR results: Rickettsia, Wolbachia, and Sodalis were observed in high densities in multiple organs, including brain, muscles, gut, Malpighian tubules, fat body, ovaries, and testes, while Arsenophonus was localized to fewer organs and in lower densities. Sodalis and Arsenophonus were observed in ovarian follicle cells but not within oocytes or laid eggs. This study highlights the connection between symbionts’ abundance and localization. We discuss the possible connections between our findings to symbiont transmission success. IMPORTANCE Many insects carry intracellular bacterial symbionts (bacteria that reside within the cells of the insect). When multiple symbiont species cohabit in a host, they may compete or cooperate for space, nutrients, and transmission, and the nature of such interactions would be reflected in the abundance of each symbiont species. Given the widespread occurrence of coinfections with maternally transmitted symbionts in insects, it is important to learn more about how they interact, where they are localized, and how these two aspects affect their co-occurrence within individual insects. Here, we studied the abundance and the localization of four symbionts, Rickettsia, Wolbachia, Sodalis, and Arsenophonus, that cohabit the parasitic wasp Spalangia cameroni. We found that symbionts’ titers differed between symbiotic communities. These results were corroborated by microscopy, which shows differential localization patterns. We discuss the findings in the contexts of community ecology, possible symbiont-symbiont interactions, and host control mechanisms that may shape the symbiotic community structure.
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spelling pubmed-90882592022-05-11 Abundance and Localization of Symbiotic Bacterial Communities in the Fly Parasitoid Spalangia cameroni Rohkin Shalom, Sarit Weiss, Benjamin Lalzar, Maya Kaltenpoth, Martin Chiel, Elad Appl Environ Microbiol Invertebrate Microbiology Multicellular eukaryotes often host multiple microbial symbionts that may cooperate or compete for host resources, such as space and nutrients. Here, we studied the abundances and localization of four bacterial symbionts, Rickettsia, Wolbachia, Sodalis, and Arsenophonus, in the parasitic wasp Spalangia cameroni. Using quantitative PCR (qPCR), we measured the symbionts’ titers in wasps that harbor different combinations of these symbionts. We found that the titer of each symbiont decreased as the number of symbiont species in the community increased. Symbionts' titers were higher in females than in males. Rickettsia was the most abundant symbiont in all the communities, followed by Sodalis and Wolbachia. The titers of these three symbionts were positively correlated in some of the colonies. Fluorescence in situ hybridization was in line with the qPCR results: Rickettsia, Wolbachia, and Sodalis were observed in high densities in multiple organs, including brain, muscles, gut, Malpighian tubules, fat body, ovaries, and testes, while Arsenophonus was localized to fewer organs and in lower densities. Sodalis and Arsenophonus were observed in ovarian follicle cells but not within oocytes or laid eggs. This study highlights the connection between symbionts’ abundance and localization. We discuss the possible connections between our findings to symbiont transmission success. IMPORTANCE Many insects carry intracellular bacterial symbionts (bacteria that reside within the cells of the insect). When multiple symbiont species cohabit in a host, they may compete or cooperate for space, nutrients, and transmission, and the nature of such interactions would be reflected in the abundance of each symbiont species. Given the widespread occurrence of coinfections with maternally transmitted symbionts in insects, it is important to learn more about how they interact, where they are localized, and how these two aspects affect their co-occurrence within individual insects. Here, we studied the abundance and the localization of four symbionts, Rickettsia, Wolbachia, Sodalis, and Arsenophonus, that cohabit the parasitic wasp Spalangia cameroni. We found that symbionts’ titers differed between symbiotic communities. These results were corroborated by microscopy, which shows differential localization patterns. We discuss the findings in the contexts of community ecology, possible symbiont-symbiont interactions, and host control mechanisms that may shape the symbiotic community structure. American Society for Microbiology 2022-04-14 /pmc/articles/PMC9088259/ /pubmed/35420439 http://dx.doi.org/10.1128/aem.02549-21 Text en Copyright © 2022 Rohkin Shalom 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 Invertebrate Microbiology
Rohkin Shalom, Sarit
Weiss, Benjamin
Lalzar, Maya
Kaltenpoth, Martin
Chiel, Elad
Abundance and Localization of Symbiotic Bacterial Communities in the Fly Parasitoid Spalangia cameroni
title Abundance and Localization of Symbiotic Bacterial Communities in the Fly Parasitoid Spalangia cameroni
title_full Abundance and Localization of Symbiotic Bacterial Communities in the Fly Parasitoid Spalangia cameroni
title_fullStr Abundance and Localization of Symbiotic Bacterial Communities in the Fly Parasitoid Spalangia cameroni
title_full_unstemmed Abundance and Localization of Symbiotic Bacterial Communities in the Fly Parasitoid Spalangia cameroni
title_short Abundance and Localization of Symbiotic Bacterial Communities in the Fly Parasitoid Spalangia cameroni
title_sort abundance and localization of symbiotic bacterial communities in the fly parasitoid spalangia cameroni
topic Invertebrate Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9088259/
https://www.ncbi.nlm.nih.gov/pubmed/35420439
http://dx.doi.org/10.1128/aem.02549-21
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