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Bacteriome-Localized Intracellular Symbionts in Pollen-Feeding Beetles of the Genus Dasytes (Coleoptera, Dasytidae)

Several insect taxa are associated with intracellular symbionts that provision limiting nutrients to their hosts. Such tightly integrated symbioses are especially common in insects feeding on nutritionally challenging diets like phloem sap or vertebrate blood, but also occur in seed-eating and omniv...

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Autores principales: Weiss, Benjamin, Kaltenpoth, Martin
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5031591/
https://www.ncbi.nlm.nih.gov/pubmed/27713733
http://dx.doi.org/10.3389/fmicb.2016.01486
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author Weiss, Benjamin
Kaltenpoth, Martin
author_facet Weiss, Benjamin
Kaltenpoth, Martin
author_sort Weiss, Benjamin
collection PubMed
description Several insect taxa are associated with intracellular symbionts that provision limiting nutrients to their hosts. Such tightly integrated symbioses are especially common in insects feeding on nutritionally challenging diets like phloem sap or vertebrate blood, but also occur in seed-eating and omnivorous taxa. Here, we characterize an intracellular symbiosis in pollen-feeding beetles of the genus Dasytes (Coleoptera, Dasytidae). High-throughput tag-encoded 16S amplicon pyrosequencing of adult D. plumbeus and D. virens revealed a single gamma-proteobacterial symbiont (‘Candidatus Dasytiphilus stammeri’) that amounts to 52.4–98.7% of the adult beetles’ entire microbial community. Almost complete 16S rRNA sequences phylogenetically placed the symbiont into a clade comprising Buchnera and other insect endosymbionts, but sequence similarities to these closest relatives were surprisingly low (83.4–87.4%). Using histological examination, three-dimensional reconstructions, and fluorescence in situ hybridization, we localized the symbionts in three mulberry-shaped bacteriomes that are associated with the mid- to hind-gut transition in adult male and female beetles. Given the specialized pollen-feeding habits of the adults that contrasts with the larvae’s carnivorous lifestyle, the symbionts may provision limiting essential amino acids or vitamins as in other intracellular symbioses, or they might produce digestive enzymes that break up the fastidious pollen walls and thereby contribute to the host’s nutrition. In either case, the presence of gamma-proteobacterial symbionts in pollen-feeding beetles indicates that intracellular mutualists are more widely distributed across insects with diverse feeding habits than previously recognized.
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spelling pubmed-50315912016-10-06 Bacteriome-Localized Intracellular Symbionts in Pollen-Feeding Beetles of the Genus Dasytes (Coleoptera, Dasytidae) Weiss, Benjamin Kaltenpoth, Martin Front Microbiol Microbiology Several insect taxa are associated with intracellular symbionts that provision limiting nutrients to their hosts. Such tightly integrated symbioses are especially common in insects feeding on nutritionally challenging diets like phloem sap or vertebrate blood, but also occur in seed-eating and omnivorous taxa. Here, we characterize an intracellular symbiosis in pollen-feeding beetles of the genus Dasytes (Coleoptera, Dasytidae). High-throughput tag-encoded 16S amplicon pyrosequencing of adult D. plumbeus and D. virens revealed a single gamma-proteobacterial symbiont (‘Candidatus Dasytiphilus stammeri’) that amounts to 52.4–98.7% of the adult beetles’ entire microbial community. Almost complete 16S rRNA sequences phylogenetically placed the symbiont into a clade comprising Buchnera and other insect endosymbionts, but sequence similarities to these closest relatives were surprisingly low (83.4–87.4%). Using histological examination, three-dimensional reconstructions, and fluorescence in situ hybridization, we localized the symbionts in three mulberry-shaped bacteriomes that are associated with the mid- to hind-gut transition in adult male and female beetles. Given the specialized pollen-feeding habits of the adults that contrasts with the larvae’s carnivorous lifestyle, the symbionts may provision limiting essential amino acids or vitamins as in other intracellular symbioses, or they might produce digestive enzymes that break up the fastidious pollen walls and thereby contribute to the host’s nutrition. In either case, the presence of gamma-proteobacterial symbionts in pollen-feeding beetles indicates that intracellular mutualists are more widely distributed across insects with diverse feeding habits than previously recognized. Frontiers Media S.A. 2016-09-22 /pmc/articles/PMC5031591/ /pubmed/27713733 http://dx.doi.org/10.3389/fmicb.2016.01486 Text en Copyright © 2016 Weiss and Kaltenpoth. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
Weiss, Benjamin
Kaltenpoth, Martin
Bacteriome-Localized Intracellular Symbionts in Pollen-Feeding Beetles of the Genus Dasytes (Coleoptera, Dasytidae)
title Bacteriome-Localized Intracellular Symbionts in Pollen-Feeding Beetles of the Genus Dasytes (Coleoptera, Dasytidae)
title_full Bacteriome-Localized Intracellular Symbionts in Pollen-Feeding Beetles of the Genus Dasytes (Coleoptera, Dasytidae)
title_fullStr Bacteriome-Localized Intracellular Symbionts in Pollen-Feeding Beetles of the Genus Dasytes (Coleoptera, Dasytidae)
title_full_unstemmed Bacteriome-Localized Intracellular Symbionts in Pollen-Feeding Beetles of the Genus Dasytes (Coleoptera, Dasytidae)
title_short Bacteriome-Localized Intracellular Symbionts in Pollen-Feeding Beetles of the Genus Dasytes (Coleoptera, Dasytidae)
title_sort bacteriome-localized intracellular symbionts in pollen-feeding beetles of the genus dasytes (coleoptera, dasytidae)
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5031591/
https://www.ncbi.nlm.nih.gov/pubmed/27713733
http://dx.doi.org/10.3389/fmicb.2016.01486
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