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Bacterial symbionts support larval sap feeding and adult folivory in (semi-)aquatic reed beetles

Symbiotic microbes can enable their host to access untapped nutritional resources but may also constrain niche space by promoting specialization. Here, we reconstruct functional changes in the evolutionary history of the symbiosis between a group of (semi-)aquatic herbivorous insects and mutualistic...

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Autores principales: Reis, Frank, Kirsch, Roy, Pauchet, Yannick, Bauer, Eugen, Bilz, Lisa Carolin, Fukumori, Kayoko, Fukatsu, Takema, Kölsch, Gregor, Kaltenpoth, Martin
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7289800/
https://www.ncbi.nlm.nih.gov/pubmed/32528063
http://dx.doi.org/10.1038/s41467-020-16687-7
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author Reis, Frank
Kirsch, Roy
Pauchet, Yannick
Bauer, Eugen
Bilz, Lisa Carolin
Fukumori, Kayoko
Fukatsu, Takema
Kölsch, Gregor
Kaltenpoth, Martin
author_facet Reis, Frank
Kirsch, Roy
Pauchet, Yannick
Bauer, Eugen
Bilz, Lisa Carolin
Fukumori, Kayoko
Fukatsu, Takema
Kölsch, Gregor
Kaltenpoth, Martin
author_sort Reis, Frank
collection PubMed
description Symbiotic microbes can enable their host to access untapped nutritional resources but may also constrain niche space by promoting specialization. Here, we reconstruct functional changes in the evolutionary history of the symbiosis between a group of (semi-)aquatic herbivorous insects and mutualistic bacteria. Sequencing the symbiont genomes across 26 species of reed beetles (Chrysomelidae, Donaciinae) spanning four genera indicates that the genome-eroded mutualists provide life stage-specific benefits to larvae and adults, respectively. In the plant sap-feeding larvae, the symbionts are inferred to synthesize most of the essential amino acids as well as the B vitamin riboflavin. The adult reed beetles’ folivory is likely supported by symbiont-encoded pectinases that complement the host-encoded set of cellulases, as revealed by transcriptome sequencing. However, mapping the occurrence of the symbionts’ pectinase genes and the hosts’ food plant preferences onto the beetles’ phylogeny reveals multiple independent losses of pectinase genes in lineages that switched to feeding on pectin-poor plants, presumably constraining their hosts’ subsequent adaptive potential.
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spelling pubmed-72898002020-06-16 Bacterial symbionts support larval sap feeding and adult folivory in (semi-)aquatic reed beetles Reis, Frank Kirsch, Roy Pauchet, Yannick Bauer, Eugen Bilz, Lisa Carolin Fukumori, Kayoko Fukatsu, Takema Kölsch, Gregor Kaltenpoth, Martin Nat Commun Article Symbiotic microbes can enable their host to access untapped nutritional resources but may also constrain niche space by promoting specialization. Here, we reconstruct functional changes in the evolutionary history of the symbiosis between a group of (semi-)aquatic herbivorous insects and mutualistic bacteria. Sequencing the symbiont genomes across 26 species of reed beetles (Chrysomelidae, Donaciinae) spanning four genera indicates that the genome-eroded mutualists provide life stage-specific benefits to larvae and adults, respectively. In the plant sap-feeding larvae, the symbionts are inferred to synthesize most of the essential amino acids as well as the B vitamin riboflavin. The adult reed beetles’ folivory is likely supported by symbiont-encoded pectinases that complement the host-encoded set of cellulases, as revealed by transcriptome sequencing. However, mapping the occurrence of the symbionts’ pectinase genes and the hosts’ food plant preferences onto the beetles’ phylogeny reveals multiple independent losses of pectinase genes in lineages that switched to feeding on pectin-poor plants, presumably constraining their hosts’ subsequent adaptive potential. Nature Publishing Group UK 2020-06-11 /pmc/articles/PMC7289800/ /pubmed/32528063 http://dx.doi.org/10.1038/s41467-020-16687-7 Text en © The Author(s) 2020 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.
spellingShingle Article
Reis, Frank
Kirsch, Roy
Pauchet, Yannick
Bauer, Eugen
Bilz, Lisa Carolin
Fukumori, Kayoko
Fukatsu, Takema
Kölsch, Gregor
Kaltenpoth, Martin
Bacterial symbionts support larval sap feeding and adult folivory in (semi-)aquatic reed beetles
title Bacterial symbionts support larval sap feeding and adult folivory in (semi-)aquatic reed beetles
title_full Bacterial symbionts support larval sap feeding and adult folivory in (semi-)aquatic reed beetles
title_fullStr Bacterial symbionts support larval sap feeding and adult folivory in (semi-)aquatic reed beetles
title_full_unstemmed Bacterial symbionts support larval sap feeding and adult folivory in (semi-)aquatic reed beetles
title_short Bacterial symbionts support larval sap feeding and adult folivory in (semi-)aquatic reed beetles
title_sort bacterial symbionts support larval sap feeding and adult folivory in (semi-)aquatic reed beetles
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7289800/
https://www.ncbi.nlm.nih.gov/pubmed/32528063
http://dx.doi.org/10.1038/s41467-020-16687-7
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