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Direct Evidence That Sunbirds’ Gut Microbiota Degrades Floral Nectar’s Toxic Alkaloids

Orange-tufted sunbirds (Cinnyris osea) feed on the nectar of the tobacco tree (Nicotiana glauca) which contains toxic pyridine alkaloids characterized by high concentrations of anabasine and much lower concentrations of nicotine. We aimed at determining whether the gut microbiota of sunbirds harbors...

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Autores principales: Gunasekaran, Mohanraj, Trabelcy, Beny, Izhaki, Ido, Halpern, Malka
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8018289/
https://www.ncbi.nlm.nih.gov/pubmed/33815326
http://dx.doi.org/10.3389/fmicb.2021.639808
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author Gunasekaran, Mohanraj
Trabelcy, Beny
Izhaki, Ido
Halpern, Malka
author_facet Gunasekaran, Mohanraj
Trabelcy, Beny
Izhaki, Ido
Halpern, Malka
author_sort Gunasekaran, Mohanraj
collection PubMed
description Orange-tufted sunbirds (Cinnyris osea) feed on the nectar of the tobacco tree (Nicotiana glauca) which contains toxic pyridine alkaloids characterized by high concentrations of anabasine and much lower concentrations of nicotine. We aimed at determining whether the gut microbiota of sunbirds harbors bacterial species that enable the birds to cope with these toxic alkaloids. An in vivo experiment that included 12 birds showed that inducing dysbiosis in sunbirds’ guts by the addition of sulfamethoxazole and trimethoprim, significantly reduced the birds’ ability to degrade anabasine (n = 3) compared to control birds (n = 3) with undisturbed microbiota. Sunbirds whose gut bacterial communities were altered by the antibacterial agents and who were fed with added nicotine, also showed a lower percentage of nicotine degradation (n = 3) in their excreta compared to the sunbirds with undisturbed microbiota (n = 3), though this difference was not significant. In an in vitro experiment, we studied the ability of Lactococcus lactis, Enterobacter hormaechei, Chryseobacterium gleum, Kocuria palustris, and Methylorubrum populi that were isolated from sunbirds’ excreta, to degrade anabasine and nicotine. By using gas chromatography-mass spectrometry (GC-MS) analysis, we successfully demonstrated, for the first time, the ability of these species to degrade the focal secondary metabolites. Our findings demonstrate the role of gut bacteria in detoxifying toxic secondary metabolites found in the N. glauca nectar. The degradation products may supply the birds with nitrogen which is scarce in nectar-rich diets. These findings support another role of bacteria in mediating the interactions between plants and their pollinators.
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spelling pubmed-80182892021-04-03 Direct Evidence That Sunbirds’ Gut Microbiota Degrades Floral Nectar’s Toxic Alkaloids Gunasekaran, Mohanraj Trabelcy, Beny Izhaki, Ido Halpern, Malka Front Microbiol Microbiology Orange-tufted sunbirds (Cinnyris osea) feed on the nectar of the tobacco tree (Nicotiana glauca) which contains toxic pyridine alkaloids characterized by high concentrations of anabasine and much lower concentrations of nicotine. We aimed at determining whether the gut microbiota of sunbirds harbors bacterial species that enable the birds to cope with these toxic alkaloids. An in vivo experiment that included 12 birds showed that inducing dysbiosis in sunbirds’ guts by the addition of sulfamethoxazole and trimethoprim, significantly reduced the birds’ ability to degrade anabasine (n = 3) compared to control birds (n = 3) with undisturbed microbiota. Sunbirds whose gut bacterial communities were altered by the antibacterial agents and who were fed with added nicotine, also showed a lower percentage of nicotine degradation (n = 3) in their excreta compared to the sunbirds with undisturbed microbiota (n = 3), though this difference was not significant. In an in vitro experiment, we studied the ability of Lactococcus lactis, Enterobacter hormaechei, Chryseobacterium gleum, Kocuria palustris, and Methylorubrum populi that were isolated from sunbirds’ excreta, to degrade anabasine and nicotine. By using gas chromatography-mass spectrometry (GC-MS) analysis, we successfully demonstrated, for the first time, the ability of these species to degrade the focal secondary metabolites. Our findings demonstrate the role of gut bacteria in detoxifying toxic secondary metabolites found in the N. glauca nectar. The degradation products may supply the birds with nitrogen which is scarce in nectar-rich diets. These findings support another role of bacteria in mediating the interactions between plants and their pollinators. Frontiers Media S.A. 2021-03-11 /pmc/articles/PMC8018289/ /pubmed/33815326 http://dx.doi.org/10.3389/fmicb.2021.639808 Text en Copyright © 2021 Gunasekaran, Trabelcy, Izhaki and Halpern. 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) and the copyright owner(s) 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
Gunasekaran, Mohanraj
Trabelcy, Beny
Izhaki, Ido
Halpern, Malka
Direct Evidence That Sunbirds’ Gut Microbiota Degrades Floral Nectar’s Toxic Alkaloids
title Direct Evidence That Sunbirds’ Gut Microbiota Degrades Floral Nectar’s Toxic Alkaloids
title_full Direct Evidence That Sunbirds’ Gut Microbiota Degrades Floral Nectar’s Toxic Alkaloids
title_fullStr Direct Evidence That Sunbirds’ Gut Microbiota Degrades Floral Nectar’s Toxic Alkaloids
title_full_unstemmed Direct Evidence That Sunbirds’ Gut Microbiota Degrades Floral Nectar’s Toxic Alkaloids
title_short Direct Evidence That Sunbirds’ Gut Microbiota Degrades Floral Nectar’s Toxic Alkaloids
title_sort direct evidence that sunbirds’ gut microbiota degrades floral nectar’s toxic alkaloids
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8018289/
https://www.ncbi.nlm.nih.gov/pubmed/33815326
http://dx.doi.org/10.3389/fmicb.2021.639808
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