Resistance and Vulnerability of Honeybee (Apis mellifera) Gut Bacteria to Commonly Used Pesticides

Agricultural and apicultural practices expose honeybees to a range of pesticides that have the potential to negatively affect their physiology, neurobiology, and behavior. Accumulating evidence suggests that these effects extend to the honeybee gut microbiome, which serves important functions for ho...

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Main Authors: Ana Cuesta-Maté, Justinn Renelies-Hamilton, Per Kryger, Annette Bruun Jensen, Veronica M. Sinotte, Michael Poulsen
Format: Article
Language:English
Published: Frontiers Media S.A. 2021-09-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2021.717990/full
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spelling doaj-5d57a704a9e24ccf912ffd3b80f7e9b02021-09-04T10:19:28ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2021-09-011210.3389/fmicb.2021.717990717990Resistance and Vulnerability of Honeybee (Apis mellifera) Gut Bacteria to Commonly Used PesticidesAna Cuesta-Maté0Justinn Renelies-Hamilton1Per Kryger2Annette Bruun Jensen3Veronica M. Sinotte4Michael Poulsen5Section for Ecology and Evolution, Department of Biology, University of Copenhagen, Copenhagen, DenmarkSection for Ecology and Evolution, Department of Biology, University of Copenhagen, Copenhagen, DenmarkEntomology and Plant Pathology, Department of Agroecology, Aarhus University, Aarhus, DenmarkSection for Organismal Biology, Department of Plant and Environmental Sciences, University of Copenhagen, Copenhagen, DenmarkSection for Ecology and Evolution, Department of Biology, University of Copenhagen, Copenhagen, DenmarkSection for Ecology and Evolution, Department of Biology, University of Copenhagen, Copenhagen, DenmarkAgricultural and apicultural practices expose honeybees to a range of pesticides that have the potential to negatively affect their physiology, neurobiology, and behavior. Accumulating evidence suggests that these effects extend to the honeybee gut microbiome, which serves important functions for honeybee health. Here we test the potential effects of the pesticides thiacloprid, acetamiprid, and oxalic acid on the gut microbiota of honeybees, first in direct in vitro inhibition assays and secondly in an in vivo caged bee experiment to test if exposure leads to gut microbiota community changes. We found that thiacloprid did not inhibit the honeybee core gut bacteria in vitro, nor did it affect overall community composition or richness in vivo. Acetamiprid did also not inhibit bacterial growth in vitro, but it did affect community structure within bees. The eight bacterial genera tested showed variable levels of susceptibility to oxalic acid in vitro. In vivo, treatment with this pesticide reduced amplicon sequence variant (ASV) richness and affected gut microbiome composition, with most marked impact on the common crop bacteria Lactobacillus kunkeei and the genus Bombella. We conducted network analyses which captured known associations between bacterial members and illustrated the sensitivity of the microbiome to environmental stressors. Our findings point to risks of honeybee exposure to oxalic acid, which has been deemed safe for use in treatment against Varroa mites in honeybee colonies, and we advocate for more extensive assessment of the long-term effects that it may have on honeybee health.https://www.frontiersin.org/articles/10.3389/fmicb.2021.717990/fullmicrobiomesymbiosisanthropogenic stressorsocial insectneonicotinoidacaricide
collection DOAJ
language English
format Article
sources DOAJ
author Ana Cuesta-Maté
Justinn Renelies-Hamilton
Per Kryger
Annette Bruun Jensen
Veronica M. Sinotte
Michael Poulsen
spellingShingle Ana Cuesta-Maté
Justinn Renelies-Hamilton
Per Kryger
Annette Bruun Jensen
Veronica M. Sinotte
Michael Poulsen
Resistance and Vulnerability of Honeybee (Apis mellifera) Gut Bacteria to Commonly Used Pesticides
Frontiers in Microbiology
microbiome
symbiosis
anthropogenic stressor
social insect
neonicotinoid
acaricide
author_facet Ana Cuesta-Maté
Justinn Renelies-Hamilton
Per Kryger
Annette Bruun Jensen
Veronica M. Sinotte
Michael Poulsen
author_sort Ana Cuesta-Maté
title Resistance and Vulnerability of Honeybee (Apis mellifera) Gut Bacteria to Commonly Used Pesticides
title_short Resistance and Vulnerability of Honeybee (Apis mellifera) Gut Bacteria to Commonly Used Pesticides
title_full Resistance and Vulnerability of Honeybee (Apis mellifera) Gut Bacteria to Commonly Used Pesticides
title_fullStr Resistance and Vulnerability of Honeybee (Apis mellifera) Gut Bacteria to Commonly Used Pesticides
title_full_unstemmed Resistance and Vulnerability of Honeybee (Apis mellifera) Gut Bacteria to Commonly Used Pesticides
title_sort resistance and vulnerability of honeybee (apis mellifera) gut bacteria to commonly used pesticides
publisher Frontiers Media S.A.
series Frontiers in Microbiology
issn 1664-302X
publishDate 2021-09-01
description Agricultural and apicultural practices expose honeybees to a range of pesticides that have the potential to negatively affect their physiology, neurobiology, and behavior. Accumulating evidence suggests that these effects extend to the honeybee gut microbiome, which serves important functions for honeybee health. Here we test the potential effects of the pesticides thiacloprid, acetamiprid, and oxalic acid on the gut microbiota of honeybees, first in direct in vitro inhibition assays and secondly in an in vivo caged bee experiment to test if exposure leads to gut microbiota community changes. We found that thiacloprid did not inhibit the honeybee core gut bacteria in vitro, nor did it affect overall community composition or richness in vivo. Acetamiprid did also not inhibit bacterial growth in vitro, but it did affect community structure within bees. The eight bacterial genera tested showed variable levels of susceptibility to oxalic acid in vitro. In vivo, treatment with this pesticide reduced amplicon sequence variant (ASV) richness and affected gut microbiome composition, with most marked impact on the common crop bacteria Lactobacillus kunkeei and the genus Bombella. We conducted network analyses which captured known associations between bacterial members and illustrated the sensitivity of the microbiome to environmental stressors. Our findings point to risks of honeybee exposure to oxalic acid, which has been deemed safe for use in treatment against Varroa mites in honeybee colonies, and we advocate for more extensive assessment of the long-term effects that it may have on honeybee health.
topic microbiome
symbiosis
anthropogenic stressor
social insect
neonicotinoid
acaricide
url https://www.frontiersin.org/articles/10.3389/fmicb.2021.717990/full
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