A low dose of an organophosphate insecticide causes dysbiosis and sex-dependent responses in the intestinal microbiota of the Japanese quail (Coturnix japonica)

Organophosphate insecticides have been directly or indirectly implicated in avian populations declining worldwide. Birds in agricultural environments are commonly exposed to these insecticides, mainly through ingestion of invertebrates after insecticide application. Despite insecticide exposure in b...

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Main Authors: Eduardo Crisol-Martínez, Laura T. Moreno-Moyano, Ngare Wilkinson, Tanka Prasai, Philip H. Brown, Robert J. Moore, Dragana Stanley
Format: Article
Language:English
Published: PeerJ Inc. 2016-05-01
Series:PeerJ
Subjects:
Online Access:https://peerj.com/articles/2002.pdf
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author Eduardo Crisol-Martínez
Laura T. Moreno-Moyano
Ngare Wilkinson
Tanka Prasai
Philip H. Brown
Robert J. Moore
Dragana Stanley
author_facet Eduardo Crisol-Martínez
Laura T. Moreno-Moyano
Ngare Wilkinson
Tanka Prasai
Philip H. Brown
Robert J. Moore
Dragana Stanley
author_sort Eduardo Crisol-Martínez
collection DOAJ
description Organophosphate insecticides have been directly or indirectly implicated in avian populations declining worldwide. Birds in agricultural environments are commonly exposed to these insecticides, mainly through ingestion of invertebrates after insecticide application. Despite insecticide exposure in birds occurring mostly by ingestion, the impact of organophosphates on the avian digestive system has been poorly researched. In this work we used the Japanese quail (Coturnix japonica) as an avian model to study short-term microbial community responses to a single dose of trichlorfon at low concentration in three sample origins of the gastrointestinal tract (GIT): caecum, large intestine and faeces. Using next-generation sequencing of 16S rRNA gene amplicons as bacterial markers, the study showed that ingestion of insecticide caused significant changes in the GIT microbiome. Specifically, microbiota composition and diversity differed between treated and untreated quail. Insecticide-associated responses in the caecum showed differences between sexes which did not occur with the other sample types. In caecal microbiota, only treated females showed significant shifts in a number of genera within the Lachnospiraceae and the Enterobacteriaceae families. The major responses in the large intestine were a significant reduction in the genus Lactobacillus and increases in abundance of a number of Proteobacteria genera. All microbial shifts in faeces occurred in phylotypes that were represented at low relative abundances. In general, changes in microbiota possibly resulted from contrasting responses towards the insecticide, either positive (e.g., biodegrading bacteria) or negative (e.g., insecticide-susceptible bacteria). This study demonstrates the significant impact that organophosphate insecticides have on the avian gut microbiota; showing that a single small dose of trichlorfon caused dysbiosis in the GIT of the Japanese quail. Further research is necessary to understand the implications on birds’ health, especially in females.
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spelling doaj.art-93f213ee4d4e4d629dc64955d494071b2023-12-03T11:06:04ZengPeerJ Inc.PeerJ2167-83592016-05-014e200210.7717/peerj.2002A low dose of an organophosphate insecticide causes dysbiosis and sex-dependent responses in the intestinal microbiota of the Japanese quail (Coturnix japonica)Eduardo Crisol-Martínez0Laura T. Moreno-Moyano1Ngare Wilkinson2Tanka Prasai3Philip H. Brown4Robert J. Moore5Dragana Stanley6School of Medical and Applied Sciences, Central Queensland University, Rockhampton, Queensland, AustraliaSchool of Biosciences, University of Melbourne, Parkville, Victoria, AustraliaSchool of Medical and Applied Sciences, Central Queensland University, Rockhampton, Queensland, AustraliaSchool of Medical and Applied Sciences, Central Queensland University, Rockhampton, Queensland, AustraliaSchool of Medical and Applied Sciences, Central Queensland University, Rockhampton, Queensland, AustraliaPoultry Cooperative Research Centre, University of New England, Armidale, New South Wales, AustraliaSchool of Medical and Applied Sciences, Central Queensland University, Rockhampton, Queensland, AustraliaOrganophosphate insecticides have been directly or indirectly implicated in avian populations declining worldwide. Birds in agricultural environments are commonly exposed to these insecticides, mainly through ingestion of invertebrates after insecticide application. Despite insecticide exposure in birds occurring mostly by ingestion, the impact of organophosphates on the avian digestive system has been poorly researched. In this work we used the Japanese quail (Coturnix japonica) as an avian model to study short-term microbial community responses to a single dose of trichlorfon at low concentration in three sample origins of the gastrointestinal tract (GIT): caecum, large intestine and faeces. Using next-generation sequencing of 16S rRNA gene amplicons as bacterial markers, the study showed that ingestion of insecticide caused significant changes in the GIT microbiome. Specifically, microbiota composition and diversity differed between treated and untreated quail. Insecticide-associated responses in the caecum showed differences between sexes which did not occur with the other sample types. In caecal microbiota, only treated females showed significant shifts in a number of genera within the Lachnospiraceae and the Enterobacteriaceae families. The major responses in the large intestine were a significant reduction in the genus Lactobacillus and increases in abundance of a number of Proteobacteria genera. All microbial shifts in faeces occurred in phylotypes that were represented at low relative abundances. In general, changes in microbiota possibly resulted from contrasting responses towards the insecticide, either positive (e.g., biodegrading bacteria) or negative (e.g., insecticide-susceptible bacteria). This study demonstrates the significant impact that organophosphate insecticides have on the avian gut microbiota; showing that a single small dose of trichlorfon caused dysbiosis in the GIT of the Japanese quail. Further research is necessary to understand the implications on birds’ health, especially in females.https://peerj.com/articles/2002.pdfMicrobiotaIntestinalJapanese quailOrganophosphateInsecticideDysbiosis
spellingShingle Eduardo Crisol-Martínez
Laura T. Moreno-Moyano
Ngare Wilkinson
Tanka Prasai
Philip H. Brown
Robert J. Moore
Dragana Stanley
A low dose of an organophosphate insecticide causes dysbiosis and sex-dependent responses in the intestinal microbiota of the Japanese quail (Coturnix japonica)
PeerJ
Microbiota
Intestinal
Japanese quail
Organophosphate
Insecticide
Dysbiosis
title A low dose of an organophosphate insecticide causes dysbiosis and sex-dependent responses in the intestinal microbiota of the Japanese quail (Coturnix japonica)
title_full A low dose of an organophosphate insecticide causes dysbiosis and sex-dependent responses in the intestinal microbiota of the Japanese quail (Coturnix japonica)
title_fullStr A low dose of an organophosphate insecticide causes dysbiosis and sex-dependent responses in the intestinal microbiota of the Japanese quail (Coturnix japonica)
title_full_unstemmed A low dose of an organophosphate insecticide causes dysbiosis and sex-dependent responses in the intestinal microbiota of the Japanese quail (Coturnix japonica)
title_short A low dose of an organophosphate insecticide causes dysbiosis and sex-dependent responses in the intestinal microbiota of the Japanese quail (Coturnix japonica)
title_sort low dose of an organophosphate insecticide causes dysbiosis and sex dependent responses in the intestinal microbiota of the japanese quail coturnix japonica
topic Microbiota
Intestinal
Japanese quail
Organophosphate
Insecticide
Dysbiosis
url https://peerj.com/articles/2002.pdf
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