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Environmental Concentrations of Sulfonamides Can Alter Bacterial Structure and Induce Diatom Deformities in Freshwater Biofilm Communities

Since the early 1920s, the intensive use of antibiotics has led to the contamination of the aquatic environment through diffuse sources and wastewater effluents. The antibiotics commonly found in surface waters include sulfamethoxazole (SMX) and sulfamethazine (SMZ), which belong to the class of sul...

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Autores principales: Kergoat, Laura, Besse-Hoggan, Pascale, Leremboure, Martin, Beguet, Jérémie, Devers, Marion, Martin-Laurent, Fabrice, Masson, Matthieu, Morin, Soizic, Roinat, Amélie, Pesce, Stéphane, Bonnineau, Chloé
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8137839/
https://www.ncbi.nlm.nih.gov/pubmed/34025605
http://dx.doi.org/10.3389/fmicb.2021.643719
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author Kergoat, Laura
Besse-Hoggan, Pascale
Leremboure, Martin
Beguet, Jérémie
Devers, Marion
Martin-Laurent, Fabrice
Masson, Matthieu
Morin, Soizic
Roinat, Amélie
Pesce, Stéphane
Bonnineau, Chloé
author_facet Kergoat, Laura
Besse-Hoggan, Pascale
Leremboure, Martin
Beguet, Jérémie
Devers, Marion
Martin-Laurent, Fabrice
Masson, Matthieu
Morin, Soizic
Roinat, Amélie
Pesce, Stéphane
Bonnineau, Chloé
author_sort Kergoat, Laura
collection PubMed
description Since the early 1920s, the intensive use of antibiotics has led to the contamination of the aquatic environment through diffuse sources and wastewater effluents. The antibiotics commonly found in surface waters include sulfamethoxazole (SMX) and sulfamethazine (SMZ), which belong to the class of sulfonamides, the oldest antibiotic class still in use. These antibiotics have been detected in all European surface waters with median concentrations of around 50 ng L(–1) and peak concentrations of up to 4–6 μg L(–1). Sulfonamides are known to inhibit bacterial growth by altering microbial production of folic acid, but sub-lethal doses may trigger antimicrobial resistance, with unknown consequences for exposed microbial communities. We investigated the effects of two environmentally relevant concentrations (500 and 5,000 ng L(–1)) of SMZ and SMX on microbial activity and structure of periphytic biofilms in stream mesocosms for 28 days. Measurement of sulfonamides in the mesocosms revealed contamination levels of about half the nominal concentrations. Exposure to sulfonamides led to slight, transitory effects on heterotrophic functions, but persistent effects were observed on the bacterial structure. After 4 weeks of exposure, sulfonamides also altered the autotrophs in periphyton and particularly the diversity, viability and cell integrity of the diatom community. The higher concentration of SMX tested decreased both diversity (Shannon index) and evenness of the diatom community. Exposure to SMZ reduced diatom species richness and diversity. The mortality of diatoms in biofilms exposed to sulfonamides was twice that in non-exposed biofilms. SMZ also induced an increase in diatom teratologies from 1.1% in non-exposed biofilms up to 3% in biofilms exposed to SMZ. To our knowledge, this is the first report on the teratological effects of sulfonamides on diatoms within periphyton. The increase of both diatom growth rate and mortality suggests a high renewal of diatoms under sulfonamide exposure. In conclusion, our study shows that sulfonamides can alter microbial community structures and diversity at concentrations currently present in the environment, with unknown consequences for the ecosystem. The experimental set-up presented here emphasizes the interest of using natural communities to increase the ecological realism of ecotoxicological studies and to detect potential toxic effects on non-target species.
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spelling pubmed-81378392021-05-22 Environmental Concentrations of Sulfonamides Can Alter Bacterial Structure and Induce Diatom Deformities in Freshwater Biofilm Communities Kergoat, Laura Besse-Hoggan, Pascale Leremboure, Martin Beguet, Jérémie Devers, Marion Martin-Laurent, Fabrice Masson, Matthieu Morin, Soizic Roinat, Amélie Pesce, Stéphane Bonnineau, Chloé Front Microbiol Microbiology Since the early 1920s, the intensive use of antibiotics has led to the contamination of the aquatic environment through diffuse sources and wastewater effluents. The antibiotics commonly found in surface waters include sulfamethoxazole (SMX) and sulfamethazine (SMZ), which belong to the class of sulfonamides, the oldest antibiotic class still in use. These antibiotics have been detected in all European surface waters with median concentrations of around 50 ng L(–1) and peak concentrations of up to 4–6 μg L(–1). Sulfonamides are known to inhibit bacterial growth by altering microbial production of folic acid, but sub-lethal doses may trigger antimicrobial resistance, with unknown consequences for exposed microbial communities. We investigated the effects of two environmentally relevant concentrations (500 and 5,000 ng L(–1)) of SMZ and SMX on microbial activity and structure of periphytic biofilms in stream mesocosms for 28 days. Measurement of sulfonamides in the mesocosms revealed contamination levels of about half the nominal concentrations. Exposure to sulfonamides led to slight, transitory effects on heterotrophic functions, but persistent effects were observed on the bacterial structure. After 4 weeks of exposure, sulfonamides also altered the autotrophs in periphyton and particularly the diversity, viability and cell integrity of the diatom community. The higher concentration of SMX tested decreased both diversity (Shannon index) and evenness of the diatom community. Exposure to SMZ reduced diatom species richness and diversity. The mortality of diatoms in biofilms exposed to sulfonamides was twice that in non-exposed biofilms. SMZ also induced an increase in diatom teratologies from 1.1% in non-exposed biofilms up to 3% in biofilms exposed to SMZ. To our knowledge, this is the first report on the teratological effects of sulfonamides on diatoms within periphyton. The increase of both diatom growth rate and mortality suggests a high renewal of diatoms under sulfonamide exposure. In conclusion, our study shows that sulfonamides can alter microbial community structures and diversity at concentrations currently present in the environment, with unknown consequences for the ecosystem. The experimental set-up presented here emphasizes the interest of using natural communities to increase the ecological realism of ecotoxicological studies and to detect potential toxic effects on non-target species. Frontiers Media S.A. 2021-05-07 /pmc/articles/PMC8137839/ /pubmed/34025605 http://dx.doi.org/10.3389/fmicb.2021.643719 Text en Copyright © 2021 Kergoat, Besse-Hoggan, Leremboure, Beguet, Devers, Martin-Laurent, Masson, Morin, Roinat, Pesce and Bonnineau. https://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
Kergoat, Laura
Besse-Hoggan, Pascale
Leremboure, Martin
Beguet, Jérémie
Devers, Marion
Martin-Laurent, Fabrice
Masson, Matthieu
Morin, Soizic
Roinat, Amélie
Pesce, Stéphane
Bonnineau, Chloé
Environmental Concentrations of Sulfonamides Can Alter Bacterial Structure and Induce Diatom Deformities in Freshwater Biofilm Communities
title Environmental Concentrations of Sulfonamides Can Alter Bacterial Structure and Induce Diatom Deformities in Freshwater Biofilm Communities
title_full Environmental Concentrations of Sulfonamides Can Alter Bacterial Structure and Induce Diatom Deformities in Freshwater Biofilm Communities
title_fullStr Environmental Concentrations of Sulfonamides Can Alter Bacterial Structure and Induce Diatom Deformities in Freshwater Biofilm Communities
title_full_unstemmed Environmental Concentrations of Sulfonamides Can Alter Bacterial Structure and Induce Diatom Deformities in Freshwater Biofilm Communities
title_short Environmental Concentrations of Sulfonamides Can Alter Bacterial Structure and Induce Diatom Deformities in Freshwater Biofilm Communities
title_sort environmental concentrations of sulfonamides can alter bacterial structure and induce diatom deformities in freshwater biofilm communities
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8137839/
https://www.ncbi.nlm.nih.gov/pubmed/34025605
http://dx.doi.org/10.3389/fmicb.2021.643719
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