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

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          Abstract

          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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            The large majority of antibiotics currently used for treating infections and the antibiotic resistance genes acquired by human pathogens each have an environmental origin. Recent work indicates that the function of these elements in their environmental reservoirs may be very distinct from the "weapon-shield" role they play in clinical settings. Changes in natural ecosystems, including the release of large amounts of antimicrobials, might alter the population dynamics of microorganisms, including selection of resistance, with consequences for human health that are difficult to predict.
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                Author and article information

                Contributors
                Journal
                Front Microbiol
                Front Microbiol
                Front. Microbiol.
                Frontiers in Microbiology
                Frontiers Media S.A.
                1664-302X
                07 May 2021
                2021
                : 12
                : 643719
                Affiliations
                [1] 1INRAE, UR RiverLy , Villeurbanne, France
                [2] 2Université Clermont Auvergne, CNRS, Sigma Clermont, Institut de Chimie de Clermont-Ferrand , Clermont–Ferrand, France
                [3] 3AgroSup Dijon, INRAE, Univ. Bourgogne Franche-Comté, Agroécologie , Dijon, France
                [4] 4INRAE, UR EABX , Cestas, France
                Author notes

                Edited by: Obulisamy Parthiba Karthikeyan, University of Houston, United States

                Reviewed by: Nikolina Udikovic-Kolic, Rudjer Boskovic Institute, Croatia; Yuyi Yang, Chinese Academy of Sciences, China

                *Correspondence: Chloé Bonnineau, chloe.bonnineau@ 123456inrae.fr

                This article was submitted to Microbiotechnology, a section of the journal Frontiers in Microbiology

                Article
                10.3389/fmicb.2021.643719
                8137839
                34025605
                a9116788-d8b1-42c8-bfa3-8cffc402ee5d
                Copyright © 2021 Kergoat, Besse-Hoggan, Leremboure, Beguet, Devers, Martin-Laurent, Masson, Morin, Roinat, Pesce and Bonnineau.

                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.

                History
                : 18 December 2020
                : 22 February 2021
                Page count
                Figures: 3, Tables: 3, Equations: 0, References: 71, Pages: 12, Words: 0
                Categories
                Microbiology
                Original Research

                Microbiology & Virology
                periphyton,antibiotic,teratogenicity,microbial ecotoxicology,sulfamethazine,sulfamethoxazole

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