Contrasting Effects of Environmental Concentrations of Sulfonamides on Microbial Heterotrophic Activities in Freshwater Sediments.

Stéphane Pesce,Laura Kergoat,Chloé Bonnineau,Laurianne Paris,Loren Billet,Pascale Besse-Hoggan

doi:10.3389/fmicb.2021.753647

Abstract

The sulfonamide antibiotics sulfamethoxazole (SMX) and sulfamethazine (SMZ) are regularly detected in surface sediments of contaminated hydrosystems, with maximum concentrations that can reach tens of μg kg–1 in stream and river sediments. Little is known about the resulting effects on the exposed benthic organisms. Here we investigated the functional response of stream sediment microbial communities exposed for 4 weeks to two levels of environmentally relevant concentrations of SMX and SMZ, tested individually. To this end, we developed a laboratory channel experiment where natural stream sediments were immersed in water contaminated with nominal environmental concentrations of 500 and 5,000 ng L–1 of SMX or SMZ, causing their accumulation in surface sediments. The mean maximum concentrations measured in the sediment (about 2.1 μg SMX kg–1 dw and 4.5 μg SMZ kg–1 dw) were consistent with those reported in contaminated rivers. The resulting chronic exposure had various effects on the functional potential of the sediment microbial communities, according to the substance (SMX or SMZ), the type of treatment (high or low) and the measured activity, with a strong influence of temporal dynamics. Whereas the SMZ treatments resulted in only transient effects on the five microbial activities investigated, we observed a significant stimulation of the β-glucosidase activity over the 28 days in the communities exposed to the high concentration of SMX. Together with the stimulation of aerobic respiration at low SMX concentrations and the reduced concentration observed in the last days, our results suggest a potential biodegradation of sulfonamides by microbial communities from sediments. Given the key functional role of surface sediment microbial communities in streams and rivers, our findings suggest that the frequently reported contamination of sediments by sulfonamides is likely to affect biogeochemical cycles, with possible impact on ecosystem functioning.

Highlights

Among contaminants of emerging concern, antibiotics are increasingly detected in aquatic ecosystems worldwide, reflecting their widespread use (Chen and Zhou, 2014; Kairigo et al, 2020; Bonnineau et al, 2021; Zheng et al, 2021)
Despite the lack of identified potential sources of contamination by sulfonamides in the sampled river section, a low concentration of SMZ was detected in the collected sediment (0.06 ± 0.10 μg kg−1 dw at D0; Figures 1B,D), while no SMX was detected
The SMZ and SMX analysis performed at D28 in the REF sediment confirmed the lack of SMX contamination and showed that SMZ concentrations in the non-spiked sediment were relatively stable over the experiment (0.10 ± 0.10 μg kg−1 dw at D28; data not shown)

Summary

Introduction

Among contaminants of emerging concern, antibiotics are increasingly detected in aquatic ecosystems worldwide, reflecting their widespread use (Chen and Zhou, 2014; Kairigo et al, 2020; Bonnineau et al, 2021; Zheng et al, 2021). Case reports and reviews on the contamination of these ecosystems by antibiotics show that sulfonamides, especially sulfamethoxazole (SMX) and sulfamethazine (SMZ), are among the most frequently detected substances (e.g., Kovalakova et al, 2020; Zheng et al, 2021). Owing to the frequent occurrence of SMZ and SMX in surface waters, there has been growing interest in assessing their toxicity toward various aquatic organisms. These include model species, such as the cyanobacterium Synechococcus leopoliensis, the protist Tetrahymena pyriformis, the microalga Pseudokirchneriella subcapitata and the crustacean Daphnia magna, with reported NOEC (no observed effect concentration) ranging from several μg L−1 to several mg L−1 (Yang et al, 2008; De Liguoro et al, 2009; Straub, 2016; U.S Environmental Protection Agency, 2019). Microbial communities are rarely taken into account in these types of test (Brandt et al, 2015), even though they are key players in a broad range of ecological processes that are essential to ecosystem functioning and that contribute to ecosystem services (Cavicchioli et al, 2019; Pesce et al, 2020)

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Results

Conclusion