Mechanism of the Synergistic Toxicity of Ampicillin and Cefazoline on <i>Selenastrum capricornutum</i>

Ampicillin (AMP) and cefazolin (CZO) are commonly used β-lactam antibiotics which are extensively globally produced. Additionally, AMP and CZO are known to have relatively high ecotoxicity. Notably, the mix of AMP and CZO creates a synergistic effect that is more harmful to the environment, and how...

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Main Authors: Feng-Ling Huang, Li-Tang Qin, Ling-Yun Mo, Hong-Hu Zeng, Yan-Peng Liang
Format: Article
Language:English
Published: MDPI AG 2024-03-01
Series:Toxics
Subjects:
Online Access:https://www.mdpi.com/2305-6304/12/3/217
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author Feng-Ling Huang
Li-Tang Qin
Ling-Yun Mo
Hong-Hu Zeng
Yan-Peng Liang
author_facet Feng-Ling Huang
Li-Tang Qin
Ling-Yun Mo
Hong-Hu Zeng
Yan-Peng Liang
author_sort Feng-Ling Huang
collection DOAJ
description Ampicillin (AMP) and cefazolin (CZO) are commonly used β-lactam antibiotics which are extensively globally produced. Additionally, AMP and CZO are known to have relatively high ecotoxicity. Notably, the mix of AMP and CZO creates a synergistic effect that is more harmful to the environment, and how exposure to AMP-CZO can induce synergism in algae remains virtually unknown. To yield comprehensive mechanistic insights into chemical toxicity, including dose–response relationships and variations in species sensitivity, the integration of multiple endpoints with de novo transcriptomics analyses were used in this study. We employed <i>Selenastrum capricornutum</i> to investigate its toxicological responses to AMP and CZO at various biological levels, with the aim of elucidating the underlying mechanisms. Our assessment of multiple endpoints revealed a significant growth inhibition in response to AMP at the relevant concentrations. This inhibition was associated with increased levels of reactive oxygen species (ROS) and perturbations in nitrogen metabolism, carbohydrate metabolism, and energy metabolism. Growth inhibition in the presence of CZO and the AMP-CZO combination was linked to reduced viability levels, elevated ROS production, decreased total soluble protein content, inhibited photosynthesis, and disruptions in the key signaling pathways related to starch and sucrose metabolism, ribosome function, amino acid biosynthesis, and the production of secondary metabolites. It was concluded from the physiological level that the synergistic effect of Chlorophyll a (Chla) and Superoxide dismutase (SOD) activity strengthened the growth inhibition of <i>S. capricornutum</i> in the AMP-CZO synergistic group. According to the results of transcriptomic analysis, the simultaneous down-regulation of <i>LHCA4</i>, <i>LHCA1</i>, <i>LHCA5,</i> and <i>sodA</i> destroyed the functions of the photosynthetic system and the antioxidant system, respectively. Such information is invaluable for environmental risk assessments. The results provided critical knowledge for a better understanding of the potential ecological impacts of these antibiotics on non-target organisms.
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spelling doaj.art-1b942246ad5b4aea898695fec08ddf6c2024-03-27T14:06:15ZengMDPI AGToxics2305-63042024-03-0112321710.3390/toxics12030217Mechanism of the Synergistic Toxicity of Ampicillin and Cefazoline on <i>Selenastrum capricornutum</i>Feng-Ling Huang0Li-Tang Qin1Ling-Yun Mo2Hong-Hu Zeng3Yan-Peng Liang4College of Environment Science and Engineering, Guilin University of Technology, Guilin 541004, ChinaCollege of Environment Science and Engineering, Guilin University of Technology, Guilin 541004, ChinaGuangxi Key Laboratory of Theory and Technology for Environmental Pollution Control, Guilin University of Technology, Guilin 541006, ChinaCollege of Environment Science and Engineering, Guilin University of Technology, Guilin 541004, ChinaCollege of Environment Science and Engineering, Guilin University of Technology, Guilin 541004, ChinaAmpicillin (AMP) and cefazolin (CZO) are commonly used β-lactam antibiotics which are extensively globally produced. Additionally, AMP and CZO are known to have relatively high ecotoxicity. Notably, the mix of AMP and CZO creates a synergistic effect that is more harmful to the environment, and how exposure to AMP-CZO can induce synergism in algae remains virtually unknown. To yield comprehensive mechanistic insights into chemical toxicity, including dose–response relationships and variations in species sensitivity, the integration of multiple endpoints with de novo transcriptomics analyses were used in this study. We employed <i>Selenastrum capricornutum</i> to investigate its toxicological responses to AMP and CZO at various biological levels, with the aim of elucidating the underlying mechanisms. Our assessment of multiple endpoints revealed a significant growth inhibition in response to AMP at the relevant concentrations. This inhibition was associated with increased levels of reactive oxygen species (ROS) and perturbations in nitrogen metabolism, carbohydrate metabolism, and energy metabolism. Growth inhibition in the presence of CZO and the AMP-CZO combination was linked to reduced viability levels, elevated ROS production, decreased total soluble protein content, inhibited photosynthesis, and disruptions in the key signaling pathways related to starch and sucrose metabolism, ribosome function, amino acid biosynthesis, and the production of secondary metabolites. It was concluded from the physiological level that the synergistic effect of Chlorophyll a (Chla) and Superoxide dismutase (SOD) activity strengthened the growth inhibition of <i>S. capricornutum</i> in the AMP-CZO synergistic group. According to the results of transcriptomic analysis, the simultaneous down-regulation of <i>LHCA4</i>, <i>LHCA1</i>, <i>LHCA5,</i> and <i>sodA</i> destroyed the functions of the photosynthetic system and the antioxidant system, respectively. Such information is invaluable for environmental risk assessments. The results provided critical knowledge for a better understanding of the potential ecological impacts of these antibiotics on non-target organisms.https://www.mdpi.com/2305-6304/12/3/217β-lactam antibioticsphotosynthetic systemantioxidant systemtranscriptomics analysis
spellingShingle Feng-Ling Huang
Li-Tang Qin
Ling-Yun Mo
Hong-Hu Zeng
Yan-Peng Liang
Mechanism of the Synergistic Toxicity of Ampicillin and Cefazoline on <i>Selenastrum capricornutum</i>
Toxics
β-lactam antibiotics
photosynthetic system
antioxidant system
transcriptomics analysis
title Mechanism of the Synergistic Toxicity of Ampicillin and Cefazoline on <i>Selenastrum capricornutum</i>
title_full Mechanism of the Synergistic Toxicity of Ampicillin and Cefazoline on <i>Selenastrum capricornutum</i>
title_fullStr Mechanism of the Synergistic Toxicity of Ampicillin and Cefazoline on <i>Selenastrum capricornutum</i>
title_full_unstemmed Mechanism of the Synergistic Toxicity of Ampicillin and Cefazoline on <i>Selenastrum capricornutum</i>
title_short Mechanism of the Synergistic Toxicity of Ampicillin and Cefazoline on <i>Selenastrum capricornutum</i>
title_sort mechanism of the synergistic toxicity of ampicillin and cefazoline on i selenastrum capricornutum i
topic β-lactam antibiotics
photosynthetic system
antioxidant system
transcriptomics analysis
url https://www.mdpi.com/2305-6304/12/3/217
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