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Response of antibiotic and heavy metal resistance genes to the co-occurrence of gadolinium and sulfamethoxazole in activated sludge systems

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Abstract

With the increasing use of antibiotics and rare earth elements (REE) during the coronavirus disease (COVID-19) pandemic, the co-occurrence of sulfamethoxazole (SMX) and gadolinium (Gd) has increased in wastewater treatment plants (WWTPs). However, the effects of SMX and Gd exposure on the transmission of antibiotic resistance genes (ARGs) and heavy metal resistance genes (MRGs) remain unknown. This study investigated the impacts of SMX and Gd on the fate of ARGs and MRGs in an activated sludge system. The diversity and relative abundance of ARGs, MRGs, and mobile genetic elements (MGEs) were detected by metagenomic sequencing. The results revealed an increased abundance of ARGs but a decreased abundance of MRGs under the joint effect of SMX and Gd. In addition, Gd alone exerted adverse effects on the proliferation and spread of ARGs and MRGs. However, SMX alone resulted in an increase in the diversity of ARGs and MRGs and promoted the growth of Pseudomonas, Thauera, and Streptomyces in the activated sludge system. Interestingly, a positive correlation was observed between most ARGs and MGEs. These findings provide comprehensive insights into the effects of co-occurring REEs and antibiotics on the fate of ARGs, MRGs, and MGEs, providing evidence to assist in controlling the spread and proliferation of ARGs and MRGs in activated sludge systems.

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References

  • Aguilar-Barajas E, Ramírez-Díaz M I, Riveros-Rosas H, Cervantes C (2010). Heavy Metal Resistance in Pseudomonads. Amsterdam: Springer, 255–282

    Google Scholar 

  • Altomare A J, Young N A, Beazley M J (2020). A preliminary survey of anthropogenic gadolinium in water and sediment of a constructed wetland. Journal of Environmental Management, 255: 109897

    Article  CAS  Google Scholar 

  • Barka E A, Vatsa P, Sanchez L, Gaveau-Vaillant N, Jacquard C, Klenk H P, Clément C, Ouhdouch Y, Van Wezel G P (2016). Taxonomy, physiology, and natural products of Actinobacteria. Microbiology and Molecular Biology Reviews, 80(1): 1–43

    Article  Google Scholar 

  • Bengtsson-Palme J, Hammaren R, Pal C, Östman M, Björlenius B, Flach C F, Fick J, Kristiansson E, Tysklind M, Larsson D J (2016). Elucidating selection processes for antibiotic resistance in sewage treatment plants using metagenomics. Science of the Total Environment, 572: 697–712

    Article  CAS  Google Scholar 

  • Braun M, Zavanyi G, Laczovics A, Berényi E, Szabó S (2018). Can aquatic macrophytes be biofilters for gadolinium based contrasting agents? Water Research, 135: 104–111

    Article  CAS  Google Scholar 

  • Button M, Cosway K, Sui J, Weber K (2019). Impacts and fate of triclosan and sulfamethoxazole in intensified re-circulating vertical flow constructed wetlands. Science of the Total Environment, 649: 1017–1028

    Article  CAS  Google Scholar 

  • Chen H, Chen R, Jing L, Bai X, Teng Y (2019). A metagenomic analysis framework for characterization of antibiotic resistomes in river environment: application to an urban river in Beijing. Environmental Pollution, 245: 398–407

    Article  CAS  Google Scholar 

  • Guo X, Yan Z, Zhang Y, Xu W, Kong D, Shan Z, Wang N (2018). Behavior of antibiotic resistance genes under extremely high-level antibiotic selection pressures in pharmaceutical wastewater treatment plants. Science of the Total Environment, 612: 119–128

    Article  CAS  Google Scholar 

  • Guo X, Zhu L, Zhong H, Li P, Zhang C, Wei D (2021). Response of antibiotic and heavy metal resistance genes to tetracyclines and copper in substrate-free hydroponic microcosms with Myriophyllum aquaticum. Journal of Hazardous Materials, 413: 125444

    Article  CAS  Google Scholar 

  • Gupta S, Graham D W, Sreekrishnan T, Ahammad S Z (2022). Effects of heavy metals pollution on the co-selection of metal and antibiotic resistance in urban rivers in UK and India. Environmental Pollution, 306: 119326

    Article  CAS  Google Scholar 

  • Indriolo E, Na G, Ellis D, Salt D E, Banks J A (2010). A vacuolar arsenite transporter necessary for arsenic tolerance in the arsenic hyperaccumulating fern Pteris vittata is missing in flowering plants. Plant Cell, 22(6): 2045–2057

    Article  CAS  Google Scholar 

  • Inoue K, Fukushi M, Sahoo S K, Veerasamy N, Furukawa A, Soyama S, Sakata A, Isoda R, Taguchi Y, Hosokawa S, et al. (2022). Measurements and future projections of Gd-based contrast agents for MRI exams in wastewater treatment plants in the Tokyo metropolitan area. Marine Pollution Bulletin, 174: 113259

    Article  CAS  Google Scholar 

  • Jami M, Ghanbari M, Kneifel W, Domig K J (2015). Phylogenetic diversity and biological activity of culturable Actinobacteria isolated from freshwater fish gut microbiota. Microbiological Research, 175: 6–15

    Article  Google Scholar 

  • Jia S, Shi P, Hu Q, Li B, Zhang T, Zhang X (2015). Bacterial community shift drives antibiotic resistance promotion during drinking water chlorination. Environmental Science & Technology, 49(20): 12271–12279

    Article  CAS  Google Scholar 

  • Karakoc Aydiner E, Bilgic Eltan S, Babayeva R, Aydiner O, Kepenekli E, Kolukisa B, Sefer A P, Yalcin Gungoren E, Karabiber E, Yucel E O, et al. (2022). Adverse COVID-19 outcomes in immune deficiencies: inequality exists between subclasses. Allergy, 77(1): 282–295

    Article  CAS  Google Scholar 

  • Karkman A, Johnson T A, Lyra C, Stedtfeld R D, Tamminen M, Tiedje J M, Virta M (2016). High-throughput quantification of antibiotic resistance genes from an urban wastewater treatment plant. FEMS Microbiology Ecology, 92(3): fiw014

    Article  Google Scholar 

  • Komijani M, Shamabadi N S, Shahin K, Eghbalpour F, Tahsili M R, Bahram M (2021). Heavy metal pollution promotes antibiotic resistance potential in the aquatic environment. Environmental Pollution, 274: 116569

    Article  CAS  Google Scholar 

  • Kruse T, Ratnadevi C M, Erikstad H A, Birkeland N K (2019). Complete genome sequence analysis of the thermoacidophilic verrucomicrobial methanotroph “us Methylacidiphilum kamchatksnss”Kaml and comparison with its closest relatives. BMC Genomics, 20(642): 1–15

    CAS  Google Scholar 

  • Li L, Xia Y, Zhang T (2017). Co-occurrence of antibiotic and metal resistance genes revealed in complete genome collection. ISME Journal, 11(3): 651–662

    Article  CAS  Google Scholar 

  • Li N, Chen J, Liu C, Yang J, Zhu C, Li H (2022). Cu and Zn exert a greater influence on antibiotic resistance and its transfer than doxycycline in agricultural soils. Journal of Hazardous Materials, 423: 127042

    Article  CAS  Google Scholar 

  • Lykoudi A, Frontistis Z, Vakros J, Manariotis I D, Mantzavinos D (2020). Degradation of sulfamethoxazole with persulfate using spent coffee grounds biochar as activator. Journal of Environmental Management, 271: 111022

    Article  CAS  Google Scholar 

  • Ma W, Ren Z, Yu L, Wu X, Yao Y, Zhang J, Guo J, Fan N, Jin R (2021). Deciphering the response of anammox process to heavy metal and antibiotic stress: arsenic enhances the permeability of extracellular polymeric substance and aggravates the inhibition of sulfamethoxazole. Chemical Engineering Journal, 426: 130815

    Article  CAS  Google Scholar 

  • Mao G, Wang D, Bai Y, Qu J (2023). Mitigating microbiological risks of potential pathogens carrying antibiotic resistance genes and virulence factors in receiving rivers: benefits of wastewater treatment plant upgrade. Frontiers of Environmental Science & Engineering, 17(7): 82

    Article  CAS  Google Scholar 

  • Otto K, Silhavy T J (2002). Surface sensing and adhesion of Escherichia coli controlled by the Cpx-signaling pathway. Proceedings of the National Academy of Sciences of the United States of America, 99(4): 2287–2292

    Article  CAS  Google Scholar 

  • Pagano G, Guida M, Tommasi F, Oral R (2015). Health effects and toxicity mechanisms of rare earth elements–knowledge gaps and research prospects. Ecotoxicology and Environmental Safety, 115: 40–48

    Article  CAS  Google Scholar 

  • Petersen C, Møller L B (2000). Control of copper homeostasis in Escherichia coli by a P-type ATPase, CopA, and a MerR-like transcriptional activator, CopR. Gene, 261(2): 289–298

    Article  CAS  Google Scholar 

  • Prigent-Combaret C, Brombacher E, Vidal O, Ambert A, Lejeune P, Landini P, Dorel C (2001). Complex regulatory network controls initial adhesion and biofilm formation in Escherichia coli via regulation of the csgD gene. Journal of Bacteriology, 183(24): 7213–7223

    Article  CAS  Google Scholar 

  • Reddy B, Dubey S K (2019). River Ganges water as reservoir of microbes with antibiotic and metal ion resistance genes: high throughput metagenomic approach. Environmental Pollution, 246: 443–451

    Article  CAS  Google Scholar 

  • Salam L B, Obayori O S, Ilori M O, Amund O O (2021). Acenaphthene biodegradation and structural and functional metagenomics of the microbial community of an acenaphthene-enriched animal charcoal polluted soil. Biocatalysis and Agricultural Biotechnology, 32: 101951

    Article  CAS  Google Scholar 

  • Song H, Shin W J, Ryu J S, Shin H S, Chung H, Lee K S (2017). Anthropogenic rare earth elements and their spatial distributions in the Han River, South Korea. Chemosphere, 172: 155–165

    Article  CAS  Google Scholar 

  • Sui Q, Chen Y, Yu D, Wang T, Hai Y, Zhang J, Chen M, Wei Y (2019). Fates of intracellular and extracellular antibiotic resistance genes and microbial community structures in typical swine wastewater treatment processes. Environment International, 133: 105183

    Article  CAS  Google Scholar 

  • Szekeres E, Baricz A, Chiriac C M, Farkas A, Opris O, Soran M L, Andrei A S, Rudi K, Balcázar J L, Dragos N, Coman C (2017). Abundance of antibiotics, antibiotic resistance genes and bacterial community composition in wastewater effluents from different Romanian hospitals. Environmental Pollution, 225: 304–315

    Article  CAS  Google Scholar 

  • Tang Y, Liang Z, Li G, Zhao H, An T (2021). Metagenomic profiles and health risks of pathogens and antibiotic resistance genes in various industrial wastewaters and the associated receiving surface water. Chemosphere, 283: 131224

    Article  CAS  Google Scholar 

  • ThomasIV J C, Oladeinde A, Kieran T J, FingerJr J W, Bayona-Vásquez N J, Cartee J C, Beasley J C, Seaman J C, Mcarthur J V, RhodesJr O E (2020). Co-occurrence of antibiotic, biocide, and heavy metal resistance genes in bacteria from metal and radionuclide contaminated soils at the Savannah River Site. Microbial Biotechnology, 13(4): 1179–1200

    Article  CAS  Google Scholar 

  • Wang J B, Li X, Zhou Z W, Fan X Y (2019). Bacterial communities, metabolic functions and resistance genes to antibiotics and metals in two saline seafood wastewater treatment systems. Bioresource Technology, 287: 121460

    Article  CAS  Google Scholar 

  • Wang X, Lan B, Fei H, Wang S, Zhu G (2021). Heavy metal could drive co-selection of antibiotic resistance in terrestrial subsurface soils. Journal of Hazardous Materials, 411: 124848

    Article  CAS  Google Scholar 

  • Weinreb J C, Rodby R A, Yee J, Wang C L, Fine D, Mcdonald R J, Perazella M A, Dillman J R, Davenport M S (2021). Use of intravenous gadolinium-based contrast media in patients with kidney disease: consensus statements from the American College of Radiology and the National Kidney Foundation. Radiology, 298(1): 28–35

    Article  Google Scholar 

  • Wen Q, Yang S, Chen Z (2021). Mesophilic and thermophilic anaerobic digestion of swine manure with sulfamethoxazole and norfloxacin: dynamics of microbial communities and evolution of resistance genes. Frontiers of Environmental Science & Engineering, 15(5): 94

    Article  CAS  Google Scholar 

  • Wu N, Xie S, Zeng M, Xu X, Li Y, Liu X, Wang X (2020). Impacts of pile temperature on antibiotic resistance, metal resistance and microbial community during swine manure composting. Science of the Total Environment, 744: 140920

    Article  CAS  Google Scholar 

  • Yang Y, Jiang X, Chai B, Ma L, Li B, Zhang A, Cole J R, Tiedje J M, Zhang T (2016). ARGs-OAP: online analysis pipeline for antibiotic resistance genes detection from metagenomic data using an integrated structured ARG-database. Bioinformatics (Oxford, England), 32(15): 2346–2351

    CAS  Google Scholar 

  • Yang Y, Li Z, Song W, Du L, Ye C, Zhao B, Liu W, Deng D, Pan Y, Lin H, et al. (2019). Metagenomic insights into the abundance and composition of resistance genes in aquatic environments: influence of stratification and geography. Environment International, 127: 371–380

    Article  CAS  Google Scholar 

  • Yin X, Jiang X T, Chai B, Li L, Yang Y, Cole J R, Tiedje J M, Zhang T (2018). ARGs-OAP v2.0 with an expanded SARG database and Hidden Markov Models for enhancement characterization and quantification of antibiotic resistance genes in environmental metagenomes. Bioinformatics (Oxford, England), 34(13): 2263–2270

    CAS  Google Scholar 

  • Yoo K, Yoo H, Lee J, Choi E J, Park J (2020). Exploring the antibiotic resistome in activated sludge and anaerobic digestion sludge in an urban wastewater treatment plant via metagenomic analysis. Journal of Microbiology (Seoul, Korea), 58(2): 123–130

    CAS  Google Scholar 

  • Zainab S M, Junaid M, Xu N, Malik R N (2020). Antibiotics and antibiotic resistant genes (ARGs) in groundwater: a global review on dissemination, sources, interactions, environmental and human health risks. Water Research, 187: 116455

    Article  CAS  Google Scholar 

  • Zhang M, Liu Y S, Zhao J L, Liu W R, He L Y, Zhang J N, Chen J, He L K, Zhang Q Q, Ying G G (2018a). Occurrence, fate and mass loadings of antibiotics in two swine wastewater treatment systems. Science of the Total Environment, 639: 1421–1431

    Article  CAS  Google Scholar 

  • Zhang Y, Gu A Z, Cen T, Li X, He M, Li D, Chen J (2018b). Subinhibitory concentrations of heavy metals facilitate the horizontal transfer of plasmid-mediated antibiotic resistance genes in water environment. Environmental Pollution, 237: 74–82

    Article  CAS  Google Scholar 

  • Zhao R, Yu K, Zhang J, Zhang G, Huang J, Ma L, Deng C, Li X, Li B (2020). Deciphering the mobility and bacterial hosts of antibiotic resistance genes under antibiotic selection pressure by metagenomic assembly and binning approaches. Water Research, 186: 116318

    Article  CAS  Google Scholar 

  • Zhao S N, Wu L L, Feng J, Song S Y, Zhang H J (2016). An ideal detector composed of a 3D Gd-based coordination polymer for DNA and Hg2+ ion. Inorganic Chemistry Frontiers, 3(3): 376–380

    Article  CAS  Google Scholar 

  • Zhou H, Cao Z, Zhang M, Ying Z, Ma L (2021). Zero-valent iron enhanced in-situ advanced anaerobic digestion for the removal of antibiotics and antibiotic resistance genes in sewage sludge. Science of the Total Environment, 754: 142077

    Article  CAS  Google Scholar 

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Acknowledgements

The work was supported by the National Key R&D Program of China (No. 2019YFC0408500). We thank Home for Researchers editorial team for language editing service.

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Authors and Affiliations

  1. School of Resources and Environmental Engineering, Hefei University of Technology, Hefei, 230009, China

    Xinrui Yuan, Kangping Cui, Yihan Chen, Shiyang Wu, Yao Zhang & Tong Liu

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  1. Xinrui Yuan
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  2. Kangping Cui
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  3. Yihan Chen
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  4. Shiyang Wu
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  5. Yao Zhang
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  6. Tong Liu
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Corresponding author

Correspondence to Kangping Cui.

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The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Highlights

• Co-occurrence of SMX and Gd(III) enhances HGT of ARGs and MRGs.

• Gd(III) alone negatively impacts ARGs and MRGs proliferation and spread.

• Streptomyces, Pseudomonas and Thauera were abundant in the presence of SMX.

• A positive correlation between internal ARGs and MGEs.

Electronic supplementary material

11783_2023_1754_MOESM1_ESM.pdf

Response of antibiotic and heavy metal resistance genes to the co-occurrence of gadolinium and sulfamethoxazole in activated sludge systems

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Yuan, X., Cui, K., Chen, Y. et al. Response of antibiotic and heavy metal resistance genes to the co-occurrence of gadolinium and sulfamethoxazole in activated sludge systems. Front. Environ. Sci. Eng. 17, 154 (2023). https://doi.org/10.1007/s11783-023-1754-5

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