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

doi:10.1007/s11783-023-1754-5

Front. Environ. Sci. Eng.

2023, Vol. 17

Issue (12) : 154 https://doi.org/10.1007/s11783-023-1754-5

RESEARCH ARTICLE

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

Xinrui Yuan, Kangping Cui(

), Yihan Chen, Shiyang Wu, Yao Zhang, Tong Liu

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

Download: PDF(7055 KB) HTML
Export: BibTeX | EndNote | Reference Manager | ProCite | RefWorks

Abstract

● 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.

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.

Keywords Antibiotic resistance genes Heavy metal resistance genes Mobile genetic elements Joint effect Activated sludge system

Corresponding Author(s): Kangping Cui

Issue Date: 24 July 2023

Cite this article:

Xinrui Yuan,Kangping Cui,Yihan Chen, et al. Response of antibiotic and heavy metal resistance genes to the co-occurrence of gadolinium and sulfamethoxazole in activated sludge systems[J]. Front. Environ. Sci. Eng., 2023, 17(12): 154.

URL:

https://academic.hep.com.cn/fese/EN/10.1007/s11783-023-1754-5
https://academic.hep.com.cn/fese/EN/Y2023/V17/I12/154

Fig.1 The composition and relative abundance of (a) ARGs, (b) MRGs, and (c) MGEs (top 20 subtypes) in all samples. R0: control group. R1: exposure to SMX alone. R2: exposure to SMX and Gd(III). R3: exposure to Gd(III) alone.

Fig.2 Principal coordinates analysis (PCoA) of (a) ARGs, (b) MRGs, and (c) MGEs.

Fig.3 Subtypes of core (a) ARGs, (b) MRGs, and (c) MGEs. The total abundance of core (d) ARGs, (e) MRGs, and (f) MGEs.

Fig.4 Relative abundance of abundant genera in four activated sludge systems.

Fig.5 Correlation heatmap of (a) ARGs vs ARGs, (b) MRGs vs MRGs, (c) MGEs vs MGEs. Network analysis showing the co-occurrence of (d) ARGs, MRGs, and MGEs. The edge width and node size are proportional to the correlation coefficients and connection numbers, respectively. The correlation combination analysis shows the correlation of ARGs, MRGs, and abundant genera. The area of the ellipse represents the strength of the correlation, and the direction represents positive or negative correlation.

1	E Aguilar-BarajasM I Ramírez-DíazH Riveros-RosasC Cervantes (2010). Heavy Metal Resistance in Pseudomonads. Amsterdam: Springer, 255–282
2	A J Altomare , N A Young , M J Beazley . (2020). A preliminary survey of anthropogenic gadolinium in water and sediment of a constructed wetland. Journal of Environmental Management, 255: 109897 https://doi.org/10.1016/j.jenvman.2019.109897
3	E A Barka , P Vatsa , L Sanchez , N Gaveau-Vaillant , C Jacquard , H P Klenk , C Clément , Y Ouhdouch , Wezel G P Van . (2016). Taxonomy, physiology, and natural products of Actinobacteria. Microbiology and Molecular Biology Reviews, 80(1): 1–43 https://doi.org/10.1128/MMBR.00019-15
4	J Bengtsson-Palme , R Hammaren , C Pal , M Östman , B Björlenius , C F Flach , J Fick , E Kristiansson , M Tysklind , D J Larsson . (2016). Elucidating selection processes for antibiotic resistance in sewage treatment plants using metagenomics. Science of the Total Environment, 572: 697–712 https://doi.org/10.1016/j.scitotenv.2016.06.228
5	M BraunG ZavanyiA LaczovicsE BerényiS Szabó (2018). Can aquatic macrophytes be biofilters for gadolinium based contrasting agents? Water Research, 135: 104–111
6	M Button , K Cosway , J Sui , K Weber . (2019). Impacts and fate of triclosan and sulfamethoxazole in intensified re-circulating vertical flow constructed wetlands. Science of the Total Environment, 649: 1017–1028 https://doi.org/10.1016/j.scitotenv.2018.08.395
7	H Chen , R Chen , L Jing , X Bai , Y Teng . (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 https://doi.org/10.1016/j.envpol.2018.11.024
8	X Guo , Z Yan , Y Zhang , W Xu , D Kong , Z Shan , N Wang . (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 https://doi.org/10.1016/j.scitotenv.2017.08.229
9	X Guo , L Zhu , H Zhong , P Li , C Zhang , D Wei . (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 https://doi.org/10.1016/j.jhazmat.2021.125444
10	S Gupta , D W Graham , T Sreekrishnan , S Z Ahammad . (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 https://doi.org/10.1016/j.envpol.2022.119326
11	E Indriolo , G Na , D Ellis , D E Salt , J A Banks . (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 https://doi.org/10.1105/tpc.109.069773
12	K Inoue , M Fukushi , S K Sahoo , N Veerasamy , A Furukawa , S Soyama , A Sakata , R Isoda , Y Taguchi , S Hosokawa . 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 https://doi.org/10.1016/j.marpolbul.2021.113259
13	M Jami , M Ghanbari , W Kneifel , K J Domig . (2015). Phylogenetic diversity and biological activity of culturable Actinobacteria isolated from freshwater fish gut microbiota. Microbiological Research, 175: 6–15 https://doi.org/10.1016/j.micres.2015.01.009
14	S Jia , P Shi , Q Hu , B Li , T Zhang , X Zhang . (2015). Bacterial community shift drives antibiotic resistance promotion during drinking water chlorination. Environmental Science & Technology, 49(20): 12271–12279 https://doi.org/10.1021/acs.est.5b03521
15	Aydiner E Karakoc , Eltan S Bilgic , R Babayeva , O Aydiner , E Kepenekli , B Kolukisa , A P Sefer , Gungoren E Yalcin , E Karabiber , E O Yucel . et al.. (2022). Adverse COVID-19 outcomes in immune deficiencies: inequality exists between subclasses. Allergy, 77(1): 282–295 https://doi.org/10.1111/all.15025
16	A Karkman , T A Johnson , C Lyra , R D Stedtfeld , M Tamminen , J M Tiedje , M Virta . (2016). High-throughput quantification of antibiotic resistance genes from an urban wastewater treatment plant. FEMS Microbiology Ecology, 92(3): fiw014 https://doi.org/10.1093/femsec/fiw014
17	M Komijani , N S Shamabadi , K Shahin , F Eghbalpour , M R Tahsili , M Bahram . (2021). Heavy metal pollution promotes antibiotic resistance potential in the aquatic environment. Environmental Pollution, 274: 116569 https://doi.org/10.1016/j.envpol.2021.116569
18	T Kruse , C M Ratnadevi , H A Erikstad , N K Birkeland . (2019). Complete genome sequence analysis of the thermoacidophilic verrucomicrobial methanotroph “Candidatus Methylacidiphilum kamchatkense” strain Kam1 and comparison with its closest relatives. BMC Genomics, 20(642): 1–15 https://doi.org/10.1186/s12864-019-5995-4
19	L Li , Y Xia , T Zhang . (2017). Co-occurrence of antibiotic and metal resistance genes revealed in complete genome collection. ISME Journal, 11(3): 651–662 https://doi.org/10.1038/ismej.2016.155
20	N Li , J Chen , C Liu , J Yang , C Zhu , H Li . (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 https://doi.org/10.1016/j.jhazmat.2021.127042
21	A Lykoudi , Z Frontistis , J Vakros , I D Manariotis , D Mantzavinos . (2020). Degradation of sulfamethoxazole with persulfate using spent coffee grounds biochar as activator. Journal of Environmental Management, 271: 111022 https://doi.org/10.1016/j.jenvman.2020.111022
22	W Ma , Z Ren , L Yu , X Wu , Y Yao , J Zhang , J Guo , N Fan , R Jin . (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 https://doi.org/10.1016/j.cej.2021.130815
23	G Mao , D Wang , Y Bai , J Qu . (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 https://doi.org/10.1007/s11783-023-1682
24	K Otto , T J Silhavy . (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 https://doi.org/10.1073/pnas.042521699
25	G Pagano , M Guida , F Tommasi , R Oral . (2015). Health effects and toxicity mechanisms of rare earth elements—knowledge gaps and research prospects. Ecotoxicology and Environmental Safety, 115: 40–48 https://doi.org/10.1016/j.ecoenv.2015.01.030
26	C Petersen , L B Møller . (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 https://doi.org/10.1016/S0378-1119(00)00509-6
27	C Prigent-Combaret , E Brombacher , O Vidal , A Ambert , P Lejeune , P Landini , C Dorel . (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 https://doi.org/10.1128/JB.183.24.7213-7223.2001
28	B Reddy , S K Dubey . (2019). River Ganges water as reservoir of microbes with antibiotic and metal ion resistance genes: high throughput metagenomic approach. Environmental Pollution, 246: 443–451 https://doi.org/10.1016/j.envpol.2018.12.022
29	L B Salam , O S Obayori , M O Ilori , O O Amund . (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 https://doi.org/10.1016/j.bcab.2021.101951
30	H Song , W J Shin , J S Ryu , H S Shin , H Chung , K S Lee . (2017). Anthropogenic rare earth elements and their spatial distributions in the Han River, South Korea. Chemosphere, 172: 155–165 https://doi.org/10.1016/j.chemosphere.2016.12.135
31	Q Sui , Y Chen , D Yu , T Wang , Y Hai , J Zhang , M Chen , Y Wei . (2019). Fates of intracellular and extracellular antibiotic resistance genes and microbial community structures in typical swine wastewater treatment processes. Environment International, 133: 105183 https://doi.org/10.1016/j.envint.2019.105183
32	E Szekeres , A Baricz , C M Chiriac , A Farkas , O Opris , M L Soran , A S Andrei , K Rudi , J L Balcázar , N Dragos , C Coman . (2017). Abundance of antibiotics, antibiotic resistance genes and bacterial community composition in wastewater effluents from different Romanian hospitals. Environmental Pollution, 225: 304–315 https://doi.org/10.1016/j.envpol.2017.01.054
33	Y Tang , Z Liang , G Li , H Zhao , T An . (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 https://doi.org/10.1016/j.chemosphere.2021.131224
34	IV J C Thomas , A Oladeinde , T J Kieran , Jr J W Finger , N J Bayona-Vásquez , J C Cartee , J C Beasley , J C Seaman , J V Mcarthur , Jr O E Rhodes . (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 https://doi.org/10.1111/1751-7915.13578
35	J B Wang , X Li , Z W Zhou , X Y Fan . (2019). Bacterial communities, metabolic functions and resistance genes to antibiotics and metals in two saline seafood wastewater treatment systems. Bioresource Technology, 287: 121460 https://doi.org/10.1016/j.biortech.2019.121460
36	X Wang , B Lan , H Fei , S Wang , G Zhu . (2021). Heavy metal could drive co-selection of antibiotic resistance in terrestrial subsurface soils. Journal of Hazardous Materials, 411: 124848 https://doi.org/10.1016/j.jhazmat.2020.124848
37	J C Weinreb , R A Rodby , J Yee , C L Wang , D Fine , R J Mcdonald , M A Perazella , J R Dillman , M S Davenport . (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 https://doi.org/10.1148/radiol.2020202903
38	Q Wen , S Yang , Z Chen . (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 https://doi.org/10.1007/s11783-020-1342-x
39	N Wu , S Xie , M Zeng , X Xu , Y Li , X Liu , X Wang . (2020). Impacts of pile temperature on antibiotic resistance, metal resistance and microbial community during swine manure composting. Science of the Total Environment, 744: 140920 https://doi.org/10.1016/j.scitotenv.2020.140920
40	Y Yang , X Jiang , B Chai , L Ma , B Li , A Zhang , J R Cole , J M Tiedje , T Zhang . (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 https://doi.org/10.1093/bioinformatics/btw136
41	Y Yang , Z Li , W Song , L Du , C Ye , B Zhao , W Liu , D Deng , Y Pan , H Lin . 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 https://doi.org/10.1016/j.envint.2019.03.062
42	X Yin , X T Jiang , B Chai , L Li , Y Yang , J R Cole , J M Tiedje , T Zhang . (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 https://doi.org/10.1093/bioinformatics/bty053
43	K Yoo , H Yoo , J Lee , E J Choi , J Park . (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 https://doi.org/10.1007/s12275-020-9309-y
44	S M Zainab , M Junaid , N Xu , R N Malik . (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 https://doi.org/10.1016/j.watres.2020.116455
45	M Zhang , Y S Liu , J L Zhao , W R Liu , L Y He , J N Zhang , J Chen , L K He , Q Q Zhang , G G Ying . (2018a). Occurrence, fate and mass loadings of antibiotics in two swine wastewater treatment systems. Science of the Total Environment, 639: 1421–1431 https://doi.org/10.1016/j.scitotenv.2018.05.230
46	Y Zhang , A Z Gu , T Cen , X Li , M He , D Li , J Chen . (2018b). Sub-inhibitory concentrations of heavy metals facilitate the horizontal transfer of plasmid-mediated antibiotic resistance genes in water environment. Environmental Pollution, 237: 74–82 https://doi.org/10.1016/j.envpol.2018.01.032
47	R Zhao , K Yu , J Zhang , G Zhang , J Huang , L Ma , C Deng , X Li , B Li . (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 https://doi.org/10.1016/j.watres.2020.116318
48	S N Zhao , L L Wu , J Feng , S Y Song , H J Zhang . (2016). An ideal detector composed of a 3D Gd-based coordination polymer for DNA and Hg2+ ion. Inorganic Chemistry Frontiers, 3(3): 376–380 https://doi.org/10.1039/C5QI00252D
49	H Zhou , Z Cao , M Zhang , Z Ying , L Ma . (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 https://doi.org/10.1016/j.scitotenv.2020.142077

[1]

FSE-23058-OF-YXR_suppl_1

Download

[1]	Zhiguo Su, Lyujun Chen, Donghui Wen. Impact of wastewater treatment plant effluent discharge on the antibiotic resistome in downstream aquatic environments: a mini review[J]. Front. Environ. Sci. Eng., 2024, 18(3): 36-.
[2]	Guannan Mao, Donglin Wang, Yaohui Bai, Jiuhui Qu. Mitigating microbiological risks of potential pathogens carrying antibiotic resistance genes and virulence factors in receiving rivers: Benefits of wastewater treatment plant upgrade[J]. Front. Environ. Sci. Eng., 2023, 17(7): 82-.
[3]	Tao Ya, Zhimin Wang, Junyu Liu, Minglu Zhang, Lili Zhang, Xiaojing Liu, Yuan Li, Xiaohui Wang. Responses of microbial interactions to elevated salinity in activated sludge microbial community[J]. Front. Environ. Sci. Eng., 2023, 17(5): 60-.
[4]	Chengsong Ye, Yuming Chen, Lin Feng, Kun Wan, Jianguo Li, Mingbao Feng, Xin Yu. Effect of the ultraviolet/chlorine process on microbial community structure, typical pathogens, and antibiotic resistance genes in reclaimed water[J]. Front. Environ. Sci. Eng., 2022, 16(8): 100-.
[5]	Yuwei Guo, Xian Xiao, Yuan Zhao, Jianguo Liu, Jizhong Zhou, Bo Sun, Yuting Liang. Antibiotic resistance genes in manure-amended paddy soils across eastern China: Occurrence and influencing factors[J]. Front. Environ. Sci. Eng., 2022, 16(7): 91-.
[6]	Ziyan Qin, Qun Gao, Qiang Dong, Joy D. Van Nostrand, Qi Qi, Yifan Su, Suo Liu, Tianjiao Dai, Jingmin Cheng, Jizhong Zhou, Yunfeng Yang. Antibiotic resistome mostly relates to bacterial taxonomy along a suburban transmission chain[J]. Front. Environ. Sci. Eng., 2022, 16(3): 32-.
[7]	Jiaheng Zhao, Bing Li, Pin Lv, Jiahui Hou, Yong Qiu, Xia Huang. Distribution of antibiotic resistance genes and their association with bacteria and viruses in decentralized sewage treatment facilities[J]. Front. Environ. Sci. Eng., 2022, 16(3): 35-.
[8]	Mingyi Yang, Lin Shi, Di Zhang, Zhaohui He, Aiping Liang, Xiao Sun. Adsorption of herring sperm DNA onto pine sawdust biochar: Thermodynamics and site energy distribution[J]. Front. Environ. Sci. Eng., 2022, 16(11): 144-.
[9]	Jian Lu, Jun Wu, Jianhua Wang. Metagenomic analysis on resistance genes in water and microplastics from a mariculture system[J]. Front. Environ. Sci. Eng., 2022, 16(1): 4-.
[10]	Caihong Huang, Zhurui Tang, Beidou Xi, Wenbing Tan, Wei Guo, Weixia Wu, Caiyun Ma. Environmental effects and risk control of antibiotic resistance genes in the organic solid waste aerobic composting system: A review[J]. Front. Environ. Sci. Eng., 2021, 15(6): 127-.
[11]	Yuan Meng, Weiyi Liu, Heidelore Fiedler, Jinlan Zhang, Xinrui Wei, Xiaohui Liu, Meng Peng, Tingting Zhang. Fate and risk assessment of emerging contaminants in reclaimed water production processes[J]. Front. Environ. Sci. Eng., 2021, 15(5): 104-.
[12]	Qingkun Ji, Caihong Zhang, Dan Li. *Influences and mechanisms of nanofullerene on the horizontal transfer of plasmid-encoded antibiotic resistance genes between E. coli* strains**[J]. Front. Environ. Sci. Eng., 2020, 14(6): 108-.
[13]	Nan Wu, Weiyu Zhang, Shiyu Xie, Ming Zeng, Haixue Liu, Jinghui Yang, Xinyuan Liu, Fan Yang. Increasing prevalence of antibiotic resistance genes in manured agricultural soils in northern China[J]. Front. Environ. Sci. Eng., 2020, 14(1): 1-.
[14]	Lian Yang, Qinxue Wen, Zhiqiang Chen, Ran Duan, Pan Yang. Impacts of advanced treatment processes on elimination of antibiotic resistance genes in a municipal wastewater treatment plant[J]. Front. Environ. Sci. Eng., 2019, 13(3): 32-.
[15]	Qiaowen Tan, Weiying Li, Junpeng Zhang, Wei Zhou, Jiping Chen, Yue Li, Jie Ma. Presence, dissemination and removal of antibiotic resistant bacteria and antibiotic resistance genes in urban drinking water system: A review[J]. Front. Environ. Sci. Eng., 2019, 13(3): 36-.

Viewed

Full text

Abstract

Cited

Shared

Discussed