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Frontiers of Environmental Science & Engineering

ISSN 2095-2201

ISSN 2095-221X(Online)

CN 10-1013/X

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2018 Impact Factor: 3.883

Front. Environ. Sci. Eng.    2022, Vol. 16 Issue (1) : 4    https://doi.org/10.1007/s11783-021-1438-y
RESEARCH ARTICLE
Metagenomic analysis on resistance genes in water and microplastics from a mariculture system
Jian Lu1,3, Jun Wu2(), Jianhua Wang1
1. CAS Key Laboratory of Coastal Environmental Processes and Ecological Remediation, Yantai Institute of Coastal Zone Research (YIC), Chinese Academy of Sciences (CAS); Shandong Key Laboratory of Coastal Environmental Processes, YICCAS, Yantai 264003, China
2. Yantai Research Institute, Harbin Engineering University, Yantai 264006, China
3. Center for Ocean Mega-Science, Chinese Academy of Sciences, Qingdao 266071, China
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Abstract

• Total 174 subtypes of ARGs were detected by metagenomic analysis.

• Chloramphenicol resistance genes were the dominant ARGs in water and microplastics.

• The abundances of MRGs were much higher than those of ARGs.

• Proteobacteria, Bacteroidetes, and Actinobacteria were the dominant phylum.

• Microplastics in mariculture system could enrich most of MRGs and some ARGs.

Microplastics existing widely in different matrices have been regarded as a reservoir for emerging contaminants. Mariculture systems have been observed to host microplastics and antibiotic resistance genes (ARGs). However, more information on proliferation of ARGs and metal resistance genes (MRGs) in mariculture system at the presence of microplastics is needed. This study used metagenomic analysis to investigate the distribution of ARGs and MRGs in water and microplastics of a typical mariculture pond. Total 18 types including 174 subtypes of ARGs were detected with the total relative abundances of 1.22/1.25 copies per 16S rRNA copy for microplastics/water. Chloramphenicol resistance genes were the dominant ARGs with the abundance of 0.35/0.42 copies per 16S rRNA copy for microplastics/water. Intergron intI1 was dominant gene among 6 detected mobile genetic elements (MGEs) with the abundance of 75.46/68.70 copies per 16S rRNA copy for water/microplastics. Total 9 types including 46 subtypes of MRGs were detected with total abundance of 5.02 × 102/6.39 × 102 copies per 16S rRNA copy for water/ microplastics while genes resistant to copper and iron served as the dominant MRGs. Proteobacteria, Bacteroidetes, and Actinobacteria accounted for 84.2%/89.5% of total microbial community. ARGs with relatively high abundance were significantly positively related to major genera, MGEs, and MRGs. Microplastics in mariculture system could enrich most of MRGs and some ARGs to serve as potential reservoir for these pollutants. The findings of this study will provide important information on resistance gene pollution at presence of microplastics in the mariculture system for further proposing suitable strategy of environmental management.

Keywords Antibiotic resistance genes      Metal resistance genes      Metagenomic analysis      Microplastics      Mariculture     
Corresponding Author(s): Jun Wu   
Issue Date: 14 September 2021
 Cite this article:   
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.
 URL:  
https://academic.hep.com.cn/fese/EN/10.1007/s11783-021-1438-y
https://academic.hep.com.cn/fese/EN/Y2022/V16/I1/4
Fig.1  The relative abundances of different types (a) and subtypes (b) of detected ARGs in water and microplastic samples (Detailed subtypes corresponding to individual digit of x-axis in Fig. 1?(b) referred to Table S1).
Fig.2  The relative abundances of detected MGEs (a), MRG types (b), and MRG subtypes (c) in water and microplastic samples.
Fig.3  Bar plot on phylum level (a), Circos diagram on genus level (b), and Fisher’s exact test bar plot on phylum level (c) of water and microplastic samples.
Fig.4  Circos diagram (a) and Fisher’s exact test bar plot (b) of KEGG level 2 pathway in water and microplastic samples.
Fig.5  Contribution of major bacterial genera to proliferation of representative ARGs.
Fig.6  Co-occurrence network between typical ARGs and bacterial genera (a), ARGs-MGEs (b), and ARGs-MRGs (c). Red lines represent the positive correlation.
1 S M Al-Salem, S Uddin, F Al-Yamani (2020). An assessment of microplastics threat to the marine environment: A short review in context of the Arabian/Persian Gulf. Marine Environmental Research, 159: 104961
https://doi.org/10.1016/j.marenvres.2020.104961 pmid: 32250880
2 M Buta, J Hubeny, W Zieliński, M Harnisz, E Korzeniewska (2021). Sewage sludge in agriculture —the effects of selected chemical pollutants and emerging genetic resistance determinants on the quality of soil and crops: A review. Ecotoxicology and Environmental Safety, 214: 112070
https://doi.org/10.1016/j.ecoenv.2021.112070 pmid: 33652361
3 G A Elizalde-Velázquez, L M Gómez-Oliván (2021). Microplastics in aquatic environments: A review on occurrence, distribution, toxic effects, and implications for human health. Science of the Total Environment, 780: 146551
https://doi.org/10.1016/j.scitotenv.2021.146551 pmid: 33773347
4 C F Flach, C Pal, C J Svensson, E Kristiansson, M Östman, J Bengtsson-Palme, M Tysklind, D G J Larsson (2017). Does antifouling paint select for antibiotic resistance? Science of the Total Environment, 590-591: 461–468
https://doi.org/10.1016/j.scitotenv.2017.01.213 pmid: 28284638
5 M A Fraiture, M Deckers, N Papazova, N H C Roosens (2020). Detection strategy targeting a chloramphenicol resistance gene from genetically modified bacteria in food and feed products. Food Control, 108: 106873
https://doi.org/10.1016/j.foodcont.2019.106873
6 J C Hanekamp, A Bast (2015). Antibiotics exposure and health risks: Chloramphenicol. Environmental Toxicology and Pharmacology, 39(1): 213–220
https://doi.org/10.1016/j.etap.2014.11.016 pmid: 25528412
7 X He, Y Xu, J Chen, J Ling, Y Li, L Huang, X Zhou, L Zheng, G Xie (2017). Evolution of corresponding resistance genes in the water of fish tanks with multiple stresses of antibiotics and heavy metals. Water Research, 124: 39–48
https://doi.org/10.1016/j.watres.2017.07.048 pmid: 28738272
8 L Huang, Y B Xu, J X Xu, J Y Ling, J L Chen, J L Zhou, L Zheng, Q P Du (2017). Antibiotic resistance genes (ARGs) in duck and fish production ponds with integrated or non-integrated mode. Chemosphere, 168: 1107–1114
https://doi.org/10.1016/j.chemosphere.2016.10.096 pmid: 27816285
9 V S Koutnik, J Leonard, S Alkidim, F J DePrima, S Ravi, E M V Hoek, S K Mohanty (2021). Distribution of microplastics in soil and freshwater environments: Global analysis and framework for transport modeling. Environmental Pollution, 274: 116552
https://doi.org/10.1016/j.envpol.2021.116552 pmid: 33545526
10 L G Li, Q Huang, X Yin, T Zhang (2020). Source tracking of antibiotic resistance genes in the environment: Challenges, progress, and prospects. Water Research, 185: 116127
https://doi.org/10.1016/j.watres.2020.116127 pmid: 33086465
11 X Liu, J Wang (2020). Algae (Raphidocelis subcapitata) mitigate combined toxicity of microplastic and lead on Ceriodaphnia dubia. Frontiers of Environmental Science & Engineering, 14(6): 97
https://doi.org/10.1007/s11783-020-1276-3
12 J Lu, Y Lin, J Wu, C Zhang (2021b). Continental-scale spatial distribution, sources, and health risks of heavy metals in seafood: challenge for the water-food-energy nexus sustainability in coastal regions? Environmental Science and Pollution Research International, (In press) doi:10.1007/s11356-020-11904-11358
pmid: 33400129
13 J Lu, J Wu, J Wu, C Zhang, Y Luo (2021a). Adsorption and desorption of steroid hormones by microplastics in seawater. Bulletin of Environmental Contamination and Toxicology, (In press)
https://doi.org/10.1007/s00128-020-02784-2 pmid: 31912186
14 J Lu, J Wu, C Zhang, Y Zhang, Y Lin, Y Luo (2018). Occurrence, distribution, and ecological-health risks of selected antibiotics in coastal waters along the coastline of China. Science of the Total Environment, 644: 1469–1476
https://doi.org/10.1016/j.scitotenv.2018.07.096 pmid: 30743859
15 J Lu, C Zhang, J Wu (2021c). Removal of steroid hormones from mariculture system using seaweed Caulerpa lentillifera. Frontiers of Environmental Science & Engineering, 16(2): 15
https://doi.org/10.1007/s11783-021-1449-8
16 J Lu, Y Zhang, J Wu (2020b). Continental-scale spatio-temporal distribution of antibiotic resistance genes in coastal waters along coastline of China. Chemosphere, 247: 125908
https://doi.org/10.1016/j.chemosphere.2020.125908 pmid: 31972491
17 J Lu, Y Zhang, J Wu, Y Luo (2019a). Effects of microplastics on distribution of antibiotic resistance genes in recirculating aquaculture system. Ecotoxicology and Environmental Safety, 184: 109631
https://doi.org/10.1016/j.ecoenv.2019.109631 pmid: 31514079
18 J Lu, Y Zhang, J Wu, J Wang, Y Cai (2020a). Fate of antibiotic resistance genes in reclaimed water reuse system with integrated membrane process. Journal of Hazardous Materials, 382: 121025
https://doi.org/10.1016/j.jhazmat.2019.121025 pmid: 31446351
19 J Lu, Y Zhang, J Wu, J Wang, C Zhang, Y Lin (2019b). Occurrence and spatial distribution of antibiotic resistance genes in the Bohai Sea and Yellow Sea areas, China. Environmental Pollution, 252(Pt A): 450–460
https://doi.org/10.1016/j.envpol.2019.05.143 pmid: 31158673
20 S Martínez-Campos, M González-Pleiter, F Fernández-Piñas, R Rosal, F Leganés (2021). Early and differential bacterial colonization on microplastics deployed into the effluents of wastewater treatment plants. Science of the Total Environment, 757: 143832
https://doi.org/10.1016/j.scitotenv.2020.143832 pmid: 33246729
21 M Mustafa, H Wang, R H Lindberg, J Fick, Y Wang, M Tysklind (2021). Identification of resistant pharmaceuticals in ozonation using QSAR modeling and their fate in electro-peroxone process. Frontiers of Environmental Science & Engineering, 15(5): 106
https://doi.org/10.1007/s11783-021-1394-6
22 M Nowrotek, Ł Jałowiecki, M Harnisz, G A Płaza (2019). Culturomics and metagenomics: In understanding of environmental resistome. Frontiers of Environmental Science & Engineering, 13(3): 40 doi:10.1007/s11783-019-1121-8
23 M Pazda, J Kumirska, P Stepnowski, E Mulkiewicz (2019). Antibiotic resistance genes identified in wastewater treatment plant systems- A review. Science of the Total Environment, 697: 134023
https://doi.org/10.1016/j.scitotenv.2019.134023 pmid: 31479900
24 D N Pham, L Clark, M Li (2021). Microplastics as hubs enriching antibiotic-resistant bacteria and pathogens in municipal activated sludge. Journal of Hazardous Materials Letters, 2: 100014
https://doi.org/10.1016/j.hazl.2021.100014
25 J C Prata, J P da Costa, I Lopes, A L Andrady, A C Duarte, T Rocha-Santos (2021). A One Health perspective of the impacts of microplastics on animal, human and environmental health. Science of the Total Environment, 777: 146094
https://doi.org/10.1016/j.scitotenv.2021.146094 pmid: 33677304
26 S Santana-Viera, S Montesdeoca-Esponda, R Guedes-Alonso, Z Sosa-Ferrera, J J Santana-Rodríguez (2021). Organic pollutants adsorbed on microplastics: Analytical methodologies and occurrence in oceans. Trends in Environmental Analytical Chemistry, 29: e00114
https://doi.org/10.1016/j.teac.2021.e00114
27 M T Sherpa, I N Najar, S Das, N Thakur (2020). Distribution of antibiotic and metal resistance genes in two glaciers of North Sikkim, India. Ecotoxicology and Environmental Safety, 203: 111037
https://doi.org/10.1016/j.ecoenv.2020.111037 pmid: 32888596
28 J Subirats, X Timoner, A Sànchez-Melsió, J L Balcázar, V Acuña, S Sabater, C M Borrego (2018). Emerging contaminants and nutrients synergistically affect the spread of class 1 integron-integrase (intI1) and sul1 genes within stable streambed bacterial communities. Water Research, 138: 77–85
https://doi.org/10.1016/j.watres.2018.03.025 pmid: 29573631
29 J H Wang, J Lu, J Wu, Y Zhang, C Zhang (2019). Proliferation of antibiotic resistance genes in coastal recirculating mariculture system. Environmental Pollution, 248: 462–470
30 J H Wang, J Lu, Y X Zhang, J Wu, Y Luo, H Liu (2018). Metagenomic analysis of antibiotic resistance genes in coastal industrial mariculture systems. Bioresource Technology, 253: 235–243
https://doi.org/10.1016/j.biortech.2018.01.035 pmid: 29353751
31 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
32 S Wendlandt, J Shen, K Kadlec, Y Wang, B Li, W J Zhang, A T Feßler, C Wu, S Schwarz (2015). Multidrug resistance genes in staphylococci from animals that confer resistance to critically and highly important antimicrobial agents in human medicine. Trends in Microbiology, 23(1): 44–54
https://doi.org/10.1016/j.tim.2014.10.002 pmid: 25455417
33 S L Wright, J Ulke, A Font, K L A Chan, F J Kelly (2020). Atmospheric microplastic deposition in an urban environment and an evaluation of transport. Environment International, 136: 105411
https://doi.org/10.1016/j.envint.2019.105411 pmid: 31889555
34 N Wu, W Zhang, S Xie, M Zeng, H Liu, J Yang, X Liu, F Yang (2020). Increasing prevalence of antibiotic resistance genes in manured agricultural soils in northern China. Frontiers of Environmental Science & Engineering, 14(1): 1
https://doi.org/10.1007/s11783-019-1180-x
35 E G Xu, Z J Ren (2021). Preventing masks from becoming the next plastic problem. Frontiers of Environmental Science & Engineering, 15(6): 125
https://doi.org/10.1007/s11783-021-1413-7 pmid: 33686360
36 Y Yang, G Liu, W Song, C Ye, H Lin, Z Li, W Liu (2019). Plastics in the marine environment are reservoirs for antibiotic and metal resistance genes. Environment International, 123: 79–86
https://doi.org/10.1016/j.envint.2018.11.061 pmid: 30502597
37 X Yin, Y Deng, L Ma, Y Wang, L Y L Chan, T Zhang (2019). Exploration of the antibiotic resistome in a wastewater treatment plant by a nine-year longitudinal metagenomic study. Environment International, 133(Pt B): 105270
https://doi.org/10.1016/j.envint.2019.105270 pmid: 31683155
38 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 pmid: 29408954
39 M Zhou, Y Xu, P Ouyang, J Ling, Q Cai, Q Du, L Zheng (2020). Spread of resistance genes from duck manure to fish intestine in simulated fish-duck pond and the promotion of cefotaxime and As. Science of the Total Environment, 731: 138693
https://doi.org/10.1016/j.scitotenv.2020.138693 pmid: 32408202
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