Metagenomic analysis on resistance genes in water and microplastics from a mariculture system

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.

Graphical abstract

Keywords

Antibiotic resistance genes / Metal resistance genes / Metagenomic analysis / Microplastics / Mariculture

References

[1] Al-Salem S M, Uddin S, Al-Yamani F (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

[2] Buta M, Hubeny J, Zieliński W, Harnisz M, Korzeniewska E (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

[3] Elizalde-Velázquez G A, Gómez-Oliván L M (2021). Microplastics in aquatic environments: A review on occurrence, distribution, toxic effects, and implications for human health. Science of the Total Environment, 780: 146551

[4] Flach C F, Pal C, Svensson C J, Kristiansson E, Östman M, Bengtsson-Palme J, Tysklind M, Larsson D G J (2017). Does antifouling paint select for antibiotic resistance? Science of the Total Environment, 590-591: 461–468

[5] Fraiture M A, Deckers M, Papazova N, Roosens N H C (2020). Detection strategy targeting a chloramphenicol resistance gene from genetically modified bacteria in food and feed products. Food Control, 108: 106873

[6] Hanekamp J C, Bast A (2015). Antibiotics exposure and health risks: Chloramphenicol. Environmental Toxicology and Pharmacology, 39(1): 213–220

[7] He X, Xu Y, Chen J, Ling J, Li Y, Huang L, Zhou X, Zheng L, Xie G (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

[8] Huang L, Xu Y B, Xu J X, Ling J Y, Chen J L, Zhou J L, Zheng L, Du Q P (2017). Antibiotic resistance genes (ARGs) in duck and fish production ponds with integrated or non-integrated mode. Chemosphere, 168: 1107–1114

[9] Koutnik V S, Leonard J, Alkidim S, DePrima F J, Ravi S, Hoek E M V, Mohanty S K (2021). Distribution of microplastics in soil and freshwater environments: Global analysis and framework for transport modeling. Environmental Pollution, 274: 116552

[10] Li L G, Huang Q, Yin X, Zhang T (2020). Source tracking of antibiotic resistance genes in the environment: Challenges, progress, and prospects. Water Research, 185: 116127

[11] Liu X, Wang J (2020). Algae (Raphidocelis subcapitata) mitigate combined toxicity of microplastic and lead on Ceriodaphnia dubia. Frontiers of Environmental Science & Engineering, 14(6): 97

[12] Lu J, Lin Y, Wu J, Zhang C (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

[13] Lu J, Wu J, Wu J, Zhang C, Luo Y (2021a). Adsorption and desorption of steroid hormones by microplastics in seawater. Bulletin of Environmental Contamination and Toxicology, (In press)

[14] Lu J, Wu J, Zhang C, Zhang Y, Lin Y, Luo Y (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

[15] Lu J, Zhang C, Wu J (2021c). Removal of steroid hormones from mariculture system using seaweed Caulerpa lentillifera. Frontiers of Environmental Science & Engineering, 16(2): 15

[16] Lu J, Zhang Y, Wu J (2020b). Continental-scale spatio-temporal distribution of antibiotic resistance genes in coastal waters along coastline of China. Chemosphere, 247: 125908

[17] Lu J, Zhang Y, Wu J, Luo Y (2019a). Effects of microplastics on distribution of antibiotic resistance genes in recirculating aquaculture system. Ecotoxicology and Environmental Safety, 184: 109631

[18] Lu J, Zhang Y, Wu J, Wang J, Cai Y (2020a). Fate of antibiotic resistance genes in reclaimed water reuse system with integrated membrane process. Journal of Hazardous Materials, 382: 121025

[19] Lu J, Zhang Y, Wu J, Wang J, Zhang C, Lin Y (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

[20] Martínez-Campos S, González-Pleiter M, Fernández-Piñas F, Rosal R, Leganés F (2021). Early and differential bacterial colonization on microplastics deployed into the effluents of wastewater treatment plants. Science of the Total Environment, 757: 143832

[21] Mustafa M, Wang H, Lindberg R H, Fick J, Wang Y, Tysklind M (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

[22] Nowrotek M, Jałowiecki Ł, Harnisz M, Płaza G A (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] Pazda M, Kumirska J, Stepnowski P, Mulkiewicz E (2019). Antibiotic resistance genes identified in wastewater treatment plant systems- A review. Science of the Total Environment, 697: 134023

[24] Pham D N, Clark L, Li M (2021). Microplastics as hubs enriching antibiotic-resistant bacteria and pathogens in municipal activated sludge. Journal of Hazardous Materials Letters, 2: 100014

[25] Prata J C, da Costa J P, Lopes I, Andrady A L, Duarte A C, Rocha-Santos T (2021). A One Health perspective of the impacts of microplastics on animal, human and environmental health. Science of the Total Environment, 777: 146094

[26] Santana-Viera S, Montesdeoca-Esponda S, Guedes-Alonso R, Sosa-Ferrera Z, Santana-Rodríguez J J (2021). Organic pollutants adsorbed on microplastics: Analytical methodologies and occurrence in oceans. Trends in Environmental Analytical Chemistry, 29: e00114

[27] Sherpa M T, Najar I N, Das S, Thakur N (2020). Distribution of antibiotic and metal resistance genes in two glaciers of North Sikkim, India. Ecotoxicology and Environmental Safety, 203: 111037

[28] Subirats J, Timoner X, Sànchez-Melsió A, Balcázar J L, Acuña V, Sabater S, Borrego C M (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

[29] Wang J H, Lu J, Wu J, Zhang Y, Zhang C (2019). Proliferation of antibiotic resistance genes in coastal recirculating mariculture system. Environmental Pollution, 248: 462–470

[30] Wang J H, Lu J, Zhang Y X, Wu J, Luo Y, Liu H (2018). Metagenomic analysis of antibiotic resistance genes in coastal industrial mariculture systems. Bioresource Technology, 253: 235–243

[31] 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

[32] Wendlandt S, Shen J, Kadlec K, Wang Y, Li B, Zhang W J, Feßler A T, Wu C, Schwarz S (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

[33] Wright S L, Ulke J, Font A, Chan K L A, Kelly F J (2020). Atmospheric microplastic deposition in an urban environment and an evaluation of transport. Environment International, 136: 105411

[34] Wu N, Zhang W, Xie S, Zeng M, Liu H, Yang J, Liu X, Yang F (2020). Increasing prevalence of antibiotic resistance genes in manured agricultural soils in northern China. Frontiers of Environmental Science & Engineering, 14(1): 1

[35] Xu E G, Ren Z J (2021). Preventing masks from becoming the next plastic problem. Frontiers of Environmental Science & Engineering, 15(6): 125

[36] Yang Y, Liu G, Song W, Ye C, Lin H, Li Z, Liu W (2019). Plastics in the marine environment are reservoirs for antibiotic and metal resistance genes. Environment International, 123: 79–86

[37] Yin X, Deng Y, Ma L, Wang Y, Chan L Y L, Zhang T (2019). Exploration of the antibiotic resistome in a wastewater treatment plant by a nine-year longitudinal metagenomic study. Environment International, 133(Pt B): 105270

[38] 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

[39] Zhou M, Xu Y, Ouyang P, Ling J, Cai Q, Du Q, Zheng L (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

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