Occurrence and possible sources of antibiotic resistance genes in seawater of the South China Sea
Jian Lu, Jun Wu, Cui Zhang, Jianhua Wang, Xia He
Occurrence and possible sources of antibiotic resistance genes in seawater of the South China Sea
● The highest absolute abundance of ARGs in seawater reached 2.3 × 104 copies/mL. ● Multidrug resistance genes were major ARGs in seawater of many sites. ● Insertion sequences were the dominant MGEs in seawater. ● Prochlorococcus _MIT9313 and Clade_la were the predominant genus in seawater. ● Anthropogenic activities had important effect on ARGs and MGEs.
Antibiotic resistance genes (ARGs) might have great effect on ecological security and human health. Oceans are important reservoirs that receive tremendous amounts of pollutants globally. However, information on the proliferation of ARGs in seawater is still limited. This study performed field sampling to investigate the occurrence and distribution of ARGs in seawater of the South China Sea, which is the deepest and largest sea in China. The results showed that the total absolute abundances of ARGs in seawater samples ranged from 2.1 × 103 to 2.3 × 104 copies/mL, with an of 5.0 × 103 copies/mL and a range of 2.2 × 103–1.8 × 104 copies/mL for those with mobile genetic elements (MGEs). Genes resistant to multidrug, aminoglycoside, tetracycline, and fluoroquinolone antibiotics accounted for 77.3%–88.6% of total ARGs in seawater. Proteobacteria and Cyanobacteria represented 32.1%–56.2% and 30.4%–49.5% of microbial community, respectively. Prochlorococcus_MIT9313 and Clade_la were the prevalent genera in seawater of the South China Sea. Complex co-occurrence relationship existed among ARGs, MGEs, and bacteria. Anthropogenic activities had critical influence on ARGs and MGEs. Hospital wastewater, wastewater treatment plant effluent, sewage, aquaculture tailwater, and runoff were determined as the important sources of ARGs in seawater of the South China Sea based on positive matrix factorization analysis.
The South China Sea / Antibiotic resistance genes / Mobile genetic element / Source apportionment
[1] |
Aguila-Torres P, González M, Maldonado J E, Miranda R, Zhang L, González-Stegmaier R, Rojas L A, Gaete A. (2022). Associations between bacterial communities and microplastics from surface seawater of the Northern Patagonian area of Chile. Environmental Pollution, 306: 119313
CrossRef
Google scholar
|
[2] |
Al-Hosani S, Oudah M M, Henschel A, Yousef L F. (2015). Global transcriptome analysis of salt acclimated Prochlorococcus AS9601. Microbiological Research, 176: 21–28
CrossRef
Google scholar
|
[3] |
Brown-Jaque M, Calero-Cáceres W, Espinal P, Rodríguez-Navarro J, Miró E, González-López J J, Cornejo T, Hurtado J C, Navarro F, Muniesa M. (2018). Antibiotic resistance genes in phage particles isolated from human faeces and induced from clinical bacterial isolates. International Journal of Antimicrobial Agents, 51(3): 434–442
CrossRef
Google scholar
|
[4] |
Celik-Saglam I, Yurtsever M, Civan M, Yurdakul S, Cetin B. (2023). Evaluation of levels and sources of microplastics and phthalic acid esters and their relationships in the atmosphere of highly industrialized and urbanized Gebze, Türkiye. Science of the Total Environment, 881: 163508
CrossRef
Google scholar
|
[5] |
Cerqueira F, Matamoros V, Bayona J M, Berendonk T U, Elsinga G, Hornstra L M, Piña B. (2019). Antibiotic resistance gene distribution in agricultural fields and crops:. a soil-to-food analysis. Environmental Research, 177: 108608
CrossRef
Google scholar
|
[6] |
Chen H, Wang S, Guo H, Huo Y, Lin H, Zhang Y. (2022). The abundance, characteristics and diversity of microplastics in the South China Sea: observation around three remote islands. Frontiers of Environmental Science & Engineering, 16(1): 9
CrossRef
Google scholar
|
[7] |
Cheng Y, Shan Y, Xue Y, Zhu Y, Wang X, Xue L, Liu Y, Qiao F, Zhang M. (2022). Variation characteristics of atmospheric methane and carbon dioxide in summertime at a coastal site in the South China Sea. Frontiers of Environmental Science & Engineering, 16(11): 139
CrossRef
Google scholar
|
[8] |
Dai Y, Zhao J, Sun C, Li D, Liu X, Wang Z, Yue T, Xing B. (2022). Interaction and combined toxicity of microplastics and per- and polyfluoroalkyl substances in aquatic environment. Frontiers of Environmental Science & Engineering, 16(10): 136
CrossRef
Google scholar
|
[9] |
Dong S, Gao P, Li B, Feng L, Liu Y, Du Z, Zhang L. (2022). Occurrence and migration of microplastics and plasticizers in different wastewater and sludge treatment units in municipal wastewater treatment plant. Frontiers of Environmental Science & Engineering, 16(11): 142
CrossRef
Google scholar
|
[10] |
Guo Y, Xiao X, Zhao Y, Liu J, Zhou J, Sun B, Liang Y. (2022). Antibiotic resistance genes in manure-amended paddy soils across eastern China: occurrence and influencing factors. Frontiers of Environmental Science & Engineering, 16(7): 91
CrossRef
Google scholar
|
[11] |
Ginn O, Nichols D, Rocha-Melogno L, Bivins A, Berendes D, Soria F, Andrade M, Deshusses M A, Bergin M, Brown J. (2021). Antimicrobial resistance genes are enriched in aerosols near impacted urban surface waters in La Paz, Bolivia. Environmental Research, 194: 110730
CrossRef
Google scholar
|
[12] |
Hitch T C A, Thomas B J, Friedersdorff J C A, Ougham H, Creevey C J. (2018). Deep sequence analysis reveals the ovine rumen as a reservoir of antibiotic resistance genes. Environmental Pollution, 235: 571–575
CrossRef
Google scholar
|
[13] |
Hooban B, Joyce A, Fitzhenry K, Chique C, Morris D. (2020). The role of the natural aquatic environment in the dissemination of extended spectrum beta-lactamase and carbapenemase encoding genes: a scoping review. Water Research, 180: 115880
CrossRef
Google scholar
|
[14] |
Hu Y, Du W, Yang C, Wang Y, Huang T, Xu X, Li W. (2023). Source identification and prediction of nitrogen and phosphorus pollution of Lake Taihu by an ensemble machine learning technique. Frontiers of Environmental Science & Engineering, 17(5): 55
CrossRef
Google scholar
|
[15] |
Jampani M, Mateo-Sagasta J, Chandrasekar A, Fatta-Kassinos D, Graham D W, Gothwal R, Moodley A, Chadag V M, Wiberg D, Langan S. (2024). Fate and transport modelling for evaluating antibiotic resistance in aquatic environments: current knowledge and research priorities. Journal of Hazardous Materials, 461: 132527
CrossRef
Google scholar
|
[16] |
Jang J, Kim M, Baek S, Shin J, Shin J, Shin S G, Kim Y M, Cho K H. (2021). Hydrometeorological Influence on antibiotic-resistance genes (ARGs) and bacterial community at a recreational beach in Korea. Journal of Hazardous Materials, 403: 123599
CrossRef
Google scholar
|
[17] |
Jiang W, Yu K, Wang N, Yang H, Yang H, Xu S, Wei C, Wang S, Wang Y. (2020). Distribution coefficients of trace metals between modern coral-lattices and seawater in the northern South China Sea: species and SST dependencies. Journal of Asian Earth Sciences, 187: 104082
CrossRef
Google scholar
|
[18] |
Jo H, Raza S, Farooq A, Kim J, Unno T. (2021). Fish farm effluents as a source of antibiotic resistance gene dissemination on Jeju Island, South Korea. Environmental Pollution, 276: 116764
CrossRef
Google scholar
|
[19] |
Koongolla J B, Lin L, Pan Y F, Yang C P, Sun D R, Liu S, Xu X R, Maharana D, Huang J S, Li H X. (2020). Occurrence of microplastics in gastrointestinal tracts and gills of fish from Beibu Gulf, South China Sea. Environmental Pollution, 258: 113734
CrossRef
Google scholar
|
[20] |
Li F, Bao Y, Chen L, Su Z, Tang Y, Wen D. (2023). Screening of priority antibiotics in Chinese seawater based on the persistence, bioaccumulation, toxicity and resistance. Environment International, 179: 108140
CrossRef
Google scholar
|
[21] |
Li H, Xu H, Yang Y L, Yang X L, Wu Y, Zhang S, Song H L. (2019). Effects of graphite and Mn ore media on electro-active bacteria enrichment and fate of antibiotic and corresponding resistance gene in up flow microbial fuel cell constructed wetland. Water Research, 165: 114988
CrossRef
Google scholar
|
[22] |
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
CrossRef
Google scholar
|
[23] |
Lu J, Wu J, Wang J. (2022a). Metagenomic analysis on resistance genes in water and microplastics from a mariculture system. Frontiers of Environmental Science & Engineering, 16(1): 4
CrossRef
Google scholar
|
[24] |
Lu J, Zhang C, Wu J. (2022d). Removal of steroid hormones from mariculture system using seaweed Caulerpa lentillifera. Frontiers of Environmental Science & Engineering, 16(2): 15
CrossRef
Google scholar
|
[25] |
Lu J, Zhang Y, Wu J. (2020). Continental-scale spatio-temporal distribution of antibiotic resistance genes in coastal waters along coastline of China. Chemosphere, 247: 125908
CrossRef
Google scholar
|
[26] |
Lu J, Zhang Y, Wu J, Wang J. (2022c). Intervention of antimicrobial peptide usage on antimicrobial resistance in aquaculture. Journal of Hazardous Materials, 427: 128154
CrossRef
Google scholar
|
[27] |
Lu J, Zhang Y, Wu J, Wang J, Zhang C, Lin Y. (2019). Occurrence and spatial distribution of antibiotic resistance genes in the Bohai Sea and Yellow Sea areas, China. Environmental Pollution, 252: 450–460
CrossRef
Google scholar
|
[28] |
Lu J, Zhang Y, Wu J, Wang J, Zhang C, Wu J. (2022b). Fate of land-based antibiotic resistance genes in marginal-sea sediment: territorial differentiation and corresponding drivers. Chemosphere, 288: 132540
CrossRef
Google scholar
|
[29] |
Lv B, Cui Y, Tian W, Wei H, Chen Q, Liu B, Zhang D, Xie B. (2020). Vessel transport of antibiotic resistance genes across oceans and its implications for ballast water management. Chemosphere, 253: 126697
CrossRef
Google scholar
|
[30] |
Makowska N, Bresa K, Koczura R, Philips A, Nowis K, Mokracka J. (2021). Urban wastewater as a conduit for pathogenic Gram-positive bacteria and genes encoding resistance to β-lactams and glycopeptides. Science of the Total Environment, 765: 144176
CrossRef
Google scholar
|
[31] |
Manoharan R K, Srinivasan S, Shanmugam G, Ahn Y H. (2021). Shotgun metagenomic analysis reveals the prevalence of antibiotic resistance genes and mobile genetic elements in full scale hospital wastewater treatment plants. Journal of Environmental Management, 296: 113270
CrossRef
Google scholar
|
[32] |
Ohore O E, Addo F G, Han N, Li X, Zhang S. (2020). Profiles of ARGs and their relationships with antibiotics, metals and environmental parameters in vertical sediment layers of three lakes in China. Journal of Environmental Management, 255: 109583
CrossRef
Google scholar
|
[33] |
Pfeifer E, Sousa J M, Touchon M, Rocha E P C. (2023). When bacteria are phage playgrounds: interactions between viruses, cells, and mobile genetic elements. Current Opinion in Microbiology, 70: 102230
CrossRef
Google scholar
|
[34] |
Šamanić I, Kalinić H, Fredotović Ž, Dželalija M, Bungur A M, Maravić A. (2021). Bacteria tolerant to colistin in coastal marine environment: detection, microbiome diversity and antibiotic resistance genes’ repertoire. Chemosphere, 281: 130945
CrossRef
Google scholar
|
[35] |
Samreen I, Ahmad H A, Malak H H. (2021). Environmental antimicrobial resistance and its drivers: a potential threat to public health. Journal of Global Antimicrobial Resistance, 27: 101–111
CrossRef
Google scholar
|
[36] |
Sanz C, Casado M, Navarro-Martin L, Cañameras N, Carazo N, Matamoros V, Bayona J M, Piña B. (2022). Implications of the use of organic fertilizers for antibiotic resistance gene distribution in agricultural soils and fresh food products: a plot-scale study. Science of the Total Environment, 815: 151973
CrossRef
Google scholar
|
[37] |
Sorinolu A J, Tyagi N, Kumar A, Munir M. (2021). Antibiotic resistance development and human health risks during wastewater reuse and biosolids application in agriculture. Chemosphere, 265: 129032
CrossRef
Google scholar
|
[38] |
Sun Q, Li J, Wang C, Chen A, You Y, Yang S, Liu H, Jiang G, Wu Y, Li Y. (2022). Research progress on distribution, sources, identification, toxicity, and biodegradation of microplastics in the ocean, freshwater, and soil environment. Frontiers of Environmental Science & Engineering, 16(1): 1
CrossRef
Google scholar
|
[39] |
Ullah R, Yasir M, Bibi F, Abujamel T S, Hashem A M, Sohrab S S, Al-Ansari A, Al-Sofyani A A, Al-Ghamdi A K, Al-sieni A, Azhar E I. (2019). Taxonomic diversity of antimicrobial-resistant bacteria and genes in the Red Sea coast. Science of the Total Environment, 677: 474–483
CrossRef
Google scholar
|
[40] |
Vanavermaete D, Hostens K, Le H M, Lessuise A, Ruttens A, Waegeneers N, De Witte B. (2023). Short- and long-term assessment of PAH, PCB, and metal contamination in the Belgian part of the North Sea. Chemosphere, 310: 136905
CrossRef
Google scholar
|
[41] |
Viana A T, Caetano T, Covas C, Santos T, Mendo S. (2018). Environmental superbugs: the case study of Pedobacter spp. Environmental Pollution, 241: 1048–1055
CrossRef
Google scholar
|
[42] |
Wu J, Lu J, Li L, Min X, Luo Y. (2018). Pollution, ecological-health risks, and sources of heavy metals in soil of the northeastern Qinghai-Tibet Plateau. Chemosphere, 201: 234–242
CrossRef
Google scholar
|
[43] |
Yang L, Liu W, Zhu D, Hou J, Ma T, Wu L, Zhu Y, Christie P. (2018). Application of biosolids drives the diversity of antibiotic resistance genes in soil and lettuce at harvest. Soil Biology & Biochemistry, 122: 131–140
CrossRef
Google scholar
|
[44] |
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
CrossRef
Google scholar
|
[45] |
Zhang Q, Liu J, Wei N, Song C, Peng J, Wu L, Mao H. (2023). Identify the contribution of vehicle non-exhaust emissions: a single particle aerosol mass spectrometer test case at typical road environment. Frontiers of Environmental Science & Engineering, 17(5): 62
CrossRef
Google scholar
|
[46] |
Zhang Y J, Hu H W, Yan H, Wang J T, Lam S K, Chen Q L, Chen D, He J Z. (2019). Salinity as a predominant factor modulating the distribution patterns of antibiotic resistance genes in ocean and river beach soils. Science of the Total Environment, 668: 193–203
CrossRef
Google scholar
|
/
〈 | 〉 |