Research progress on antibiotic resistance genes in typical marine ecosystems
WANG Wei1, ZHANG Xiao-di1, GAO Hui2, YANG Song-yue3, YOU Jun-jie1, ZHANG Yin-tian1, ZHI Li-wen1, NA Guang-shui1
1. Yazhou Bay Innovation Institute/Hainan Key Laboratory for Coastal Marine Eco-environment and Carbon Sink/College of Ecology and Environment, Hainan Tropical Ocean University, Sanya 572022, China; 2. National Marine Environmental Monitoring Center, Dalian 116023, China; 3. College of Chemistry and Chemical Engineering, Ocean University of China, Qingdao 266100, China
Abstract：Pollution of antibiotic resistant genes (ARGs) in marine ecosystems is characterized by its concealment and difficulty in governance, posing potential risks to ecology and human health. However, the current researches are most focused on specific marine ecosystems or areas, lacking a comprehensive overview and comparative analysis of ARGs pollution in China's marine ecosystems. The study summarized the presence of ARGs in mangroves, coral reefs, estuaries, and bay ecosystems. It analyzed their major transmission pathways and influencing factors, and discussed the potential ecological risks and assessment methods caused by ARGs. The results indicate that ARGs are ubiquitously presented with exhibit complex compositions in typical marine ecosystems of China. Exogenous inputs are the major driving factors of their prevalence, and the regulatory effects of environmental variables also play an undeniable role. ARGs pose potential hazards to marine ecosystems, however, the current systems for ecological risk quantification are still imperfect. This study provides critical evidence for the comprehensive assessment and effective control of ARG pollution in China's typical marine ecosystems.
[1] Hofer U. Rise in global antibiotic use[J]. Nature Reviews Microbiology, 2022,20(2):63. [2] Zhao H, Wei L, Li H, et al. Appropriateness of antibiotic prescriptions in ambulatory care in China:a nationwide descriptive database study[J]. The Lancet Infectious Diseases, 2021,21(6):847-857. [3] Titilawo Y, Obi L, Okoh A. Antimicrobial resistance determinants of Escherichia coli isolates recovered from some rivers in Osun State, South-Western Nigeria:Implications for public health[J]. Science of The Total Environment, 2015,523:82-94. [4] Zhang Y, Wang J, Lu J, et al. Antibiotic resistance genes might serve as new indicators for wastewater contamination of coastal waters:Spatial distribution and source apportionment of antibiotic resistance genes in a coastal bay[J]. Ecological Indicators, 2020,114:106299. [5] 那广水,隗广科,高会,等.中国近岸海洋和海岛环境中抗生素抗性基因的研究进展[J].海洋环境科学, 2023,42(2):326-332. Na G S, Wei G K, Gao H, et al. Research progress on antibiotic resistance genes in coastal ocean and island environments of China[J]. Marine Environmental Science, 2023,42(2):326-332. [6] Zheng D, Yin G, Liu M, et al. A systematic review of antibiotics and antibiotic resistance genes in estuarine and coastal environments[J]. Science of The Total Environment, 2021,777:146009. [7] 贾世杰,高会旺,祁建华.海洋环境中抗生素抗性基因研究进展[J].环境化学, 2023,42(3):792-804. Jia S J, Gao H W, Qi J H. Antibiotic resistance genes in marine environment-A review[J]. Environmental Chemistry, 2023,42(3):792-804. [8] He L X, He L Y, Gao F Z, et al. Mariculture affects antibiotic resistome and microbiome in the coastal environment[J]. Journal of Hazardous Materials, 2023,452:131208. [9] 李十盛,高会,赵富强,等.水产养殖环境中抗生素抗性基因的研究进展[J].中国环境科学, 2021,41(11):5314-5325. Li S S, Gao H, Zhao F Q, et al. Research progress on the occurrence and influencing factors of antibiotic resistance genes in aquaculture environment[J]. China Environmental Science, 2021,41(11):5314-5325. [10] Han Y, Wang J, Zhao Z, et al. Detecting antibiotic resistance genes and human potential pathogenic Bacteria in fishmeal by culture-independent method[J]. Environmental Science and Pollution Research, 2019,26(9):8665-8674. [11] Wang J H, Lu J, Wu J, et al. Proliferation of antibiotic resistance genes in coastal recirculating mariculture system[J]. Environmental Pollution, 2019,248:462-470. [12] Su Z, Li A, Chen J, et al. Wastewater discharge drives ARGs spread in the coastal area:A case study in Hangzhou Bay, China[J]. Marine Pollution Bulletin, 2020,151:110856. [13] Huang J, Zhu J, Liu S, et al. Estuarine salinity gradient governs sedimentary bacterial community but not antibiotic resistance gene profile[J]. Science of The Total Environment, 2022,806:151390. [14] Chen J, Zhang Z, Lei Z, et al. Occurrence and distribution of antibiotic resistance genes in the coastal sediments of effluent-receiving areas of WWTPs, China[J]. Bioresource Technology Reports, 2020,11:100511. [15] Kotlarska E,Łuczkiewicz A, Pisowacka M, et al. Antibiotic resistance and prevalence of class 1and 2integrons in Escherichia coli isolated from two wastewater treatment plants, and their receiving waters (Gulf of Gdansk, Baltic Sea, Poland)[J]. Environmental Science and Pollution Research, 2015,22(3):2018-2030. [16] Fonti V, Di Cesare A,Šangulin J, et al. Antibiotic Resistance Genes and Potentially Pathogenic Bacteria in the Central Adriatic Sea:Are They Connected to Urban Wastewater Inputs?[J]. Water, 2021,13(23):3335. [17] Williams N L R, Siboni N, McLellan S L, et al. Rainfall leads to elevated levels of antibiotic resistance genes within seawater at an Australian beach[J]. Environmental Pollution, 2022,307:119456. [18] Sazykin I S, Khmelevtsova L E, Seliverstova E Yu, et al. Effect of Antibiotics Used in Animal Husbandry on the Distribution of Bacterial Drug Resistance (Review)[J]. Applied Biochemistry and Microbiology, 2021,57(1):20-30. [19] Zhao B, van Bodegom P M, Trimbos K B. Antibiotic resistance genes in interconnected surface waters as affected by agricultural activities[J]. Biomolecules, 2023,13(2):231. [20] Voigt A M, Zacharias N, Timm C, et al. Association between antibiotic residues, antibiotic resistant bacteria and antibiotic resistance genes in anthropogenic wastewater-An evaluation of clinical influences[J]. Chemosphere, 2020,241:125032. [21] Lin L, Yuan K, Liang X, et al. Occurrences and distribution of sulfonamide and tetracycline resistance genes in the Yangtze River Estuary and nearby coastal area[J]. Marine Pollution Bulletin, 2015, 100(1):304-310. [22] Cao J, Hu Y, Liu F, et al. Metagenomic analysis reveals the microbiome and resistome in migratory birds[J]. Microbiome, 2020,8(1):1-18. [23] Ewbank A C, Esperón F, Sacristán C, et al. Seabirds as anthropization indicators in two different tropical biotopes:A One Health approach to the issue of antimicrobial resistance genes pollution in oceanic islands[J]. Science of The Total Environment, 2021,754:142141. [24] Cardoso M D, Santos A F D M, Rodrigues M D S, et al. Salmonella spp. profiles isolated from seabird samples from the Brazilian coast[J]. Preventive Veterinary Medicine, 2021,193:105413. [25] Cáliz J, Subirats J, Triadó-Margarit X, et al. Global dispersal and potential sources of antibiotic resistance genes in atmospheric remote depositions[J]. Environment International, 2022,160:107077. [26] Rossi F, Péguilhan R, Turgeon N, et al. Quantification of antibiotic resistance genes (ARGs) in clouds at a mountain site (puy de Dôme, central France)[J]. Science of The Total Environment, 2023,865:161264. [27] Zhu L, Zhao Y, Yang K, et al. Host bacterial community of MGEs determines the risk of horizontal gene transfer during composting of different animal manures[J]. Environmental Pollution, 2019,250:166-174. [28] Li W, Su H, Cao Y, et al. Antibiotic resistance genes and bacterial community dynamics in the seawater environment of Dapeng Cove, South China[J]. Science of The Total Environment, 2020,723:138027. [29] Chen B, Liang X, Nie X, et al. The role of class I integrons in the dissemination of sulfonamide resistance genes in the Pearl River and Pearl River Estuary, South China[J]. Journal of Hazardous Materials, 2015,282:61-67. [30] Gao Q, Li Y, Qi Z, et al. Diverse and abundant antibiotic resistance genes from mariculture sites of China's coastline[J]. Science of The Total Environment, 2018,630:117-125. [31] 李媛.高桥红树林区常用抗生素残留及细菌耐药性研究[D].湛江:广东海洋大学, 2013. Li Y. Occurence and distribution of seleted antibitiotics and antibiotic resistance of bacteria isolated in Gaoqiao Mangrove area, China[D]. Zhanjiang:Guangdong Ocean University, 2013. [32] Liu S, Su H, Pan Y F, et al. Spatial and seasonal variations of antibiotics and antibiotic resistance genes and ecological risks in the coral reef regions adjacent to two typical islands in South China Sea[J]. Marine Pollution Bulletin, 2020,158:111424. [33] 姜春霞,黎平,李森楠,等.海南东寨港海水和沉积物中抗生素抗性基因污染特征研究[J].生态环境学报, 2019,28(1):128-135. Jiang C X, Li P, Li S N, et al. Pollution characteristics of antibiotic resistance genes in seawater and sediment of Dongzhai Harbor, Hainan Province[J]. Ecology and Environmental Sciences, 2019,28(1):128-135. [34] 周曙仡聃,朱永官,黄福义.微塑料对海水抗生素抗性基因的影响[J].环境科学, 2021,42(8):3785-3790. Zhou S Y D, Zhu Y G, Huang F Y. Microplastic-induced alterations to antibiotic resistance genes in seawater[J]. Environmental Science, 2021,42(8):3785-3790. [35] 吴效俭,施国静,王莹莹.微塑料影响抗性基因的传播与水平基因转移[J].中国环境科学, 2022,42(8):3957-3968. Wu X J Shi G J, Wang Y Y. Effects of microplastics on the spread and horizontal gene transfer of antibiotic resistance genes[J]. China Environmental Science, 2022,42(8):3957-3968. [36] Gao Q, Li Y, Qi Z, et al. Diverse and abundant antibiotic resistance genes from mariculture sites of China's coastline[J]. Science of The Total Environment, 2018,630:117-125. [37] 黄福义,杨凯,张子兴,等.微塑料对河口沉积物抗生素抗性基因的影响[J].环境科学, 2019,0(5):2234-2239. Huang F Y, Yang K, Zhang Z X, et al. Effects of microplastics on antibiotic resistance genes in estuarine sediments[J]. Environmental Science, 2019,40(5):2234-2239. [38] Zeng Q, Xiang J, Yang C, et al. Microplastics affect nitrogen cycling and antibiotic resistance genes transfer of sediment[J]. Chemical Engineering Journal, 2023,454:140193. [39] Sun R, Li T, Qiu S, et al. Occurrence of antibiotic resistance genes carried by plastic waste from mangrove wetlands of the South China Sea[J]. Science of The Total Environment, 2023,864:161111. [40] Chen Y R, Sha R R, Sun X li, et al. Combined effect of Cu-and ZnO-NPs on antibiotic resistance genes in an estuarine water[J]. Frontiers in Marine Science, 2023,9:1086606. [41] Lu J, Wang Y, Jin M, et al. Both silver ions and silver nanoparticles facilitate the horizontal transfer of plasmid-mediated antibiotic resistance genes[J]. Water Research, 2020,169:115229. [42] Melby E S, Mensch A C, Lohse S E, et al. Formation of supported lipid bilayers containing phase-segregated domains and their interaction with gold nanoparticles[J]. Environmental Science:Nano, 2016,3(1):45-55. [43] 孙源.中国沿海海洋贝类中典型纳米颗粒物的赋存及其对抗生素抗性基因的影响[D].上海:华东师范大学, 2022. Sun Y. Occurrence of typical nanoparticles and their effects on antibiotic resistance genes in marine shellfish along the coast of China[D]. Shanghai:East China Normal University, 2022. [44] Chen Y R, Guo X P, Feng J N, et al. Impact of ZnO nanoparticles on the antibiotic resistance genes (ARGs) in estuarine water:ARG variations and their association with the microbial community[J]. Environmental Science:Nano, 2019,6(8):2405-2419. [45] Zhu Y G, Zhao Y, Li B, et al. Continental-scale pollution of estuaries with antibiotic resistance genes[J]. Nature Microbiology, 2017,2(4):16270. [46] 徐秋鸿,刘曙光,娄厦,等.长江口近岸地区抗生素抗性基因与微生物群落分布特征[J].环境科学, 2023,44(1):158-168. Xu Q H, Liu S G, Lou S, et al. Distributions of antibiotic resistance genes and microbial communities in the nearshore area of the Yangtze River Estuary[J]. Environmental Science, 2023,44(1):158-168. [47] Jiang C, Diao X, Wang H, et al. Diverse and abundant antibiotic resistance genes in mangrove area and their relationship with bacterial communities-A study in Hainan Island, China[J]. Environmental Pollution, 2021,276:116704. [48] Xin R, Zhang Y, Zhang K, et al. Investigation of the antimicrobial susceptibility patterns of marine cyanobacteria in Bohai Bay:Cyanobacteria may be important hosts of antibiotic resistance genes in marine environment[J]. Science of The Total Environment, 2024,909:168516. [49] Wang J, Wang J, Zhao Z, et al. PAHs accelerate the propagation of antibiotic resistance genes in coastal water microbial community[J]. Environmental Pollution, 2017,231:1145-1152. [50] Sepúlveda-Correa A, Daza-Giraldo L V, Polanía J, et al. Genes associated with antibiotic tolerance and synthesis of antimicrobial compounds in a mangrove with contrasting salinities[J]. Marine Pollution Bulletin, 2021,171:112740. [51] Shi X, Xia Y, Wei W, et al. Accelerated spread of antibiotic resistance genes (ARGs) induced by non-antibiotic conditions:Roles and mechanisms[J]. Water Research, 2022,224:119060. [52] Chen J, Su Z, Dai T, et al. Occurrence and distribution of antibiotic resistance genes in the sediments of the East China Sea bays[J]. Journal of Environmental Sciences, 2019,81(7):156-167. [53] Hong B, Ba Y, Niu L, et al. A comprehensive research on antibiotic resistance genes in microbiota of aquatic animals[J]. Frontiers in Microbiology, 2018,9:1617. [54] Calero-Cáceres W, Balcázar J L. Antibiotic resistance genes in bacteriophages from diverse marine habitats[J]. Science of The Total Environment, 2019,654:452-455. [55] 张越,胡雪莹,王旭明.噬菌体编码的抗生素抗性基因研究进展[J].中国环境科学, 2022,42(5):2315-2320. Zhang Y, Hu X Y, Wang X M. Recent advances on antibiotic resistance genes encoded by bacteriophages[J]. China Environmental Science, 2022,42(5):2315-2320. [56] Lu J, Zhang Y, Wu J, et al. Occurrence and spatial distribution of antibiotic resistance genes in the Bohai Sea and Yellow Sea areas, China[J]. Environmental Pollution, 2019,252:450-460. [57] Li Q W, Na G S, Zhang L X, et al. Effects of corresponding and non-corresponding contaminants on the fate of sulfonamide and quinolone resistance genes in the Laizhou Bay, China[J]. Marine Pollution Bulletin, 2018,128:475-482. [58] Li F, Mai Z, Qiu C, et al. Dissemination of antibiotic resistance genes from the Pearl River Estuary to adjacent coastal areas[J]. Marine Environmental Research, 2023,188:105978. [59] Liu S, Xu Q, Lou S, et al. Spatiotemporal distributions of sulfonamide and tetracycline resistance genes and microbial communities in the coastal areas of the Yangtze River Estuary[J]. Ecotoxicology and Environmental Safety, 2023,259:115025. [60] 曹佳雯.三沙湾海水养殖环境中抗生素抗性基因的时空分布特征研究[D].厦门:厦门大学, 2019. Cao J W. Study on the spatial and temporal distribution characteristics of antibiotic resistance genes in mariculture environment in Sansha Bay[D]. Xiamen:Xiamen University, 2019. [61] Wang J, Lu J, Wu J, et al. Seasonal distribution of antibiotic resistance genes under the influence of land-ocean interaction in a semi-enclosed bay[J]. Chemosphere, 2022,301:134718. [62] Zhang Y. Occurrence of intracellular and extracellular antibiotic resistance genes in coastal areas of Bohai Bay (China) and the factors affecting them[J]. Environmental Pollution, 2018,236:126-136. [63] Lu X M, Lu P Z. Seasonal variations in antibiotic resistance genes in estuarine sediments and the driving mechanisms[J]. Journal of Hazardous Materials, 2020,383:121164. [64] Niu Z G, Zhang K, Zhang Y. Occurrence and distribution of antibiotic resistance genes in the coastal area of the Bohai Bay, China[J]. Marine Pollution Bulletin, 2016,107(1):245-250. [65] Zhao Z, Zhang K, Wu N, et al. Estuarine sediments are key hotspots of intracellular and extracellular antibiotic resistance genes:A high-throughput analysis in Haihe Estuary in China[J]. Environment International, 2020,135:105385. [66] 陆大培.长江口及邻近海域沉积物中抗生素抗性基因时空分布特征及其与环境因子相关性研究[D].上海:华东师范大学, 2019. Lu D P. Temporal and spatial distribution characteristics of antibiotic resistance genes and their correlations with environmental factors in sediments from the Yangtze Estuary and adjacent coastal area[D]. Shanghai:East China Normal University, 2019. [67] Li W, Su H, Cao Y, et al. Antibiotic resistance genes and bacterial community dynamics in the seawater environment of Dapeng Cove, South China[J]. Science of The Total Environment, 2020,723:138027. [68] 姜春霞.海南红树林沉积物中抗生素分布特征及抗性基因多样性研究[D].海口:海南大学, 2019. Jiang C X. The distribution of antibiotics and the diversity of antibiotic resistance genes in sediments from Hainan Mangrove area.[D]. Haikou:Hainan University, 2019. [69] 阮孙兰.海南东寨港红树林典型区域抗生素抗性基因时空分布特征及影响因素研究[D].海口:海南大学, 2018. Ruan S L. Spatial and temporal distribution of antibiotic resistance genes and its influencing factors in a typical mangrove area of Dongzhai Harbor, Hainan[D]. Haikou:Hainan University, 2018. [70] Liu T, Lun J, Zheng P, et al. Diversity and distribution of antibiotics and antibiotic resistance genes in seven national mangrove nature reserves, South China[J]. International Biodeterioration&Biodegradation, 2020,153:105000. [71] Liu Z, Wan X, Zhang C, et al. Deep sequencing reveals comprehensive insight into the prevalence, mobility, and hosts of antibiotic resistance genes in mangrove ecosystems[J]. Journal of Environmental Management, 2023,335:117580. [72] Zhao H, Zhang J, Chen X, et al. Climate and nutrients regulate biographical patterns and health risks of antibiotic resistance genes in mangrove environment[J]. Science of The Total Environment, 2023, 854:158811. [73] Wang C, Hu R, Strong P J, et al. Prevalence of antibiotic resistance genes and bacterial pathogens along the soil-mangrove root continuum[J]. Journal of Hazardous Materials, 2021,408:124985. [74] Ghosh A, Saha R, Bhadury P. Metagenomic insights into surface water microbial communities of a South Asian mangrove ecosystem[J]. PeerJ, 2022,10:e13169. [75] Sun R, Liu Y, Li T, et al. Plastic wastes and surface antibiotic resistance genes pollution in mangrove environments[J]. Environmental Monitoring and Assessment, 2023,195(6):634. [76] 吴钟解,唐佳,蔡文启,等.海南岛东海岸珊瑚礁生态系统中抗生素抗性基因的赋存特征[J].热带生物学报, 2022,13(5):464-471. Wu Z J, Tang J, Cai W Q, et al. Occurrence and charact-eristics of antibiotic resistance genes in the oral reef ecosystems along the east coast of Hainan Island[J]. Journal of Tropical Biology, 2022, 13(5):464-471. [77] 陈笑雪,王智源,管仪庆,等.淡水环境中抗生素抗性基因的来源、归趋和风险[J].生态毒理学报, 2021,16(3):14-27. Chen X X, Wang Z, Guan Y Q, et al. Source, fate and risk of antibiotic resistance genes in freshwater environment[J]. Asian Journal of Ecotoxicology, 2021,16(3):14-27. [78] Qin Y, Ren X, Zhang Y, et al. Distribution characteristics of antibiotic resistance genes and microbial diversity in the inshore aquaculture area of Wenchang, Hainan, China[J]. Science of The Total Environment, 2024,914:169695. [79] Zhao S, Liu X, Cheng D, et al. Temporal-spatial variation and partitioning prediction of antibiotics in surface water and sediments from the intertidal zones of the Yellow River Delta, China[J]. Science of The Total Environment, 2016,569-570:1350-1358. [80] Zhang R, Yu K, Li A, et al. Antibiotics in coral reef fishes from the South China Sea:Occurrence, distribution, bioaccumulation, and dietary exposure risk to human[J]. Science of The Total Environment, 2020,704:135288. [81] Wu D, Su Y, Xi H, et al. Urban and agriculturally influenced water contribute differently to the spread of antibiotic resistance genes in a mega-city river network[J]. Water Research, 2019,158:11-21. [82] Zou K, Zhu Y, Jiang Y, et al. Distinct stochastic processes drive bacterial community assembly and co-occurrence patterns with common antibiotic resistance genes in two highly urbanised coastal ecosystems of the Pearl River Estuary[J]. Journal of Hazardous Materials, 2023,459:132161. [83] Wei G, Gao H, Li S, et al. The occurrence and abundance of antibiotic resistance genes in rivers of tropical islands:a case of Hainan Island, China[J]. Environmental Science and Pollution Research International, 2023,30(38):88936-88948. [84] Gao H, Zhang L, Lu Z, et al. Complex migration of antibiotic resistance in natural aquatic environments[J]. Environmental Pollution, 2018,232:1-9. [85] Xiong S, Wang K, Yan H, et al. Geographic patterns and determinants of antibiotic resistomes in coastal sediments across complex ecological gradients[J]. Frontiers in Microbiology, 2022,13:922580. [86] Ohore O E, Ifon B E, Wang Y, et al. Vertical changes in water depth and environmental variables drove the antibiotics and antibiotic resistomes distribution, and microbial food web structures in the estuary and marine ecosystems[J]. Environment International, 2023, 178:108118. [87] Zhang M, Hou L, Zhu Y, et al. Composition and distribution of bacterial communities and antibiotic resistance genes in fish of four mariculture systems[J]. Environmental Pollution, 2022,311:119934. [88] Nielsen M C, Wang N, Jiang S C. Acquisition of antibiotic resistance genes on human skin after swimming in the ocean[J]. Environmental Research, 2021,197:110978. [89] Amarasiri M, Sano D, Suzuki S. Understanding human health risks caused by antibiotic resistant bacteria (ARB) and antibiotic resistance genes (ARG) in water environments:Current knowledge and questions to be answered[J]. Critical Reviews in Environmental Science and Technology, 2020,50(19):2016-2059. [90] Goh S G, Jiang P, Ng C, et al. A new modelling framework for assessing the relative burden of antimicrobial resistance in aquatic environments[J]. Journal of Hazardous Materials, 2022,424:127621. [91] Cuadrat R R C, Sorokina M, Andrade B G, et al. Global ocean resistome revealed:Exploring antibiotic resistance gene abundance and distribution in TARA Oceans samples[J]. GigaScience, 2020, 9(5):1-12.
