Enunciatively, antibiotic resistance genes (ARGs) have attracted global attention because of their pronounced dangers on human health or ecosystems. The bacterial community (BC) and ARG profile transmission of the fish/water samples were analyzed under high-throughput (HT)-qPCR. ARGs from different fish samples and different ponds varied significantly. In the same pond type, the ARGs in water outnumbered the ARGs in fish based on 16S rRNA gene copies with significant differences, although their genetic structures were similar based on shared characteristics. The highest ARG removal efficiencies of the five pond types rated 98.08–75.6% for top 6 antibiotics (fluoroquinolone > glycopeptide > tetracycline > aminoglycoside > macrolide–lincosamide–streptogramin B > rifamycin). Majority (33) of shared ARGs were discovered in water, although 14 featured in fish and 7 in both mediums. Fusobacteria (0.5–61%), Bacteroidetes (11–57%), and Proteobacteria (15–53%) dominated other phyla. Spirochaetes, Epsilonbacteraeota, aad7, and mefA demonstrated stronger potential to change ARG structures.
Shared ARG redundancy correlation analyses revealed tighter relationships among Bacteroidetes, Spirochaetes, and Epsilonbacteraeota, which probably favored ARG partitioning. Although 28.07% variations were unexplainable, mobile genetic elements + BC predominantly influenced 35.50% ARG structural changes while transposase resistance genes, and BC contributed 10.90% and 25.44%, respectively. Analyzed ARGs of the entire aquaculture systems demonstrated significant differential characteristics (numbers, relative abundances, and structural distributions) (p < 0.05). The fish and water ARGs detected in this study constitute indicators for tracing ARG contamination in large-scale environments where antibiotics usage is ubiquitous. The findings imply that the entire aquaculture system understudied are hotspots for advanced antibiotic resistome analyses.
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References
1.
AmorosoV.B. (2000). “Status, Species Richness and Ecosystem Diversity in Mindanao Islands, “Saving the Hottest of the Hotspots”. Proceedings of the National Biodiversity Conservation Priority-Setting Workshop. Mindanao Regional Consultation Malagos Garden Resort, Davao City, Philippines, pp. 17–32.
California Environmental Associates (CEA). (2018). Offshore Finfish Aquaculture Global Review and U.S. Prospects. CA, USA: The David Lucide & Packard Foundation, p. 1.
4.
CareyT.M.D., YonA., BeadlesC., and WinesR. (2020). Identifying and Prioritizing Research Gap. UNC, The Cecil G. NC, USA: SHEP Center for Health Services Research, p. 1.
5.
CaoJ., HuY., LiuF., WangY., BiY., LvN., LiJ., ZhuB., and GaoG.F. (2020). Metagenomic analysis reveals the microbiome and resistome in migratory birds. Microbiome, 8, 26.
6.
DongH., ChenY., WangJ., ZhangY., ZhangP., LiX., ZouJ., and ZhouA. (2021). Interactions of microplastics and antibiotic resistance genes and their effects on the aquaculture environments. J. Hazard. Mater. 403, 0304.
7.
DuB., YangQ., WangR., WangR., WangQ., and XinY. (2019). Evolution of antibiotic resistance and the relationship between the antibiotic resistance genes and microbial compositions under long-term exposure to tetracycline and sulfamethoxazole. Int. J. Environ. Res. Public Health, 16, 4681.
8.
GrahamD.W., BergeronG., BourassaM.W., DicksonJ., GomesF., HoweA., KahnL.H., MorleyP.S., ScottH.M., SimjeeS., SingerR.S., SmithT.C., StorrsC., and WittumT.E. (2019). Complexities in understanding antimicrobial resistance across domesticated animal, human, and environmental systems. Ann. N. Y. Acad. Sci. 1441, 17.
9.
GufeC., HodoboT.C., MbonjaniB., MajongaO., MarumureJ., MusariS., JongiG., MakayaP.V., and MachakwaJ. (2019). Antimicrobial profiling of bacteria isolated from fish sold at informal market in Mufakose, Zimbabwe. Int. J. Microbiol. 2019, 1.
10.
GuoX., YangY., LuD.P., NiuZ.S., FengJ.N., ChenY.R., TouF.Y., GarnerE., XuJ., LiuM., and Hochella, JrM.F. (2018). Biofilms as a sink for antibiotic resistance genes (ARGs) in the Yangtze Estuary. Water Res. 129, 277.
11.
HanQ.F., ZhaoS., ZhangX.R., WangX.L., SongC., and WangS.G. (2020a). Distribution, combined pollution and risk assessment of antibiotics in typical marine aquaculture farms surrounding the Yellow Sea, North China. Env. Int. 138, 1.
12.
HanZ., ZhangY., AnW., LuJ., HuJ., and YangM. (2020b). Antibiotic resistomes in drinking water sources across a large geographical scale: Multiple drivers and co-occurrence with opportunistic bacterial pathogens. Water Res. 183, 0043.
13.
HaysL. (2020). The Current State of Antibiotics in Aquaculture. Earth City, MO: QB Labs.
14.
HeX., XuY., ChenJ., LingJ., LiY., HuangL., ZhouX., ZhengL., and XieG. (2017). Evolution of corresponding resistance genes in the water of fish tanks with multiple stresses of antibiotics and heavy metals. Water Res. 124, 39.
15.
HongB., YuS., NiuY., DingJ., LinQ.Y., LinX.D., and HuW.W. (2020). Spectrum and environmental risks of residual pharmaceuticals in stream water with emphasis on its relation to epidemic infectious disease and anthropogenic activity in watershed. J. Hazard. Mater. 385, 121594.
16.
HouL., ZhangL., LiF., HuangS., YangJ., MaC., ZhangD., YuC., and HuA. (2021). Urban ponds as hotspots of antibiotic resistome in the urban environment. J. Hazard. Mater. 403, 124008.
17.
HuY.J., and CowlingB.J. (2020). Reducing antibiotics use in Livestock China. Bull. World Health Organ. 98, 360.
18.
HuertaB., MartiE., GrosM., and ArmengolJ. (2013). Exploring the links between antibiotic occurrence, antibiotic resistance, and bacterial communities in water supply reservoirs. Sci. Total Environ. 456–457, 161.
19.
JiaoY-N., ZhouZ-C., ChenT., WeiY-Y., ZhengJ., GaoR-X., and ChenH. (2018). Biomarkers of antibiotic resistance genes during seasonal changes in waste water treatment systems. Environ. Pollut. 234, 79.
20.
KimY.B., JeonJ.H., ChoiS., ShinJ., LeeY., and KimY.M. (2018). Use of a filtering process to remove solid waste and antibiotic resistance genes from effluent of a flow-through fish farm. Sci. Total Environ. 615, 289.
21.
KovalakovaP., CizmasL., McDonaldT.J., MarsalekB., FengM., and SharmaV.K. (2020). Occurrence and toxicity of antibiotics in the aquatic environment: A review. Chemosphere, 251, 126351.
22.
LaiW.W.P., LinY.C., WangY.H., GuoY.L., and LinA.Y.C. (2018). Occurrence of emerging contaminants in aquaculture waters: Cross-contamination between aquaculture systems and surrounding waters. Water Air Soil Pollut. 229, 1.
23.
LalumeraG.M., CalamariD., GalliP., CastiglioniS., CrosaG., and FanelliR. (2004). Preliminary investigation on the environmental occurrence and effects of antibiotics used in aquaculture in Italy. Chemosphere, 54, 661.
24.
LuJ., ZhangY.X., and WuJ. (2020). Continental-scale spatio-temporal distribution of antibiotic resistance genes in coastal waters along coastline of China. Chemosphere, 247, 125908.
MeiK., LiaoL., ZhuY., LuP., WangZ., DahlgrenR.A., and ZhangM. (2014). Evaluation of spatial-temporal variations and trends in surface water quality across a rural-suburban-urban interface. Environ. Sci. Pollut. Res. 21, 8036.
27.
MogS.N., TesiaS., WaikhomD., PandaS.P., SharmaS., and VarshneyS. (2020). Problems of antibiotic resistance associated with oxytetracycline use in aquaculture: A review. J. Entomol. Zool. Stud. 8, 75.
28.
OksanenJ., BlanchetF.G., KindtR., LegendreP., MinchinP.R., O'HaraR.B., SimpsonG.L., SolymosP., StevensM.H.H., and WagnerH.H. (2014). Vegan: Community Ecology Package. R package version. 2.2-0.
29.
OuyangL., ChenH., LiuX., WongM.H., XuF., YangX., XuW., ZengQ., WangW., and LiS. (2020). Characteristics of spatial and seasonal bacterial community structures in a river under anthropogenic disturbances. Environ. Pollut. 264, 0269.
30.
Protocol for Agarose gel electrophoresis. Available at: public.callutheran.edu/~revie/protocols/Agarosegels-TBE.pdf (accessed August27, 2021).
31.
SáenzJ.S., MarquesT.V., BaroneR., CyrinoJ., KublikS., NesmeJ., SchloterM., RathS., and VestergaardG. (2019). Oral administration of antibiotics increased the potential mobility of bacterial resistance genes in the gut of the fish Piaractus mesopotamicus. Microbiome, 7, 24.
32.
ShenX., JinG., ZhaoY., and ShaoX. (2020). Prevalence and distribution analysis of antibiotic resistance genes in a large-scale aquaculture environment. Sci. Total Environ. 711, 134626.
33.
TiimubB.M., ZhouZ.C., ZhuL., LiuY., ShauiX., XuL., NiyungekoC., MengL., SunY., and ChenH. (2021). Characteristics of bacterial community and ARGs profile in engineered goldfish tanks with stresses of sulfanilamide and copper. Environ. Sci. Pollut. Res. 28, 38706.
34.
TongL., QinL., GuanC., WilsonM.E., LiX., ChengD., MaJ., LiuH., and GongF. (2020). Antibiotic resistance gene profiling in response to antibiotic usage and environmental factors in the surface water and groundwater of Honghu Lake, China. Environ. Sci. Pollut. Res. 27, 31995.
35.
TurnerS., PryerK.M., MiaoV.P.W., and PalmerJ.D. (1999). Investigating deep phylogenetic relationships among cyanobacteria and plastids by small submit rRNA sequence analysis. J. Eukaryot. Microbiol. 46, 327.
36.
WangJ.H., LuJ., WuJ., ZhangY.X., and ZhangC. (2019). Proliferation of antibiotic resistance genes in coastal recirculating mariculture system. Environ. Pollut. 248, 462.
37.
WoolhouseM., WaughC., PerryM.R., and NairH. (2016). Global disease burden due to antibiotic resistance -State of the evidence. J. Global Health. 6, 1.
38.
XuH., WangL., BaoX., JiangN., YangX., HaoZ., ChangY., and DingJ. (2019). Microbial communities in sea cucumber (Apostichopus japonicus) culture pond and the effects of environmental factors. Aquac. Res. 50, 1257.
39.
YangY., LiZ., SongW., DuL, YeC., ZhaoB., LiuW., DengD., PanY., LinH., and CaoX. (2019). Metagenomic insights into the abundance and composition of resistance genes in aquatic environments: Influence of stratification and geography. Environ. Int. 127, 371.
40.
YangY., XingS., ChenY., WuR., WangY., MiJ., and LiaoX. (2021). Profiles of bacteria/phagecomediated ARGs in pig farm wastewater treatment plants in China: Association with mobile genetic elements, bacteria communities and environmental factors. J. Hazard. Mater. 404, Part B, 124149.
41.
YuanJ., NiM., LiuM., ZhengY., and GuZ. (2019). Occurrence of antibiotics and antibiotic resistance genes in a typical estuary aquaculture region of Hangzhou Bay, China. Mar. Pollut. Bull. 138, 376.
42.
YiY., LinY., WangW., and SongJ. (2021). Habitat and seasonal variations in bacterial community structure and diversity in sediments of a Shallow lake. Eco Ind. 120, 106959.
43.
YuK., LiP., ChenY., ZhangB., HuangY., HuangF., and HeY. (2020). Antibiotic resistome associated with microbial communities in an integrated wastewater reclamation system. Water Res. 173, 115541.
44.
ZhangJ., BuheC., YuD., ZhongH., and WeiY. (2020). Ammonia stress reduces antibiotic efflux but enriches horizontal gene transfer of antibiotic resistance genes in anaerobic digestion. Bioresour. Technol. 295, 122191.
45.
ZhaoY., YangQ.E., ZhouX., WangF., MuurinenJ., VirtaM.P., BrandtK.K., and ZhuY. (2020). Antibiotic resistome in the livestock and aquaculture industries: Status and solutions. Crit. Rev. Environ. Sci. Technol. 51, 1.
46.
ZhengQ., ZhangR., WangY., PanX., TangJ., and ZhangG. (2012). Occurrence and distribution of antibiotics in the Beibu Gulf, China: impacts of river discharge and aquaculture activities. Mar. Environ. Res. 78, 26.
47.
ZhengJ., GaoR.X., WeiX.Y., ChenT., FanJ.Q., ZhouZ.C., TiimubB.M., JiaoY., and ChenH. (2017). High-throughput profiling and analysis of antibiotic resistance genes in East Tiaoxi River, China. Environ. Pollut. 230, 648.
48.
ZhengJ., ZhouZ., WeiY., ChenT., FengW., and ChenH. (2018). High-throughput profiling of seasonal variations of antibiotic resistance gene transport in a peri-urban river. Environ Int. 114, 87.
49.
ZhouM., YuS., HongB., LiJ., HanH., and QieG. (2021a). Antibiotics control in aquaculture requires more than antibiotic-free feeds: A tilapia farming case. Environ. Pollut. 268 (Pt B), 115854.
50.
ZhouQ., WangM., ZhongX., LiuP., XieX., WangxiaoJ., and SunY. (2019). Dissemination of resistance genes in duck/fish polyculture ponds in Guangdong Province: Correlations between Cu and Zn and antibiotic resistance genes. Environ. Sci. Pollut. Res. 26, 8182.
51.
ZhouZ., FengW., HanY., ZhengJ., ChenT., WeiY., GillingsM., ZhuY., and ChenH. (2018). Prevalence and transmission of antibiotic resistance and microbiota between humans and water environments. Environ. Int. 121 (Pt 2), 1155.
52.
ZhouZ., LinZ., ShuaiX., ZhengJ., MengL., ZhuL., SunY., Shang. W., and ChenH. (2021b). Temporal variation and sharing of antibiotic resistance genes between water and wild fish gut in a peri-urban river. J. Environ. Sci. 103, 12.
53.
ZhouZ., ZhengJ., WeiY., ChenT., DahlgrenR.A., ShangX., and ChenH. (2017). Antibiotic resistance genes in an urban river as impacted by bacterial community and physicochemical parameters. Environ. Sci. Pollut. Res. 24, 23753.
54.
ZhuY., PanD., HuX., HanH., LinM., and WangC. (2017). An electrochemical sensor based on reduced graphene oxide/gold nanoparticles modified electrode for determination of iron in coastal waters. Sensors Actuators B Chem. 243, 1.
55.
ZhuY.G., JohnsonT.A., SuJ.Q., QiaoM., GuoG.X., StedtfeldR.D., HashshamS.A., and TiedjeJ.M. (2013). Diverse and abundant antibiotic resistance genes in Chinese swine farms. Proc. Natl. Acad. Sci. U. S. A. 110, 3435.
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