Cited by 73Pharmaceutical and Antibiotic Environmental ImpactsAntibiotic Resistance in BacteriaWastewater Treatment and Nitrogen Removal

Biological Mitigation of Antibiotic Resistance Gene Dissemination by Antioxidant-Producing Microorganisms in Activated Sludge Systems

Open access
Ren, Chong-Yang, Wu, En-Ling, Hartmann, Erica M., Zhao, He-Ping·2021·Environmental Science & Technology

Abstract

Antibiotic resistance is the principal mechanism of an evergrowing bacterial threat. Antibiotic residues in the environment are a major contributor to the spread of antibiotic resistance genes (ARGs). Subinhibitory concentrations of antibiotics cause bacteria to produce reactive oxygen species (ROS), which can lead to mutagenesis and horizontal gene transfer (HGT) of ARGs; however, little is known about the mitigation of ARG dissemination through ROS removal by antioxidants. In this study, we examine how antioxidant-producing microorganisms inoculated in replicate activated sludge systems can biologically mitigate the dissemination of ARGs. Through quantitative polymerase chain reaction (qPCR), we showed that antioxidant-producing microorganisms could decrease the persistence of the RP4 plasmid and alleviate enrichment of ARGs ( sul1 ) and class 1 integrons ( intl1 ). Metagenomic sequencing identified the most diverse resistome and the most mutated Escherichia coli ARGs in the reactor that contained antibiotics but no antioxidant-producing microorganisms, suggesting that antioxidant-producing microorganisms mitigated ARG enrichment and mutation. Host classification revealed that antioxidant-producing microorganisms decreased the diversity of ARG hosts by shaping the microbial community through competition and functional pathway changes. Conjugative experiments demonstrated that conjugative transfer of ARGs could be mitigated by coculture with antioxidant-producing microorganisms. Overall, this is a novel study that shows how ARG enrichment and HGT can be mitigated through bioaugmentation with antioxidant-producing microorganisms.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1021/acs.est.1c04641

Cites

4 of 4 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • Antioxidant-producing microorganisms can mitigate ARG enrichment and dissemination by reducing ROS levels, limiting genetic mutations and plasmid-mediated ARG transfer.

    “Recent studies have demonstrated that antioxidant-producing microorganisms can mitigate ARG enrichment and dissemination by reducing ROS levels, thereby limiting genetic mutations and plasmid-mediated ARG transfer in microbial communities [87,302].”

    From Harnessing bacterial consortia for effective bioremediation: targeted removal of heavy metals, hydrocarbons, and persistent pollutants (2025) · cites this paper as [302]

    The Results and Discussion report a smaller antibiotic-induced rise in ROS in bioaugmented reactors, fewer mutated E. coli ARGs, and reduced conjugative transfer of the ARG-carrying RP4 plasmid. But the paper says bioaugmentation *may* reduce mutation by scavenging ROS and presents reduced oxidative stress as a hypothesis for the transfer result. The citing sentence overstates those proposed mechanisms as demonstrated causal effects. (LLM, conf=0.86)

    Experimental — accuracy not yet measured

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

Flagged first, then by citations

Research works printed but not linked: 76

  1. [2]Davies J; Davies D Origins and evolution of antibiotic resistance. Microbiol. Mol. Biol. R 2010, 74, 417– 433. PMC2937522 20805405
  2. [3]Lopatkin AJ; Huang S; Smith RP; Srimani JK; Sysoeva TA; Bewick S; Karig DK; You L Antibiotics as a selective driver for conjugation dynamics. Nat. Microbiol 2016, 1, 16044. 27572835 PMC5010019
  3. [4]Pärnänen KMM; Narciso-Da-Rocha C; Kneis D; Berendonk TU; Cacace D; Do TT; Elpers C; Fatta-Kassinos D; Henriques I; Jaeger T; Karkman A; Martinez JL; Michael SG; Michael-Kordatou I; O'Sullivan K; Rodriguez-Mozaz S; Schwartz T; Sheng H; Sørum H; Stedtfeld RD; Tiedje JM; Giustina SVD; Walsh F; Vaz-Moreira I; Virta M; Manaia CM Antibiotic resistance in European wastewater treatment plants mirrors the pattern of clinical antibiotic resistance prevalence. Sci. Adv 2019, 5, eaau9124. 30944853 PMC6436925
  4. [6]Kraemer SA; Ramachandran A; Perron GG Antibiotic pollution in the environment: from microbial ecology to public policy. Microorganisms 2019, 7, 180. PMC6616856 31234491
  5. [7]He Y; Yuan QB; Mathieu J; Stadler L; Senehi N; Sun R; Alvarez PJJ Antibiotic resistance genes from livestock waste: occurrence, dissemination, and treatment. npj Clean Water 2020, 3, 4.
  6. [9]Wang J; Chu L; Wojnárovits L; Takács E Occurrence and fate of antibiotics, antibiotic resistant genes (ARGs) and antibiotic resistant bacteria (ARB) in municipal wastewater treatment plant: An overview. Sci. Total Environ 2020, 744, 140997. 32755790
  7. [10]Baquero F; Martinez JL; Canton R Antibiotics and antibiotic resistance in water environments. Curr. Opin. Biotechnol 2008, 19, 260– 265. 18534838
  8. [11]Kovalakova P; Cizmas L; McDonald TJ; Marsalek B; Feng M; Sharma VK Occurrence and toxicity of antibiotics in the aquatic environment: A review. Chemosphere 2020, 251, 126351. 32443222
  9. [12]Zhao X; Li Y; Yang L; Wang X; Chen Z; Shen J Screen and study of tetracycline-degrading bacteria from activated sludge and granular sludge. Clean 2018, 46, 1700411.1– 1700411.6.
  10. [13]Andam CP; Fournier GP; Gogarten JP Multilevel populations and the evolution of antibiotic resistance through horizontal gene transfer. FEMS Microbiol. Rev 2011, 35, 756– 767. 21521245
  11. [14]Davies J Inactivation of antibiotics and the dissemination of resistance genes. Science 1994, 264, 375– 382. 8153624
  12. [15]Fonseca JD; Knight GM; McHugh TD The complex evolution of antibiotic resistance in Mycobacterium tuberculosis. Int. J. Infect. Dis 2015, 32, 94– 100. 25809763
  13. [16]Wellington EMH; Boxall ABA; Cross P; Feil EJ; Gaze WH; Hawkey PM; Johnson-Rollings AS; Jones DL; Lee NM; Otten W; Thomas CM; Williams AP The role of the natural environment in the emergence of antibiotic resistance in Gram-negative bacteria. Lancet Infect. Dis 2013, 13, 155– 165. 23347633
  14. [17]Watkins RR; Bonomo RA Overview: The ongoing threat of antimicrobial resistance. Infect. Dis. Clin. North Am 2020, 34, 649– 658. 33011053
  15. [18]Dwyer DJ; Kohanski MA; Hayete B; Collins JJ Gyrase inhibitors induce an oxidative damage cellular death pathway in Escherichia coli. Mol. Syst. Biol 2007, 3, 91. 17353933 PMC1847949
  16. [19]Kohanski MA; Dwyer DJ; Hayete B; Lawrence CA; Collins JJ A common mechanism of cellular death induced by bactericidal antibiotics. Cell 2007, 130, 797– 810. 17803904
  17. [20]Kohanski MA; Dwyer DJ; Wierzbowski J; Cottarel G; Collins JJ Mistranslation of membrane proteins and two-component system activation trigger antibiotic-mediated cell death. Cell 2008, 135, 679– 690. 19013277 PMC2684502
  18. [21]Brumaghim JL; Li Y; Henle E; Linn S Effects of hydrogen peroxide upon nicotinamide nucleotide metabolism in Escherichia coli: changes in enzyme levels and nicotinamide nucleotide pools and studies of the oxidation of NAD(P)H by Fe(III). J. Biol. Chem 2003, 278, 42495– 42504. 12913009
  19. [22]Fridovich I The biology of oxygen radicals. Science 1978, 201, 875– 880. 210504
  20. [23]Goswami M; Mangoli SH; Jawali N Involvement of reactive oxygen species in the action of ciprofloxacin against Escherichia coli. Antimicrob. Agents Chemother 2006, 50, 949– 954. 16495256 PMC1426460
  21. [24]Wang X; Zhao X Contribution of oxidative damage to antimicrobial lethality. Antimicrob. Agents Chemother 2009, 53, 1395– 1402. 19223646 PMC2663088
  22. [25]Fang FC Antibiotic and ROS linkage questioned. Nat. Biotechnol 2013, 31, 415– 416. 23657395
  23. [26]Kohanski MA; DePristo MA; Collins JJ Sublethal antibiotic treatment leads to multidrug resistance via radical-induced mutagenesis. Mol. Cell 2010, 37, 311– 320. 20159551 PMC2840266
  24. [28]Dwyer DJ; Belenky PA; Yang JH; Macdonald IC; Martell JD; Takahashi N; Chan CTY; Lobritz MA; Braff D; Schwarz EG; Pati M; Vercruysse M; Ralifo PS; Allison KR; Khalil AS; Ting AY; Walker GC; Collins JJ Antibiotics induce redox-related physiological alterations as part of their lethality. Proc. Natl. Acad. Sci. U.S.A 2014, 111, E2100– E2109. 24803433 PMC4034191
  25. [29]Qiu Z; Yu Y; Chen Z; Jin M; Yang D; Zhao Z; Wang J; Shen Z; Wang X; Qian D; Huang A; Zhang B; L. J Nanoalumina promotes the horizontal transfer of multiresistance genes mediated by plasmids across genera. Proc. Natl. Acad. Sci. U.S.A 2012, 109, 4944– 4949. 22411796 PMC3323979
  26. [30]Wang Y; Lu J; Mao LK; Li J; Yuan ZG; Bond PL; Guo JH Antiepileptic drug carbamazepine promotes horizontal transfer of plasmid-borne multi-antibiotic resistance genes within and across bacterial genera. ISME J. 2019, 13, 509– 522. 30291330 PMC6331567
  27. [31]Wang Y; Lu J; Engelstadter J; Zhang S; Ding PB; Mao LK; Yuan ZG; Bond PL; Guo JH Non-antibiotic pharmaceuticals enhance the transmission of exogenous antibiotic resistance genes through bacterial transformation. ISME J. 2020, 14, 2179– 2196. 32424247 PMC7367833
  28. [32]Shi LD; Xu QJ; Liu JY; Han ZX; Zhao HP Will a Non-antibiotic Metalloid Enhance the Spread of Antibiotic Resistance Genes: The Selenate Story. Environ. Sci. Technol 2021, 55, 1004– 1014. 33356195
  29. [33]Moore MM; Breedveld MW; Autor AP The role of carotenoids in preventing oxidative damage in the pigmented yeast, Rhodotorula mucilaginosa. Arch. Biochem. Biophys 1989, 270, 419– 431. 2650623
  30. [34]Frengova GI; Beshkova DM Carotenoids from Rhodotorula and Phaffia: yeasts of biotechnological importance. J. Ind. Microbiol. Biotechnol 2009, 36, 163– 180. 18982370
  31. [35]Asker D; Beppu T; Ueda K Unique diversity of carotenoid-producing bacteria isolated from Misasa, a radioactive site in Japan. Appl. Microbiol. Biotechnol 2007, 77, 383– 392. 17828533
  32. [36]Takaichi S Carotenoids in Algae: Distributions, Biosyntheses and Functions. 2011, 9, 1101– 1118. PMC3131562 21747749
  33. [37]Shah MMR; Liang YM; Cheng JJ; Daroch M Astaxanthin-Producing Green Microalga Haematococcus pluvialis: From Single Cell to High Value Commercial Products. Front. Plant Sci 2016, 7, 531. 27200009 PMC4848535
  34. [38]Makarova KS; Aravind L; Wolf YI; Tatusov RL; Minton KW; Koonin EV; Daly MJ Genome of the extremely radiation-resistant bacterium Deinococcus radiodurans viewed from the perspective of comparative genomics. Microbiol. Mol. Biol. Rev 2001, 65, 44– 79. 11238985 PMC99018
  35. [39]Xu Z; Tian B; Sun Z; Lin J; Hua Y Identification and functional analysis of a phytoene desaturase gene from the extremely radioresistant bacterium Deinococcus radiodurans. Microbiology 2007, 153, 1642– 1652. 17464079
  36. [40]Daly MJ; Gaidamakova EK; Matrosova VY; Kiang JG; Fukumoto R; Lee DY; Wehr NB; Viteri GA; Berlett BS; Levine RL Small-molecule antioxidant proteome-shields in Deinococcus radiodurans. PLoS One 2010, 5, e12570. 20838443 PMC2933237
  37. [41]Lin SM; Baek CY; Jung JH; Kim WS; Song HY; Lee JH; Ji HJ; Zhi Y; Kang BS; Bahn YS; Seo HS; Lim S Antioxidant activities of an exopolysaccharide (deinopol) produced by the extreme radiation-resistant bacterium Deinococcus radiodurans. Sci. Rep 2020, 10, 55. 31919371 PMC6952347
  38. [42]Buzzini P Batch and fed-batch carotenoid production by Rhodotorula glutinis-Debaryomyces castellii co-cultures in corn syrup. J. Appl. Microbiol 2001, 90, 843– 847. 11348447
  39. [43]Buzzini P; Innocenti M; Turchetti B; Libkind D; van Broock M; Mulinacci N Carotenoid profiles of yeasts belonging to the genera Rhodotorula, Rhodosporidium, Sporobolomyces, and Sporidiobolus. Can. J. Microbiol 2007, 53, 1024– 1031. 17898860
  40. [44]Breierová E G. T; Marová I; Čertík M, Kogan G Enhanced antioxidant formula based on a selenium-supplemented carotenoid-producing yeast biomass. Chem. Biodivers 2008, 5, 440– 446. 18357552
  41. [45]Irazusta V; Nieto-Peñalver CG; Cabral ME; Amoroso MJ; de Figueroa LIC Relationship among carotenoid production, copper bioremediation and oxidative stress in Rhodotorula mucilaginosa RCL-11. Process Biochem. 2013, 48, 803– 809.
  42. [47]Zhang Y; Gu AZ; He M; Li D; Chen JM Subinhibitory concentrations of disinfectants promote the horizontal transfer of multidrug resistance genes within and across genera. Environ. Sci. Technol 2017, 51, 570– 580. 27997135
  43. [48]Lu J; Wang Y; Li J; Mao LK; Nguyen SH; Duarte T; Coin L; Bond P; Yuan ZG; Guo JH Triclosan at environmentally relevant concentrations promotes horizontal transfer of multidrug resistance genes within and across bacterial genera. Environ. Int 2018, 121, 1217– 1226. 30389380
  44. [49]Rodriguez RLM; Konstantinidis KT Nonpareil: a redundancy-based approach to assess the level of coverage in metagenomic datasets. Bioinformatics 2014, 30, 629– 635. 24123672
  45. [50]Bolger AM; Lohse M; Usadel B Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 2014, 30, 2114– 2120. 24695404 PMC4103590
  46. [51]Bankevich A; Nurk S; Antipov D; Gurevich AA; Dvorkin M; Kulikov AS; Lesin VM; Nikolenko SI; Pham S; Prjibelski AD; Pyshkin AV; Sirotkin AV; Vyahhi N; Tesler G; Alekseyev MA; Pevzner PA SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J. Comput. Biol 2012, 19, 455– 477. 22506599 PMC3342519
  47. [52]Kang DWD; Li F; Kirton E; Thomas A; Egan R; An H; Wang Z MetaBAT 2: an adaptive binning algorithm for robust and efficient genome reconstruction from metagenome assemblies. PeerJ 2019, 7, e7359. 31388474 PMC6662567
  48. [53]Parks DH; Imelfort M; Skennerton CT; Hugenholtz P; Tyson GW CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes. Genome Res. 2015, 25, 1043– 1055. 25977477 PMC4484387
  49. [54]Alcock BP; Raphenya AR; Lau TTY; Tsang KK; Bouchard M; Edalatmand A; Huynh W; Nguyen AV; Cheng AA; Liu S; Min SY; Miroshnichenko A; Tran HK; Werfalli RE; Nasir JA; Oloni M; Speicher DJ; Florescu A; Singh B; Faltyn M; Hernandez-Koutoucheva A; Sharma AN; Bordeleau E; Pawlowski AC; Zubyk HL; Dooley D; Griffiths E; Maguire F; Winsor GL; Beiko RG; Brinkman FSL; Hsiao WWL; Domselaar GV; McArthur AG CARD 2020: antibiotic resistome surveillance with the comprehensive antibiotic resistance database. Nucleic Acids Res. 2020, 48, D517– D525. 31665441 PMC7145624
  50. [55]Buchfink B; Xie C; Huson DH Fast and sensitive protein alignment using DIAMOND. Nat. Methods 2015, 12, 59– 60. 25402007
  51. [56]Ma LP; Xia Y; Li B; Yang Y; Li LG; Tiedje JM; Zhang T Metagenomic assembly reveals hosts of antibiotic resistance genes and the shared resistome in pig, chicken, and human feces. Environ. Sci. Technol 2016, 50, 420– 427. 26650334
  52. [57]Leplae R; Lima-Mendez G; Toussaint A ACLAME: A CLAssification of mobile genetic elements, update 2010. Nucleic Acids Res. 2010, 38, D57– D61. 19933762 PMC2808911
  53. [58]Bowers RM; Kyrpides NC; Stepanauskas R; Harmon-Smith M; Doud D; Reddy TBK; Schulz F; Jarett J; Rivers AR; Eloe-Fadrosh EA; Tringe SG; Ivanova NN; Copeland A; Clum A; Becraft ED; Malmstrom RR; Birren B; Podar M; Bork P; Weinstock GM; Garrity GM; Dodsworth JA; Yooseph S; Sutton G; Glöckner FO; Gilbert JA; Nelson WC; Hallam SJ; Jungbluth SP; Ettema TJG; Tighe S; Konstantinidis KT; Liu WT; Baker BJ; Rattei T; Eisen JA; Hedlund B; McMahon KD; Fierer N; Knight R; Finn R; Cochrane G; Karsch-Mizrachi I; Tyson GW; Rinke C; Consortium;, T. G. S.; Lapidus A; Meyer F; Yilmaz P; Parks DH; Eren AM; Schriml L; Banfield JF; Hugenholtz P; Woyke T Minimum information about a single amplified genome (MISAG) and a metagenome-assembled genome (MIMAG) of bacteria and archaea %J Nature Biotechnology. Nat. Biotechnol 2017, 35, 725– 731. 28787424 PMC6436528
  54. [59]Kümmerer K Antibiotics in the aquatic environment – a review – part II. Chemosphere 2009, 75, 435– 441. 19178931
  55. [60]Rodriguez-Mozaz S; Chamorro S; Marti E; Huerta B; Gros M; Sànchez-Melsió A; Borrego CM; Barceló D; Balcázar JL Occurrence of antibiotics and antibiotic resistance genes in hospital and urban wastewaters and their impact on the receiving river. Water Res. 2015, 69, 234– 242. 25482914
  56. [61]Aminov RI; Mackie RI J. F. M. L. Evolution and ecology of antibiotic resistance genes. 2010, 147– 161. 17490428
  57. [62]Kotzerke A; Sharma S; Schauss K; Heuer H; Thiele-Bruhn S; Smalla K; Wilke BM; Schloter M Alterations in soil microbial activity and N-transformation processes due to sulfadiazine loads in pig-manure. Environ. Pollut 2008, 153, 315– 322. 17905496
  58. [63]Thiele-Bruhn S; Beck IC Effects of sulfonamide and tetracycline antibiotics on soil microbial activity and microbial biomass. Chemosphere 2005, 59, 457– 465. 15788168
  59. [64]Kim S; Aga DS Potential ecological and human health impacts of antibiotics and antibiotic-resistant bacteria from wastewater treatment plants. J. Toxicol. Env. Heal. B. Crit. Rev 2007, 10, 559– 573. 18049923
  60. [65]Úbeda C; Maiques E; Knecht E; Lasa Í; Novick RP; Penadés JR Antibiotic-induced SOS response promotes horizontal dissemination of pathogenicity island-encoded virulence factors in staphylococci. Mol. Microbiol 2005, 56, 836– 844. 15819636
  61. [66]Zhu YG; Johnson TA; Su JQ; Qiao M; Guo GX; Stedtfeld RD; Hashsham SA; Tiedje JM Diverse and abundant antibiotic resistance genes in Chinese swine farms. Proc. Natl. Acad. Sci. U.S.A 2013, 110, 3435– 3440. 23401528 PMC3587239
  62. [67]Millan AS; MacLean RC Fitness costs of plasmids: a limit to plasmid transmission. Microbiol. Spectr 2017, 5, 1– 12. PMC11687550 28944751
  63. [68]Werisch M; Berger U; Berendonk TU Conjugative plasmids enable the maintenance of low cost non-transmissible plasmids. Plasmid 2017, 91, 96– 104. 28461122
  64. [69]Götz A; Pukall R; Smit E; Tietze E; Prager R; Tschäpe H; Elsas JDV; Smalla K Detection and characterization of broad-host-range plasmids in environmental bacteria by PCR. Appl. Environ. Microbiol 1996, 62, 2621– 2628. 8779598 PMC168041
  65. [70]Ren C; Wang YY; Tian LL; Chen M; Sun J; Li L Genetic bioaugmentation of activated sludge with dioxin-catabolic plasmids harbored by Rhodococcus sp. strain p52. Environ. Sci. Technol 2018, 52, 5339– 5348. 29608291
  66. [71]Knapp CW D. J; Ehlert PAI; Graham DW Evidence of Increasing Antibiotic Resistance Gene Abundances in Archived Soils since 1940. Environ. Sci. Technol 2010, 44, 580– 587. 20025282
  67. [72]Tello A; Telfer AJEHP Selective Pressure of Antibiotic Pollution on Bacteria of Importance to Public Health. Environ. Health Perspect 2012, 120, 1100– 1106. 22571927 PMC3440082
  68. [73]An XL; Su JQ; Li B; Ouyang WY; Zhao Y; Chen QL; Cui L; Chen H; Gillings MR; Zhang T; Zhu YG Tracking antibiotic resistome during wastewater treatment using high throughput quantitative PCR. Environ. Int 2018, 117, 146– 153. 29751164
  69. [74]Forsberg KJ; Patel S; Gibson MK; Lauber CL; Knight R; Fierer N; Dantas G Bacterial phylogeny structures soil resistomes across habitats. Nature 2014, 509, 612– 616. 24847883 PMC4079543
  70. [75]Guo B; Yu N; Weissbrodt DG; Liu Y Effects of micro-aeration on microbial niches and antimicrobial resistances in blackwater anaerobic digesters. Water Res. 2021, 196, 117035. 33751974
  71. [77]Smillie CS; Smith MB; Friedman J; Cordero OX; David LA; Alm EJ Ecology drives a global network of gene exchange connecting the human microbiome. Nature 2011, 480, 241– 244. 22037308
  72. [78]Wright GD Antibiotic resistance in the environment: a link to the clinic? Curr. Opin. Microbiol 2010, 13, 589– 594. 20850375
  73. [79]Blaustein RA; Seed PC; Hartmann EM; McMahon K Biotransformation of doxorubicin promotes resilience in simplified intestinal microbial communities. mSphere 2021, 6, e00068– 21. PMC8265622 34192503
  74. [80]Wang HL; Li P; Wang Y; Liu L; Yao JM Metagenomic insight into the bioaugmentation mechanism of Phanerochaete chrysosporium in an activated sludge system treating coking wastewater. J. Hazard. Mater 2017, 321, 820– 829. 27720470
  75. [81]Dejonghe W; Boon N; Seghers D; Top EM; Verstraete W Bioaugmentation of soils by increasing microbial richness: Missing links. Environ. Microbiol 2001, 3, 649– 657. 11722545
  76. [82]Andersson DI; Hughes D Microbiological effects of sublethal levels of antibiotics. Nat. Rev. Microbiol 2014, 12, 465– 478. 24861036

Authors
Ren, C.-Y., Wu, E.-L., Hartmann, E. M., & Zhao, H.-P.
Affiliations
  • MOE Key Lab of Environmental Remediation and Ecosystem Health, College of Environmental and Resource Science, Zhejiang University, Hangzhou 310058, China
  • Northwestern University (US)
  • Zhejiang University (CN)
Corresponding author
Zhao, He-Ping
Venue
Environmental Science & Technology
Published
2021-10-07
Volume
55
Issue
23
Pages
15831-15842
ISSN
  • 0013-936X (ISSN-L)
  • 1520-5851
OpenAlex
W3203249899
Cited by
73
References
4
Citations by year
2026: 19 · 2025: 18 · 2024: 14 · 2023: 12 · 2022: 10
FWCI
2.20
Type
journal article
Language
en
Open access
Locations
  • Environmental Science & Technology (publishedVersion)
  • PubMed (publishedVersion)
  • PubMed Central (acceptedVersion)
Funders
  • National Natural Science Foundation of China (21836003, 32061133002)
  • Key Laboratory of Urban Water Resource and Environment, Harbin Institute of Technology (QAK201903)
  • Zhejiang Province (2020C03011, 2021C03171)
Topics
  • Physical Sciences › Environmental Science › Pollution › Pharmaceutical and Antibiotic Environmental Impacts
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Medicine › Antibiotic Resistance in Bacteria
  • Physical Sciences › Environmental Science › Pollution › Wastewater Treatment and Nitrogen Removal
Keywords
antibiotic resistance genes, bioaugmentation, activated sludge, reactive oxygen species, horizontal gene transfer, conjugative transfer, RP4 plasmid, sul1, class 1 integron, resistome, Escherichia coli, antibiotic residues
MeSH terms
Anti-Bacterial Agents, Antioxidants, Drug Resistance, Microbial, Genes, Bacterial, Sewage

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review