| Citation: | LIN Yanhan, BAO Ruiqi, FU Jingyi, CHEN Leyi, CHEN Hong. Role of bacteriophages in spread of antibiotic resistance genes in wastewater treatment systems: a review[J]. ENVIRONMENTAL ENGINEERING , 2025, 43(9): 107-118. doi: 10.13205/j.hjgc.202509012 |
| [1] |
NAGHAVI M,VOLLSET S E,IKUTA K S,et al. Global burden of bacterial antimicrobial resistance in 2019:a systematic analysis[J]. The Lancet,2022,399:629-655.
|
| [2] |
WANG S,MA X,LIU Y,et al. Fate of antibiotics,antibiotic-resistant bacteria,and cell-free antibiotic-resistant genes in full-scale membrane bioreactor wastewater treatment plants[J]. Bioresource Technology,2020,302:122825.
|
| [3] |
FANG H,WANG H,CAI L,et al. Prevalence of antibiotic resistance genes and bacterial pathogens in long-term manured greenhouse soils as revealed by metagenomic survey[J]. Environmental Science & Technology,2015,49(2):1095-1104.
|
| [4] |
CELIA M. Assessing the risk of antibiotic resistance transmission from the environment to humans:non-direct proportionality between abundance and risk[J]. Trends in Microbiology,2017,25(3):173-181.
|
| [5] |
BARR J J,SLATER F R,FUKUSHIMA T,et al. Evidence for bacteriophage activity causing community and performance changes in a phosphorus-removal activated sludge[J]. FEMS Microbiology Ecology,2010,74(3):631-642.
|
| [6] |
SHAPIRO O H,KUSHMARO A. Bacteriophage ecology in environmental biotechnology processes[J]. Current Opinion in Biotechnology,2011,22(3):449-455.
|
| [7] |
FEINER R,ARGOV T,RABINOVICH L,et al. A new perspective on lysogeny:prophages as active regulatory switches of bacteria[J]. Nature Reviews Microbiology,2015,13(10):641-650.
|
| [8] |
RUAN C,RAMONEDA J,KAN A,et al. Phage predation accelerates the spread of plasmid-encoded antibiotic resistance[J]. Nature Communications,2024,15(1):1-12.
|
| [9] |
ARIA M,CUCCURULLO C. bibliometrix:an R-tool for comprehensive science mapping analysis[J]. Journal of Informetrics,2017,11(4):959-975.
|
| [10] |
SUTTLE C A. Viruses in the sea[J]. Nature,2005,437(7057):356-361.
|
| [11] |
LIAN K,LIU F,LI Y,et al. Environmental gradients shape microbiome assembly and stability in the East China sea[J]. Environmental Research,2023,238:1-14.
|
| [12] |
ADRIAENSSENS E M,KRAMER R,VAN GOETHEM M W,et al. Environmental drivers of viral community composition in Antarctic soils identified by viromics[J]. Microbiome,2017,5(1):1-14.
|
| [13] |
SHKOPOROV A N,CLOONEY A G,SUTTON T D S,et al. The human gut virome is highly diverse,stable,and individual specific[J]. Cell Host & Microbe,2019,26(4):527-541.
|
| [14] |
JIAN H,YI Y,WANG J,et al. Diversity and distribution of viruses inhabiting the deepest ocean on Earth[J]. The ISME Journal,2021,15(10):3094-3110.
|
| [15] |
ZHAO J,LI B,LV P,et al. Distribution of antibiotic resistance genes and their association with bacteria and viruses in decentralized sewage treatment facilities[J]. Frontiers of Environmental Science & Engineering,2022,16(3):1-14.
|
| [16] |
PETROVICH M L,ZILBERMAN A,KAPLAN A,et al. Microbial and viral communities and their antibiotic resistance genes throughout a hospital wastewater treatment system[J]. Frontiers in Microbiology,2020,11:1-13.
|
| [17] |
LIU W,XU C,LI T,et al. Temporal dynamics and contribution of phage community to the prevalence of antibiotic resistance genes in a full-scale sludge anaerobic digestion plant[J]. Environmental Science & Technology,2024,58(14):6296-6304.
|
| [18] |
HOWARD-VARONA C,HARGREAVES K R,ABEDON S T,et al. Lysogeny in nature:mechanisms,impact and ecology of temperate phages[J]. The ISME Journal,2017,11(7):1511-1520.
|
| [19] |
POPA O,LANDAN G,DAGAN T. Phylogenomic networks reveal limited phylogenetic range of lateral gene transfer by transduction[J]. The ISME Journal,2017,11(2):543-554.
|
| [20] |
TOUCHON M,MOURA De Sousa J A,ROCHA E P. Embracing the enemy:the diversification of microbial gene repertoires by phage-mediated horizontal gene transfer[J]. Current Opinion in Microbiology,2017,38:66-73.
|
| [21] |
CHIANG Y N,PENADÉS J R,CHEN J. Genetic transduction by phages and chromosomal islands:The new and noncanonical[J]. PLOS Pathogens,2019,15(8):1-7.
|
| [22] |
THOMPSON L R,ZENG Q,KELLY L,et al. Phage auxiliary metabolic genes and the redirection of cyanobacterial host carbon metabolism[J]. Proceedings of the National Academy of Sciences,2011,108(39):757-764.
|
| [23] |
SHI L D,DONG X,LIU Z,et al. A mixed blessing of viruses in wastewater treatment plants[J]. Water Research,2022,215:1-12.
|
| [24] |
YUAN L,JU F. Potential auxiliary metabolic capabilities and activities reveal biochemical impacts of viruses in municipal wastewater treatment plants[J]. Environmental Science & Technology,2023,57(13):5485-5498.
|
| [25] |
PIRSAHEB M,MOHAMADI M,MANSOURI A M,et al. Process modeling and optimization of biological removal of carbon,nitrogen and phosphorus from hospital wastewater in a continuous feeding & intermittent discharge(CFID)bioreactor[J]. Korean Journal of Chemical Engineering,2015,32(7):1340-1353.
|
| [26] |
SANDER M,SCHMIEGER H. Method for host-independent detection of generalized transducing bacteriophages in natural habitats[J]. Applied and Environmental Microbiology,2001,67(4):1490-1493.
|
| [27] |
MAGANHA DE ALMEIDA KUMLIEN A C,BORREGO C M,BALCÁZAR J L. Antimicrobial resistance and bacteriophages:an overlooked intersection in water disinfection[J]. Trends in Microbiology,2021,29(6):517-527.
|
| [28] |
BALCAZAR J L. Bacteriophages as vehicles for antibiotic resistance genes in the environment[J]. PLOS Pathogens,2014,10(7):1-4.
|
| [29] |
FILLOL-SALOM A,BACIGALUPE R,HUMPHREY S,et al. Lateral transduction is inherent to the life cycle of the archetypical Salmonella phage P22[J]. Nature Communications,2021,12(1):1-12.
|
| [30] |
KENZAKA T,TANI K,SAKOTANI A,et al. High-frequency phage-mediated gene transfer among escherichia coli cells,determined at the single-cell level[J]. Applied and Environmental Microbiology,2007,73(10):3291-3299.
|
| [31] |
CHEN J,QUILES-PUCHALT N,CHIANG Y N,et al. Genome hypermobility by lateral transduction[J]. Science,2018,362(6411):207-212.
|
| [32] |
ZHANG Y,GUO Y,QIU T,et al. Bacteriophages:Underestimated vehicles of antibiotic resistance genes in the soil[J]. Frontiers in Microbiology,2022,13:1-12.
|
| [33] |
LIN Z,ZHOU Z,SHUAI X,et al. Landscape of plasmids encoding β-lactamases in disinfection residual Enterobacteriaceae from wastewater treatment plants[J]. Water Research,2024,255:1-11.
|
| [34] |
ZHU L,YUAN L,SHUAI X Y,et al. Deciphering basic and key traits of antibiotic resistome in influent and effluent of hospital wastewater treatment systems[J]. Water Research,2023,231:1-11.
|
| [35] |
LEKUNBERRI I,VILLAGRASA M,BALCÁZAR J L,et al. Contribution of bacteriophage and plasmid DNA to the mobilization of antibiotic resistance genes in a river receiving treated wastewater discharges[J]. Science of The Total Environment,2017,601/602:206-209.
|
| [36] |
CALERO-CÁCERES W,MELGAREJO A,COLOMER-LLUCH M,et al. Sludge as a potential important source of antibiotic resistance genes in both the bacterial and bacteriophage fractions[J]. Environmental Science & Technology,2014,48(13):7602-7611.
|
| [37] |
YANG Y,SHI W,LU S Y,et al. Prevalence of antibiotic resistance genes in bacteriophage DNA fraction from Funan River water in Sichuan,China[J]. Science of The Total Environment,2018,626:835-841.
|
| [38] |
ROSS J,TOPP E. Abundance of antibiotic resistance genes in bacteriophage following soil fertilization with dairy manure or municipal biosolids,and evidence for potential transduction[J]. Applied and Environmental Microbiology,2015,81(22):7905-7913.
|
| [39] |
DEBROAS D,SIGURET C. Viruses as key reservoirs of antibiotic resistance genes in the environment[J]. The ISME Journal,2019,13(11):2856-2867.
|
| [40] |
BROWN-JAQUE M,CALERO-CÁCERES W,MUNIESA M. Transfer of antibiotic-resistance genes via phage-related mobile elements[J]. Plasmid,2015,79:1-7.
|
| [41] |
WANG J,CHU L,WOJNÁROVITS L,et al. Occurrence and fate of antibiotics,antibiotic resistant genes(ARGs)and antibiotic resistant bacteria(ARB)in municipal wastewater treatment plant:An overview[J]. Science of The Total Environment,2020,744:1-11.
|
| [42] |
SHUAI X,ZHOU Z,BA X,et al. Bacteriophages:vectors of or weapons against the transmission of antibiotic resistance genes in hospital wastewater systems?[J]. Water Research,2024,248:1-10.
|
| [43] |
LI X,CHEN T,REN Q,et al. Phages in sludge from the A/O wastewater treatment process play an important role in the transmission of ARGs[J]. Science of The Total Environment,2024,926:1-10.
|
| [44] |
CHEN T,MO C,YUAN Y,et al. Short-,long-read metagenome and virome reveal the profile of phage-mediated ARGs in anoxic-oxic processes for swine wastewater treatment[J]. Journal of Hazardous Materials,2024,468:1-10.
|
| [45] |
YANG Y,XING S,CHEN Y,et al. Profiles of bacteria/phage-comediated ARGs in pig farm wastewater treatment plants in China:Association with mobile genetic elements,bacterial communities and environmental factors[J]. Journal of Hazardous Materials,2021,404:1-11.
|
| [46] |
WANG M,XIONG W,LIU P,et al. Metagenomic insights into the contribution of phages to antibiotic resistance in water samples related to swine feedlot wastewater treatment[J]. Frontiers in Microbiology,2018,9:1-10.
|
| [47] |
KANG Y,WANG J,WANG Y,et al. Profiles of phage in global hospital wastewater:association with microbial hosts,antibiotic resistance genes,metal resistance genes,and mobile genetic elements[J]. Science of the Total Environment,2024,926:1-13.
|
| [48] |
LI Z,GUO X,LIU B,et al. Metagenome sequencing reveals shifts in phage-associated antibiotic resistance genes from influent to effluent in wastewater treatment plants[J]. Water Research,2024,253:121289.
|
| [49] |
PIRES J,SANTOS R,MONTEIRO S. Antibiotic resistance genes in bacteriophages from wastewater treatment plant and hospital wastewaters[J]. Science of The Total Environment,2023,892:1-8.
|
| [50] |
MAIQUES E,ÚBEDA C,CAMPOY S,et al. β-Lactam antibiotics induce the SOS response and horizontal transfer of virulence factors in Staphylococcus aureus[J]. Journal of Bacteriology,2006,188(7):2726-2729.
|
| [51] |
COMEAU A M,TÉTART F,TROJET S N,et al. Phage-antibiotic synergy(PAS):β-lactam and quinolone antibiotics stimulate virulent phage growth[J]. PLOS One,2007,2(8):799.
|
| [52] |
MODI S R,LEE H H,SPINA C S,et al. Antibiotic treatment expands the resistance reservoir and ecological network of the phage metagenome[J]. Nature,2013,499(7457):219-222.
|
| [53] |
JIANG S C,PAUL J H. Gene Transfer by Transduction in the marine environment[J]. Applied and Environmental Microbiology,1998,64(8):2780-2787.
|
| [54] |
VARGA M,PANTU ČEK R,RU ŽIČKOVÁ V,et al. Molecular characterization of a new efficiently transducing bacteriophage identified in meticillin-resistant Staphylococcus aureus[J]. The Journal of General Virology,2016,97(1):258-268.
|
| [55] |
GULINO K,RAHMAN J,BADRI M,et al. Initial mapping of the New York city wastewater virome[J]. mSystems,2020,5(3):1-18.
|
| [56] |
WU Q,LIU W T. Determination of virus abundance,diversity and distribution in a municipal wastewater treatment plant[J]. Water Research,2009,43(4):1101-1109.
|
| [57] |
RIZZO L,CELIA M,MERLIN C,et al. Urban wastewater treatment plants as hotspots for antibiotic resistant bacteria and genes spread into the environment:A review[J]. Science of the Total Environment,2013,447:345-360.
|
| [58] |
CALERO-CÁCERES W,MUNIESA M. Persistence of naturally occurring antibiotic resistance genes in the bacteria and bacteriophage fractions of wastewater[J]. Water Research,2016,95:11-18.
|
| [59] |
SUN R,YU P,ZUO P,et al. Bacterial concentrations and water turbulence influence the importance of conjugation versus phage-mediated antibiotic resistance gene transfer in suspended growth systems[J]. ACS Environmental Au,2022,2(2):156-165.
|
| [60] |
HUANG J,DAI X,WU Z,et al. Conjugative transfer of streptococcal prophages harboring antibiotic resistance and virulence genes[J]. The ISME Journal,2023,17(9):1467-1481.
|
| [61] |
VARGA M,PANTUČEK R,RUŽIČKOVÁ V,et al. Molecular characterization of a new efficiently transducing bacteriophage identified in meticillin-resistant Staphylococcus aureus[J]. Journal of General Virology,2016,97(1):258-268.
|
| [62] |
DŽUNKOVÁ M,LOW S J,DALY J N,et al. Defining the human gut host–phage network through single-cell viral tagging[J]. Nature Microbiology,2019,4(12):2192-2203.
|
| [63] |
ENAULT F,BRIET A,BOUTEILLE L,et al. Phages rarely encode antibiotic resistance genes:a cautionary tale for virome analyses[J]. The ISME Journal,2017,11(1):237-247.
|
| [64] |
BILLAUD M,LAMY-BESNIER Q,LOSSOUARN J,et al. Analysis of viromes and microbiomes from pig fecal samples reveals that phages and prophages rarely carry antibiotic resistance genes[J]. ISME Communications,2021,1(1):1-10.
|
| [65] |
WANG Q,WANG M,YANG Q,et al. The role of bacteriophages in facilitating the horizontal transfer of antibiotic resistance genes in municipal wastewater treatment plants[J]. Water Research,2025,268:1-12.
|
| [66] |
LUO X Q,WANG P,LI J L,et al. Viral community-wide auxiliary metabolic genes differ by lifestyles,habitats,and hosts[J]. Microbiome,2022,10(1):1-18.
|
| [67] |
CHEN Y,WANG Y,PAEZ-ESPINO D,et al. Prokaryotic viruses impact functional microorganisms in nutrient removal and carbon cycle in wastewater treatment plants[J]. Nature Communications,2021,12(1):1-11.
|
| [68] |
REISOGLU Ş,AYDIN S. Bacteriophages as a promising approach for the biocontrol of antibiotic resistant pathogens and the reconstruction of microbial interaction networks in wastewater treatment systems:a review[J]. Science of the Total Environment,2023,890(164291):1-7.
|
| [69] |
JI M,LIU Z,SUN K,et al. Bacteriophages in water pollution control:advantages and limitations[J]. Frontiers of Environmental Science & Engineering,2021,15(5):1-15.
|
| [70] |
YU P,MATHIEU J,LU G W,et al. Control of antibiotic-resistant bacteria in activated sludge using polyvalent phages in conjunction with a production host[J]. Environmental Science & Technology Letters,2017,4(4):137-142.
|
| [71] |
GRAMI E,SALHI N,SEALEY K S,et al. Siphoviridae bacteriophage treatment to reduce abundance and antibiotic resistance of Pseudomonas aeruginosa in wastewater[J]. International Journal of Environmental Science and Technology,2022,19(4):3145-3154.
|
| [72] |
MELO L D R,OLIVEIRA H,PIRES D P,et al. Phage therapy efficacy:a review of the last 10 years of preclinical studies[J]. Critical Reviews in Microbiology,2020:78-99.
|
| [73] |
KEEN E C,BLISKOVSKY V V,MALAGON F,et al. Novel“superspreader” bacteriophages promote horizontal gene transfer by transformation[J]. mBio,2017,8(1):1-12.
|
| [74] |
ABE K,NOMURA N,SUZUKI S. Biofilms:hot spots of horizontal gene transfer(HGT)in aquatic environments,with a focus on a new HGT mechanism[J]. FEMS Microbiology Ecology,2020,96(5):1-12.
|
| [75] |
WANG Y Q,LI W,ZHUANG J long,et al. Bacteriophage-mediated extracellular DNA release is important for the structural stability of aerobic granular sludge[J]. Science of the Total Environment,2020,726:1-11.
|
| [76] |
SUTTLE C A. Marine viruses-major players in the global ecosystem[J]. Nature Reviews Microbiology,2007,5(10):801-812.
|
| [77] |
WINTER M,BUCKLING A,HARMS K,et al. Antimicrobial resistance acquisition via natural transformation:context is everything[J]. Current Opinion in Microbiology,2021,64:133-138.
|
| [78] |
BONIFÁCIO M,MATEUS C,ALVES A R,et al. Natural transformation as a mechanism of horizontal gene transfer in Aliarcobacter butzleri[J]. Pathogens,2021,10(7):1-15.
|