First practice on bacteriophage-mediated disinfection of tailwater: targeted removal of multidrug-resistant Vibrio parahaemolyticus and associated antibiotic resistance genes

Yanxi Liu , Jian Lu , Jun Wu , Jianhua Wang , Brian J. Boman

ENG. Environ. ›› 2026, Vol. 20 ›› Issue (12) : 179

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ENG. Environ. ›› 2026, Vol. 20 ›› Issue (12) :179 DOI: 10.1007/s11783-026-2279-5
RESEARCH ARTICLE
First practice on bacteriophage-mediated disinfection of tailwater: targeted removal of multidrug-resistant Vibrio parahaemolyticus and associated antibiotic resistance genes
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Abstract

Multidrug-resistant (MDR) pathogens and associated antibiotic resistance genes (ARGs) in tailwater pose a threat to public health and food safety. Bacteriophages have emerged as promising biocontrol agents for MDR pathogens, yet their efficacy in disinfecting tailwater for the elimination of MDR pathogens and ARGs remains unexplored. We developed a bacteriophage-mediated disinfection technique for targeted removal of MDR Vibrio parahaemolyticus and ARGs from aquaculture tailwater. A novel lytic Caudoviricetes phage VBY against MDR V. parahaemolyticus was isolated from aquaculture, while its disinfection performance in aquaculture tailwater outperformed ozone (O3) and ultraviolet (UV) controls. Genomic and phylogenetic analyses identified VBY as a Caudoviricetes, lacking virulence factors and ARGs. The phage VBY exhibited robust stability under aquaculture-relevant environmental conditions and potential activity against biofilms, accompanied by significant ARGs reduction. In the real tailwater treatment system, the phage VBY achieved 5.5-log reduction in MDR bacterial loads and 4–6 log suppression of key ARGs over 72 h. Phage treatment maintained a remarkably long-term inhibitory effect. The phage VBY could preserve water quality during the removal of MDR V. parahaemolyticus, which overcame the key limitation of conventional chemical disinfection strategies. These findings demonstrated that phage-mediated disinfection, which could effectively remove MDR pathogens and the associated ARGs from recycled tailwater, was an environmentally sustainable water treatment technique.

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Keywords

Tailwater / Water disinfection / Bacteriophage / Multidrug resistance / Targeted removal

Highlight

● Tailwater disinfection for targeting removal of MDR Vibrio and ARGs using phage was developed.

● A novel lytic Caudoviricetes phage VBY against MDR Vibrio parahaemolyticus was isolated.

● The disinfection performance of phage VBY outperformed O3 and UV controls.

● Phage VBY exhibited robust stability under aquaculture-relevant environmental conditions.

● The findings proved the advantage on recycled tailwater disinfection using phage.

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Yanxi Liu, Jian Lu, Jun Wu, Jianhua Wang, Brian J. Boman. First practice on bacteriophage-mediated disinfection of tailwater: targeted removal of multidrug-resistant Vibrio parahaemolyticus and associated antibiotic resistance genes. ENG. Environ., 2026, 20 (12) : 179 DOI:10.1007/s11783-026-2279-5

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References

[1]

Ahmed H A , El Bayomi R M , Hussein M A , Khedr M H E , Abo Remela E M , El-Ashram A M M . (2018). Molecular characterization, antibiotic resistance pattern and biofilm formation of Vibrio parahaemolyticus and V. cholerae isolated from crustaceans and humans. International Journal of Food Microbiology, 274: 31–37

[2]

Algammal A M , Alghamdi S , Almessiry B K , Kabrah A , Sindi A S , Alshahrani M Y , Al-Olayan E , Youssef F M , Abdelsamea S S , Dayrit G B . et al. (2025). In-depth characterization of virulence traits, pathogenicity, antibiogram, and antibiotic resistance genes of MDR Vibrio parahaemolyticus retrieved from shrimp. Scientific Reports, 15(1): 34285

[3]

Azzam M I , Nasr-Eldin M A , Mohammed F A , Omran K A . (2025). Whole genome sequencing of the novel polyvalent bacteriophage Malk1: a powerful biocontrol agent for water pollution. Water Research, 276: 123259

[4]

Bankevich A , Nurk S , Antipov D , Gurevich A A , Dvorkin M , Kulikov A S , Lesin V M , Nikolenko S I , Pham S , Prjibelski A D . et al. (2012). SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. Journal of Computational Biology, 19(5): 455–477

[5]

Brettin T , Davis J J , Disz T , Edwards R A , Gerdes S , Olsen G J , Olson R , Overbeek R , Parrello B , Pusch G D . et al. (2015). RASTtk: a modular and extensible implementation of the RAST algorithm for building custom annotation pipelines and annotating batches of genomes. Scientific Reports, 5: 8365

[6]

Changsen C , Likhitrattanapisal S , Lunha K , Chumpol W , Jiemsup S , Prachumwat A , Kongkasuriyachai D , Ingsriswang S , Chaturongakul S , Lamalee A . et al. (2023). Incidence, genetic diversity, and antimicrobial resistance profiles of Vibrio parahaemolyticus in seafood in Bangkok and eastern Thailand. PeerJ, 11: e15283

[7]

Choi Y , He H , Dodd M C , Lee Y . (2021). Degradation kinetics of antibiotic resistance gene mecA of methicillin-resistant Staphylococcus aureus (MRSA) during water disinfection with chlorine, ozone, and ultraviolet light. Environmental Science & Technology, 55(4): 2541–2552

[8]

Hatfull G F , Dedrick R M , Schooley R T . (2022). Phage therapy for antibiotic-resistant bacterial infections. Annual Review of Medicine, 73: 197–211

[9]

Høiby N , Bjarnsholt T , Givskov M , Molin S , Ciofu O . (2010). Antibiotic resistance of bacterial biofilms. International Journal of Antimicrobial Agents, 35(4): 322–332

[10]

Huang Q J , Butaye P , Ng P H , Zhang J , Cai W L , St-Hilaire S . (2024). Impact of low-dose ozone nanobubble treatments on antimicrobial resistance genes in pond water. Frontiers in Microbiology, 15: 1393266

[11]

Islam M , Mahbub N U , Shin W S , Oh M H . (2024). Phage-encoded depolymerases as a strategy for combating multidrug-resistant Acinetobacter baumannii. Frontiers in Cellular and Infection Microbiology, 14: 1462620

[12]

Jończyk-Matysiak E , Łodej N , Kula D , Owczarek B , Orwat F , Międzybrodzki R , Neuberg J , Bagińska N , Weber-Dąbrowska B , Górski A . (2019). Factors determining phage stability/activity: challenges in practical phage application. Expert Review of Anti-Infective Therapy, 17(8): 583–606

[13]

Kar P , Das T K , Ghosh S , Pradhan S , Chakrabarti S , Mondal K C , Ghosh K . (2022). Characterization of a Vibrio-infecting bacteriophage, VPMCC5, and proposal of its incorporation as a new genus in the Zobellviridae family. Virus Research, 321: 198904

[14]

Kuziel G A , Rakoff-Nahoum S . (2022). The gut microbiome. Current Biology, 32(6): R257–R264

[15]

Letchumanan V , Chan K G , Lee L H . (2014). Vibrio parahaemolyticus: a review on the pathogenesis, prevalence, and advance molecular identification techniques. Frontiers in Microbiology, 5: 705

[16]

Li L Y , Zhao Y , Han G L , Guo J R , Meng Z , Chen M . (2020). Progress in the study and use of seawater vegetables. Journal of Agricultural and Food Chemistry, 68(22): 5998–6006

[17]

Li L Z , Meng H M , Gu D , Li Y , Jia M D . (2019). Molecular mechanisms of Vibrio parahaemolyticus pathogenesis. Microbiological Research, 222: 43–51

[18]

Liu C , Olivares C I , Pinto A J , Lauderdale C V , Brown J , Selbes M , Karanfil T . (2017). The control of disinfection byproducts and their precursors in biologically active filtration processes. Water Research, 124: 630–653

[19]

Liu W T , Hao L L , Xia H , Wang H J , Hou W F , Wang H X , Zhou M . (2023). Inhibitory effect of two closely related phages on Vibrio parahaemolyticus. Foodborne Pathogens and Disease, 20(4): 149–157

[20]

Liu Y X , Liu M J , Hu R , Bai J , He X Q , Jin Y . (2021). Isolation of the novel phage PHB09 and Its potential use against the plant pathogen Pseudomonas syringae pv. actinidiae. Viruses, 13(11): 2275

[21]

Lomeli-Ortega C O , Sun M M , Balcázar J L. . (2024). Unraveling the interaction between soil microbiomes and their potential for restoring polluted soils. Frontiers of Environmental Science & Engineering, 18(8): 104

[22]

Lopatek M , Wieczorek K , Osek J . (2018). Antimicrobial resistance, virulence factors, and genetic profiles of Vibrio parahaemolyticus from seafood. Applied and Environmental Microbiology, 84(16): e00537–18

[23]

Lu J , Wu J , Wang J H , Boman B J . (2026). Competitive exclusion between antibiotic resistance genes and nitrogen functional genes in long-term recirculating aquaculture system based on metagenomic perspective. Journal of Environmental Chemical Engineering, 14(3): 122918

[24]

Lu J , Wu J , Zhang C , Wang J H , He X . (2024). Occurrence and possible sources of antibiotic resistance genes in seawater of the South China Sea. Frontiers of Environmental Science & Engineering, 18(9): 108

[25]

Mathieu J , Yu P F , Zuo P X , Da Silva M L B , Alvarez P J J . (2019). Going viral: emerging opportunities for phage-based bacterial control in water treatment and reuse. Accounts of Chemical Research, 52(4): 849–857

[26]

Mitsuwan W , Boripun R , Saengsawang P , Intongead S , Boonplu S , Chanpakdee R , Morita Y , Boonmar S , Rojanakun N , Suksriroj N . et al. (2025). Multidrug resistance, biofilm-forming ability, and molecular characterization of Vibrio species isolated from foods in Thailand. Antibiotics, 14(3): 235

[27]

Mok J S , Cho S R , Park Y J , Jo M R , Ha K S , Kim P H , Kim M J . (2021). Distribution and antimicrobial resistance of Vibrio parahaemolyticus isolated from fish and shrimp aquaculture farms along the Korean coast. Marine Pollution Bulletin, 171: 112785

[28]

Molina-Quiroz R C , Silva-Valenzuela C A . (2023). Interactions of Vibrio phages and their hosts in aquatic environments. Current Opinion in Microbiology, 74: 102308

[29]

Moryl M, Różalski A, de Figueiredo J A P, Palatyńska-Ulatowska A (2023). How do phages disrupt the structure of Enterococcus faecalis biofilm? International Journal of Molecular Sciences, 24(24): 17260

[30]

Olawade D B , Fapohunda O , Egbon E , Ebiesuwa O A , Usman S O , Faronbi A O , Fidelis S C . (2024). Phage therapy: a targeted approach to overcoming antibiotic resistance. Microbial Pathogenesis, 197: 107088

[31]

Ren Y , Wang L L , Chen R J , Li X Y , Li S Y , Li J B , Li Q , Wang Z H , Xu Y P . (2022). Isolation and characterization of a novel phage vB_ValP_VA-RY-3 infecting Vibrio alginolyticus. Virus Research, 322: 198945

[32]

Samir S . (2021). Bacteriophages as therapeutic agents: alternatives to antibiotics. Recent Patents on Biotechnology, 15(1): 25–33

[33]

Seemann T . (2014). Prokka: rapid prokaryotic genome annotation. Bioinformatics, 30(14): 2068–2069

[34]

Singh S , Samson R , Hassard F . (2025). Phage therapy for environmental biotechnology applications. Frontiers in Microbiology, 16: 1621103

[35]

Tiwari A , Gomez-Alvarez V , Siponen S , Sarekoski A , Hokajärvi A M , Kauppinen A , Torvinen E , Miettinen I T , Pitkänen T . (2022). Bacterial genes encoding resistance against antibiotics and metals in well-maintained drinking water distribution systems in Finland. Frontiers in Microbiology, 12: 803094

[36]

Wang D , Fletcher G C , On S L W , Palmer J S , Gagic D , Flint S H . (2023a). Biofilm formation, sodium hypochlorite susceptibility and genetic diversity of Vibrio parahaemolyticus. International Journal of Food Microbiology, 385: 110011

[37]

Wang J H , Lu J , Wu J , Zhang C , Feng Y X , Boman B J . (2026). Fate and attenuation of antibiotic resistance genes in a constructed seawater wetland used for aquaculture tailwater treatment. Engineering Environment, 20(3): 47

[38]

Wang L , Zhou J C , Li Z H , Zhang X , Leung K M Y , Yuan L , Sheng G P . (2023b). Facet-specific photocatalytic degradation of extracellular antibiotic resistance genes by hematite nanoparticles in aquatic environments. Environmental Science & Technology, 57(51): 21835–21845

[39]

Wang N , Lu J , Wu J , Zhang C , Wang J H , Agathos S N , Feng Y X . (2025). A novel Oocystis algal strain enables highly efficient simultaneous biodegradation of bisphenol A and carbon capture in seawater. Frontiers of Environmental Science & Engineering, 19(10): 131

[40]

Wei Q , Yang Z W , Wang G C , Yang D , Li H B , Zhou S Q , Chen T J , Zhao Y , Li J W , Shi D Y . et al. (2026). Degradation of extracellular antibiotic resistance genes in water and their degradation prediction using a multivariate nonlinear fitting model. Journal of Hazardous Materials, 507: 141791

[41]

Wick R R , Schultz M B , Zobel J , Holt K E . (2015). Bandage: interactive visualization of de novo genome assemblies. Bioinformatics, 31(20): 3350–3352

[42]

Wu J , Lu J , Wang J H , Boman B J . (2026). Metagenomic-based observations regarding the inhibition effect of viruses on resistance genes in aquaculture system. Engineering Environment, 20(6): 88

[43]

Xu C J , Su G G , Zhao K S , Wang H , Xu X Q , Li Z Q , Hu Q , Xu J . (2023). Assessment of greenhouse gases emissions and intensity from Chinese marine aquaculture in the past three decades. Journal of Environmental Management, 329: 117025

[44]

Xu Q , Hu X F , Wang Y B . (2021). Alternatives to conventional antibiotic therapy: potential therapeutic strategies of combating antimicrobial-resistance and biofilm-related infections. Molecular Biotechnology, 63(12): 1103–1124

[45]

Zang B , Zhou H , Nan H K , Li Y , Li Q , Sano D , Chen R . (2025). Exploring the potential positive impact of phage-bacterium interactions on membrane fouling mitigation. Frontiers of Environmental Science & Engineering, 19(10): 139

[46]

Zhang Y X , Lu J , Wu J , Wang J H , Luo Y M . (2020). Potential risks of microplastics combined with superbugs: enrichment of antibiotic resistant bacteria on the surface of microplastics in mariculture system. Ecotoxicology and Environmental Safety, 187: 109852

[47]

Zhou H B , Liu X M , Hu W Y , Yang J , Jiang H , Sun X J , Bie X M , Lu Z X , Xue F , Zeng D X . et al. (2022). Prevalence, antimicrobial resistance and genetic characterization of Vibrio para-haemolyticus isolated from retail aquatic products in Nanjing, China. Food Research International, 162: 112026

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