Bacteriophages in water pollution control: Advantages and limitations
Mengzhi Ji, Zichen Liu, Kaili Sun, Zhongfang Li, Xiangyu Fan, Qiang Li
Bacteriophages in water pollution control: Advantages and limitations
•Phages can be better indicators of enteric viruses than fecal indicator bacteria.
•Multiple phages should be added to the microbial source tracking toolbox.
•Engineered phage or phage cocktail can effectively target resistant bacteria.
•In phage use, phage-mediated horizontal gene transfer cannot be ignored.
•More schemes are needed to prevent phage concentration from decreasing.
Wastewater is a breeding ground for many pathogens, which may pose a threat to human health through various water transmission pathways. Therefore, a simple and effective method is urgently required to monitor and treat wastewater. As bacterial viruses, bacteriophages (phages) are the most widely distributed and abundant organisms in the biosphere. Owing to their capacity to specifically infect bacterial hosts, they have recently been used as novel tools in water pollution control. The purpose of this review is to summarize and evaluate the roles of phages in monitoring pathogens, tracking pollution sources, treating pathogenic bacteria, infecting bloom-forming cyanobacteria, and controlling bulking sludge and biofilm pollution in wastewater treatment systems. We also discuss the limitations of phage usage in water pollution control, including phage-mediated horizontal gene transfer, the evolution of bacterial resistance, and phage concentration decrease. This review provides an integrated outlook on the use of phages in water pollution control.
Phage / Water pollution monitoring / Harmful bacteria biocontrol / Horizontal gene transfer / Bacterial resistance
[1] |
Ahmed W, Lobos A, Senkbeil J, Peraud J, Gallard J, Harwood V J (2018). Evaluation of the novel crAssphage marker for sewage pollution tracking in storm drain outfalls in Tampa, Florida. Water Research, 131: 142–150
CrossRef
Google scholar
|
[2] |
Amarasiri M, Kitajima M, Nguyen T H, Okabe S, Sano D (2017). Bacteriophage removal efficiency as a validation and operational monitoring tool for virus reduction in wastewater reclamation. Water Research, 121: 258–269
CrossRef
Google scholar
|
[3] |
Aracic S, Manna S, Petrovski S, Wiltshire J L, Mann G, Franks A E (2015). Innovative biological approaches for monitoring and improving water quality. Frontiers in Microbiology, 6: 826
CrossRef
Google scholar
|
[4] |
Ayyaru S, Choi J, Ahn Y H (2018). Biofouling reduction in a MBR by the application of a lytic phage on a modified nanocomposite membrane. Environmental Science. Water Research & Technology, 4(10): 1624–1638
CrossRef
Google scholar
|
[5] |
Bányai K, Estes M K, Martella V, Parashar U D (2018). Viral gastroenteritis. Lancet, 392(10142): 175–186
CrossRef
Google scholar
|
[6] |
Batinovic S, Wassef F, Knowler S A, Rice D T, Stanton C R, Rose J, Tucci J, Nittami T, Vinh A, Drummond G R, Sobey C G, Chan H T, Seviour R J, Petrovski S, Franks A E (2019). Bacteriophages in Natural and Artificial Environments. Pathogens (Basel, Switzerland), 8(3): 100
CrossRef
Google scholar
|
[7] |
Bhattacharjee A S, Choi J, Motlagh A M, Mukherji S T, Goel R (2015). Bacteriophage therapy for membrane biofouling in membrane bioreactors and antibiotic‐resistant bacterial biofilms. Biotechnology and Bioengineering, 112(8): 1644–1654
CrossRef
Google scholar
|
[8] |
Bivins A, Crank K, Greaves J, North D, Wu Z, Bibby K (2020). Cross-assembly phage and pepper mild mottle virus as viral water quality monitoring tools–potential, research gaps, and way forward. Current Opinion in Environmental Science & Health, 16: 54-61
CrossRef
Google scholar
|
[9] |
Brown-Jaque M, Calero-Cáceres W, Espinal P, Rodríguez-Navarro J, Miró E, González-López J J, Cornejo T, Hurtado J C,Navarro F, Muniesa M (2018). Antibiotic resistance genes in phage particles isolated from human faeces and induced from clinical bacterial isolates. International Journal of Antimicrobial Agents, 51(3): 434–442
CrossRef
Google scholar
|
[10] |
Calero-Cáceres W, Méndez J, Martín-Díaz J, Muniesa M (2017). The occurrence of antibiotic resistance genes in a Mediterranean river and their persistence in the riverbed sediment. Environmental Pollution, 223: 384–394
CrossRef
Google scholar
|
[11] |
Calero-Cáceres W, Muniesa M (2016). Persistence of naturally occurring antibiotic resistance genes in the bacteria and bacteriophage fractions of wastewater. Water Research, 95: 11–18
CrossRef
Google scholar
|
[12] |
Calero-Cáceres W, Ye M, Balcázar J L (2019). Bacteriophages as environmental reservoirs of antibiotic resistance. Trends in microbiology, 27(7): 570–577
CrossRef
Google scholar
|
[13] |
Chaudhry W N, Haq I U, Andleeb S, Qadri I (2014). Characterization of a virulent bacteriophage LK1 specific for Citrobacter freundii isolated from sewage water. Journal of Basic Microbiology, 54(6): 531–541
CrossRef
Google scholar
|
[14] |
Chen J, Carpena N, Quiles-Puchalt N, Ram G, Novick R P, Penadés J R (2015). Intra-and inter-generic transfer of pathogenicity island-encoded virulence genes by cos phages. ISME Journal, 9(5): 1260–1263
CrossRef
Google scholar
|
[15] |
Cheng X, Delanka-Pedige H M, Munasinghe-Arachchige S P, Abeysiriwardana-Arachchige I S, Smith G B, Nirmalakhandan N, Zhang Y (2020). Removal of antibiotic resistance genes in an algal-based wastewater treatment system employing Galdieria sulphuraria: A comparative study. Science of the Total Environment, 711: 134435
CrossRef
Google scholar
|
[16] |
Chyerochana N, Kongprajug A, Somnark P, Leelapanang Kamphaengthong P, Mongkolsuk S, Sirikanchana K (2020). Distributions of enterococci and human-specific bacteriophages of enterococci in a tropical watershed. International Journal of Hygiene and Environmental Health, 226: 113482
CrossRef
Google scholar
|
[17] |
Cinek O, Mazankova K, Kramna L, Odeh R, Alassaf A, Ibekwe M U, Ahmadov G, Mekki H, Abdullah M A, Elmahi B M, Hyöty H, Rainetova P (2018). Quantitative CrAssphage real-time PCR assay derived from data of multiple geographically distant populations. Journal of Medical Virology, 90(4): 767–771
CrossRef
Google scholar
|
[18] |
Crank K, Li X, North D, Ferraro G B, Iaconelli M, Mancini P, La Rosa G, Bibby K (2020). CrAssphage abundance and correlation with molecular viral markers in Italian wastewater. Water Research, 184: 116161
CrossRef
Google scholar
|
[19] |
de Brauwere A, Ouattara N K, Servais P (2014). Modeling fecal indicator bacteria concentrations in natural surface waters: A review. Critical Reviews in Environmental Science and Technology, 44(21): 2380–2453
CrossRef
Google scholar
|
[20] |
Deng Y, Li B, Zhang T (2018). Bacteria that make a meal of sulfonamide antibiotics: Blind spots and emerging opportunities. Environmental Science & Technology, 52(7): 3854–3868
CrossRef
Google scholar
|
[21] |
Dias E, Ebdon J, Taylor H (2018). The application of bacteriophages as novel indicators of viral pathogens in wastewater treatment systems. Water Research, 129: 172–179
CrossRef
Google scholar
|
[22] |
Diston D, Sinreich M, Zimmermann S, Baumgartner A, Felleisen R (2015). Evaluation of molecular-and culture-dependent MST markers to detect fecal contamination and indicate viral presence in good quality groundwater. Environmental Science & Technology, 49(12): 7142–7151
CrossRef
Google scholar
|
[23] |
Diston D, Wicki M (2015). Occurrence of bacteriophages infecting Bacteroides host strains (ARABA 84 and GB-124) in fecal samples of human and animal origin. Journal of Water and Health, 13(3): 654–661
CrossRef
Google scholar
|
[24] |
Doss J, Culbertson K, Hahn D, Camacho J, Barekzi N (2017). A review of phage therapy against bacterial pathogens of aquatic and terrestrial organisms. Viruses, 9(3): 50
CrossRef
Google scholar
|
[25] |
Dow P, Kotz K, Gruszka S, Holder J, Fiering J (2018). Acoustic separation in plastic microfluidics for rapid detection of bacteria in blood using engineered bacteriophage. Lab on a Chip, 18(6): 923–932
CrossRef
Google scholar
|
[26] |
Dutilh B E, Cassman N, Mcnair K, Sanchez S E, Silva G G, Boling L, Barr J J, Speth D R, Seguritan V, Aziz R K, Felts B, Dinsdale E A, Mokili J L, Edwards R A (2014). A highly abundant bacteriophage discovered in the unknown sequences of human faecal metagenomes. Nature Communications, 5(1): 4498
CrossRef
Google scholar
|
[27] |
Edwards R A, Vega A A, Norman H M, Ohaeri M, Levi K, Dinsdale E A, Cinek O, Aziz R K, Mcnair K, Barr J J, Bibby K, Brouns S J J, Cazares A, de Jonge P A, Desnues C, Díaz Muñoz S L, Fineran P C, Kurilshikov A, Lavigne R, Mazankova K, McCarthy D T, Nobrega F L, Reyes Muñoz A, Tapia G, Trefault N, Tyakht A V, Vinuesa P, Wagemans J, Zhernakova A, Aarestrup F M, Ahmadov G, Alassaf A, Anton J, Asangba A, Billings E K, Cantu V A, Carlton J M, Cazares D, Cho G S, Condeff T, Cortés P, Cranfield M, Cuevas D A, De la Iglesia R, Decewicz P, Doane M P, Dominy N J, Dziewit L, Elwasila B M, Eren A M, Franz C, Fu J, Garcia-Aljaro C, Ghedin E, Gulino K M, Haggerty J M, Head S R, Hendriksen R S, Hill C, Hyöty H, Ilina E N, Irwin M T, Jeffries T C, Jofre J, Junge R E, Kelley S T, Khan Mirzaei M, Kowalewski M, Kumaresan D, Leigh S R, Lipson D, Lisitsyna E S, Llagostera M, Maritz J M, Marr L C, McCann A, Molshanski-Mor S, Monteiro S, Moreira-Grez B, Morris M, Mugisha L, Muniesa M, Neve H, Nguyen N, Nigro O D, Nilsson A S, O’Connell T, Odeh R, Oliver A, Piuri M, Prussin A J II, Qimron U, Quan Z X, Rainetova P, Ramírez-Rojas A, Raya R, Reasor K, Rice G A O, Rossi A, Santos R, Shimashita J, Stachler E N, Stene L C, Strain R, Stumpf R, Torres P J, Twaddle A, Ugochi Ibekwe M A, Villagra N, Wandro S, White B, Whiteley A, Whiteson K L, Wijmenga C, Zambrano M M, Zschach H, Dutilh B E (2019). Global phylogeography and ancient evolution of the widespread human gut virus crAssphage. Nature Microbiology, 4(10): 1727–1736
CrossRef
Google scholar
|
[28] |
Ertürk G, Lood R (2018). Bacteriophages as biorecognition elements in capacitive biosensors: Phage and host bacteria detection. Sensors and Actuators. B, Chemical, 258: 535–543
CrossRef
Google scholar
|
[29] |
Farkas K, Walker D I, Adriaenssens E M, Mcdonald J E, Hillary L S, Malham S K, Jones D L (2020). Viral indicators for tracking domestic wastewater contamination in the aquatic environment. Water Research, 181: 115926
CrossRef
Google scholar
|
[30] |
Gabiatti N, Yu P, Mathieu J, Lu G W, Wang X, Zhang H, Soares H M, Alvarez P J (2018). Bacterial endospores as phage genome carriers and protective shells. Applied and Environmental Microbiology, 84(18): e01186-18
CrossRef
Google scholar
|
[31] |
Gao E B, Gui J F, Zhang Q Y (2012). A novel cyanophage with a cyanobacterial nonbleaching protein A gene in the genome. Journal of Virology, 86(1): 236–245
CrossRef
Google scholar
|
[32] |
García‐Aljaro C, Ballesté EMuniesa M, Jofre J (2017). Determination of crAssphage in water samples and applicability for tracking human faecal pollution. Microbial Biotechnology, 10(6): 1775–1780 doi:10.1111/1751-7915.12841
|
[33] |
Gu J, Han B, Wang J (2020). COVID-19: gastrointestinal manifestations and potential fecal-oral transmission. Gastroenterology, 158(6): 1518–1519
CrossRef
Google scholar
|
[34] |
Guzmán C, Mocé-Llivina L, Lucena F, Jofre J (2008). Evaluation of Escherichia coli host strain CB390 for simultaneous detection of somatic and F-specific coliphages. Applied and Environmental Microbiology, 74(2): 531–534
CrossRef
Google scholar
|
[35] |
Hagedorn C, Blanch A R, Harwood V J (2011). Microbial Source Tracking: Methods, Applications, and Case Studies. Dordrecht: Springer Science & Business Media
|
[36] |
Hampton H G, Watson B N, Fineran P C (2020). The arms race between bacteria and their phage foes. Nature, 577(7790): 327–336
CrossRef
Google scholar
|
[37] |
Hamza I A, Bibby K (2019). Critical issues in application of molecular methods to environmental virology. Journal of Virological Methods, 266: 11–24
CrossRef
Google scholar
|
[38] |
Haramoto E, Fujino S, Otagiri M (2015). Distinct behaviors of infectious F-specific RNA coliphage genogroups at a wastewater treatment plant. Science of the Total Environment, 520: 32–38
CrossRef
Google scholar
|
[39] |
Hodgson K R, Torok V A, Turnbull A R (2017). Bacteriophages as enteric viral indicators in bivalve mollusc management. Food Microbiology, 65: 284–293
CrossRef
Google scholar
|
[40] |
Jassim S A, Limoges R G (2013). Impact of external forces on cyanophage–host interactions in aquatic ecosystems. World Journal of Microbiology & Biotechnology, 29(10): 1751–1762
CrossRef
Google scholar
|
[41] |
Jassim S A, Limoges R G, El-Cheikh H (2016). Bacteriophages biocontrol in wastewater treatment. World Journal of Microbiology & Biotechnology, 32(4): 70
CrossRef
Google scholar
|
[42] |
Jassim S A, Limoges R G (2017). Bacteriophages: Practical Applications for Nature’s Biocontrol. Dordrecht: Springer
|
[43] |
Jofre J, Blanch A R, Lucena F, Muniesa M (2014). Bacteriophages infecting Bacteroides as a marker for microbial source tracking. Water Research, 55: 1–11
CrossRef
Google scholar
|
[44] |
Jofre J, Lucena F, Blanch A R, Muniesa M (2016). Coliphages as model organisms in the characterization and management of water resources. Water (Basel), 8(5): 199
CrossRef
Google scholar
|
[45] |
Jun J W, Giri S S, Kim H J, Yun S K, Chi C, Chai J Y, Lee B C, Park S C (2016). Bacteriophage application to control the contaminated water with Shigella. Scientific Reports, 6: 22636
CrossRef
Google scholar
|
[46] |
Karumidze N, Kusradze I, Rigvava S, Goderdzishvili M, Rajakumar K, Alavidze Z (2013). Isolation and characterisation of lytic bacteriophages of Klebsiella pneumoniae and Klebsiella oxytoca. Current Microbiology, 66(3): 251–258
CrossRef
Google scholar
|
[47] |
Khan F M, Gupta R (2020). Escherichia coli (E. coli) as an Indicator of Fecal Contamination in Groundwater: A Review. New York: Springer, 225–235
|
[48] |
Kotay S M, Datta T, Choi J, Goel R (2011). Biocontrol of biomass bulking caused by Haliscomenobacter hydrossis using a newly isolated lytic bacteriophage. Water Research, 45(2): 694–704
CrossRef
Google scholar
|
[49] |
Kwiatek M, Parasion S, Rutyna P, Mizak L, Gryko R, Niemcewicz M, Olender A, Łobocka M (2017). Isolation of bacteriophages and their application to control Pseudomonas aeruginosa in planktonic and biofilm models. Research in Microbiology, 168(3): 194–207
CrossRef
Google scholar
|
[50] |
Larrañaga O, Brown-Jaque M, Quirós P, Gómez-Gómez C, Blanch A R, Rodríguez-Rubio L, Muniesa M (2018). Phage particles harboring antibiotic resistance genes in fresh-cut vegetables and agricultural soil. Environment International, 115: 133–141
CrossRef
Google scholar
|
[51] |
Lekunberri I, Subirats J, Borrego C M, Balcázar J L (2017a). Exploring the contribution of bacteriophages to antibiotic resistance. Environmental Pollution, 220: 981–984
CrossRef
Google scholar
|
[52] |
Lekunberri I, Villagrasa M, Balcázar J L, Borrego C M (2017b). Contribution of bacteriophage and plasmid DNA to the mobilization of antibiotic resistance genes in a river receiving treated wastewater discharges. Science of the Total Environment, 601-602: 206–209
CrossRef
Google scholar
|
[53] |
Leung S S, Morales S, Britton W, Kutter E, Chan H K (2018). Microfluidic-assisted bacteriophage encapsulation into liposomes. International Journal of Pharmaceutics, 545(1–2): 176–182
CrossRef
Google scholar
|
[54] |
Li B, Ju F, Cai L, Zhang T (2015). Profile and fate of bacterial pathogens in sewage treatment plants revealed by high-throughput metagenomic approach. Environmental Science & Technology, 49(17): 10492–10502
CrossRef
Google scholar
|
[55] |
Li L L, Yu P, Wang X, Yu S S, Mathieu J, Yu H Q, Alvarez P J (2017). Enhanced biofilm penetration for microbial control by polyvalent phages conjugated with magnetic colloidal nanoparticle clusters (CNCs). Environmental Science. Nano, 4(9): 1817–1826
CrossRef
Google scholar
|
[56] |
Liang Y, Jin X, Huang Y, Chen S (2018). Development and application of a real-time polymerase chain reaction assay for detection of a novel gut bacteriophage (CrAssphage). Journal of Medical Virology, 90(3): 464–468
CrossRef
Google scholar
|
[57] |
Lin N T, Chiou P Y, Chang K C, Chen L K, Lai M J (2010). Isolation and characterization of AB2: A novel bacteriophage of Acinetobacter baumannii. Research in Microbiology, 161(4): 308–314
CrossRef
Google scholar
|
[58] |
Liu M, Gill J J, Young R, Summer E J (2015). Bacteriophages of wastewater foaming-associated filamentous Gordonia reduce host levels in raw activated sludge. Scientific Reports, 5(1): 13754
CrossRef
Google scholar
|
[59] |
Lu T K, Collins J J (2007). Dispersing biofilms with engineered enzymatic bacteriophage. Proceedings of the National Academy of Sciences of the United States of America, 104(27): 11197–11202
CrossRef
Google scholar
|
[60] |
Maal K B, Delfan A S, Salmanizadeh S (2015). Isolation and identification of two novel Escherichia Coli bacteriophages and their application in wastewater treatment and coliform’s phage therapy. Jundishapur Journal of Microbiology, 8(3): e14945
CrossRef
Google scholar
|
[61] |
Mathieu J, Yu P, Zuo P, Da Silva M L, Alvarez P J (2019). Going viral: Emerging opportunities for phage-based bacterial control in water treatment and reuse. Accounts of Chemical Research, 52(4): 849–857
CrossRef
Google scholar
|
[62] |
McMinn B R, Ashbolt N J, Korajkic A (2017). Bacteriophages as indicators of faecal pollution and enteric virus removal. Letters in Applied Microbiology, 65(1): 11–26
CrossRef
Google scholar
|
[63] |
Moazeni M, Nikaeen M, Hadi M, Moghim S, Mouhebat L, Hatamzadeh M, Hassanzadeh A (2017). Estimation of health risks caused by exposure to enteroviruses from agricultural application of wastewater effluents. Water Research, 125: 104–113
CrossRef
Google scholar
|
[64] |
Monteiro R, Pires D P, Costa A R, Azeredo J (2019). Phage therapy: going temperate? Trends in Microbiology, 27(4): 368–378
CrossRef
Google scholar
|
[65] |
Motlagh A M, Bhattacharjee A S, Goel R (2016). Biofilm control with natural and genetically-modified phages. World Journal of Microbiology & Biotechnology, 32(4): 67
CrossRef
Google scholar
|
[66] |
Muniesa M, Ballesté E, Imamovic L, Pascual-Benito M, Toribio-Avedillo D, Lucena F, Blanch A, Jofre J (2018). Bluephage: A rapid method for the detection of somatic coliphages used as indicators of fecal pollution in water. Water Research, 128: 10–19
CrossRef
Google scholar
|
[67] |
Petrovski S, Seviour R J, Tillett D (2011a). Characterization of the genome of the polyvalent lytic bacteriophage GTE2, which has potential for biocontrol of Gordonia-, Rhodococcus-, and Nocardia-stabilized foams in activated sludge plants. Applied and Environmental Microbiology, 77(12): 3923–3929
CrossRef
Google scholar
|
[68] |
Petrovski S, Seviour R J, Tillett D (2011b). Prevention of Gordonia and Nocardia stabilized foam formation by using bacteriophage GTE7. Applied and Environmental Microbiology, 77(21): 7864–7867
CrossRef
Google scholar
|
[69] |
Pires D P, Melo L D R, Vilas Boas D, Sillankorva S, Azeredo J (2017). Phage therapy as an alternative or complementary strategy to prevent and control biofilm-related infections. Current Opinion in Microbiology, 39: 48–56
CrossRef
Google scholar
|
[70] |
Purnell S, Ebdon J, Wilkins H, Taylor H (2018). Human-specific phages infecting Enterococcus host strain MW47: are they reliable microbial source tracking markers? Journal of Applied Microbiology, 124(5): 1274–1282
CrossRef
Google scholar
|
[71] |
Purnell S E, Ebdon J E, Taylor H D (2011). Bacteriophage lysis of Enterococcus host strains: A tool for microbial source tracking? Environmental Science & Technology, 45(24): 10699–10705
CrossRef
Google scholar
|
[72] |
Rémy B, Mion S, Plener L, Elias M, Chabrière E, Daudé D (2018). Interference in bacterial quorum sensing: A biopharmaceutical perspective. Frontiers in Pharmacology, 9: 203
CrossRef
Google scholar
|
[73] |
Richter Ł, Janczuk-Richter M, Niedziółka-Jönsson J, Paczesny J, Hołyst R (2018). Recent advances in bacteriophage-based methods for bacteria detection. Drug Discovery Today, 23(2): 448–455
CrossRef
Google scholar
|
[74] |
Rodriguez-Mozaz S, Chamorro S, Marti E, Huerta B, Gros M, Sànchez-Melsió A, Borrego C M, Barceló D, Balcázar J L (2015). Occurrence of antibiotics and antibiotic resistance genes in hospital and urban wastewaters and their impact on the receiving river. Water Research, 69: 234–242
CrossRef
Google scholar
|
[75] |
Şener Ş, Şener E, Davraz A (2017). Evaluation of water quality using water quality index (WQI) method and GIS in Aksu River (SW-Turkey). Science of the Total Environment, 584-585: 131–144
CrossRef
Google scholar
|
[76] |
Shkoporov A N, Khokhlova E V, Fitzgerald C B, Stockdale S R, Draper L A, Ross R P, Hill C (2018). CrAss001 represents the most abundant bacteriophage family in the human gut and infects Bacteroides intestinalis. Nature Communications, 9(1): 4781
CrossRef
Google scholar
|
[77] |
Soller J A, Schoen M E, Bartrand T, Ravenscroft J E, Ashbolt N J (2010). Estimated human health risks from exposure to recreational waters impacted by human and non-human sources of faecal contamination. Water Research, 44(16): 4674–4691
CrossRef
Google scholar
|
[78] |
Stachler E, Kelty C, Sivaganesan M, Li X, Bibby K, Shanks O C (2017). Quantitative CrAssphage PCR Assays for Human Fecal Pollution Measurement. Environmental Science & Technology, 51(16): 9146–9154
CrossRef
Google scholar
|
[79] |
Su J Q, An X L, Li B, Chen Q L, Gillings M R, Chen H, Zhang T, Zhu Y G (2017). Metagenomics of urban sewage identifies an extensively shared antibiotic resistome in China. Microbiome, 5(1): 84
CrossRef
Google scholar
|
[80] |
Toribio-Avedillo D, Martín-Díaz J, Jofre J, Blanch A R, Muniesa M (2019). New approach for the simultaneous detection of somatic coliphages and F-specific RNA coliphages as indicators of fecal pollution. Science of the Total Environment, 655: 263–272
CrossRef
Google scholar
|
[81] |
Touchon M, Moura de Sousa J A, Rocha E P (2017). Embracing the enemy: the diversification of microbial gene repertoires by phage-mediated horizontal gene transfer. Current Opinion in Microbiology, 38: 66–73
CrossRef
Google scholar
|
[82] |
Turki Y, Ouzari H, Mehri I, Ammar A B, Hassen A (2012). Evaluation of a cocktail of three bacteriophages for the biocontrol of Salmonella of wastewater. Food Research International, 45(2): 1099–1105
CrossRef
Google scholar
|
[83] |
Vijayavel K, Byappanahalli M N, Ebdon J, Taylor H, Whitman R, Kashian D (2014). Enterococcus phages as potential tool for identifying sewage inputs in the Great Lakes region. Journal of Great Lakes Research, 40(4): 989–993
CrossRef
Google scholar
|
[84] |
Vijayavel K, Fujioka R, Ebdon J, Taylor H (2010). Isolation and characterization of Bacteroides host strain HB-73 used to detect sewage specific phages in Hawaii. Water Research, 44(12): 3714–3724
CrossRef
Google scholar
|
[85] |
Wang M, Liu P, Zhou Q, Tao W, Sun Y, Zeng Z (2018). Estimating the contribution of bacteriophage to the dissemination of antibiotic resistance genes in pig feces. Environmental Pollution, 238: 291–298
CrossRef
Google scholar
|
[86] |
Wangkahad B, Mongkolsuk S, Sirikanchana K (2017). Integrated multivariate analysis with nondetects for the development of human sewage source-tracking tools using bacteriophages of Enterococcus faecalis. Environmental Science & Technology, 51(4): 2235–2245
CrossRef
Google scholar
|
[87] |
Wei Y, Kirby A, Levin B R (2011). The population and evolutionary dynamics of Vibrio cholerae and its bacteriophage: Conditions for maintaining phage-limited communities. American Naturalist, 178(6): 715–725
CrossRef
Google scholar
|
[88] |
Wu B, Wang R, Fane A G (2017). The roles of bacteriophages in membrane-based water and wastewater treatment processes: A review. Water Research, 110: 120–132
CrossRef
Google scholar
|
[89] |
Wu Z, Greaves J, Arp L, Stone D, Bibby K (2020). Comparative fate of CrAssphage with culturable and molecular fecal pollution indicators during activated sludge wastewater treatment. Environment International, 136: 105452
CrossRef
Google scholar
|
[90] |
Yang Y, Shi W, Lu S Y, Liu J, Liang H, Yang Y, Duan G, Li Y, Wang H, Zhang A (2018). Prevalence of antibiotic resistance genes in bacteriophage DNA fraction from Funan River water in Sichuan, China. Science of the Total Environment, 626: 835–841
CrossRef
Google scholar
|
[91] |
Yang Y, Xie X, Tang M, Liu J, Tuo H, Gu J, Tang Y, Lei C, Wang H, Zhang A (2020). Exploring the profile of antimicrobial resistance genes harboring by bacteriophage in chicken feces. Science of the Total Environment, 700: 134446
CrossRef
Google scholar
|
[92] |
Yen M, Cairns L S, Camilli A (2017). A cocktail of three virulent bacteriophages prevents Vibrio cholerae infection in animal models. Nature Communications, 8(1): 14187
CrossRef
Google scholar
|
[93] |
Yoshida-Takashima Y, Yoshida M, Ogata H, Nagasaki K, Hiroishi S, Yoshida T (2012). Cyanophage infection in the bloom-forming cyanobacteria Microcystis aeruginosa in surface freshwater. Microbes and Environments, 27(4): 350–355
CrossRef
Google scholar
|
[94] |
Yu P, Mathieu J, Li M, Dai Z, Alvarez P J (2016). Isolation of polyvalent bacteriophages by sequential multiple-host approaches. Applied and Environmental Microbiology, 82(3): 808–815
CrossRef
Google scholar
|
[95] |
Yu P, Mathieu J, Lu G W, Gabiatti N, Alvarez P J (2017). Control of antibiotic-resistant bacteria in activated sludge using polyvalent phages in conjunction with a production host. Environmental Science & Technology Letters, 4(4): 137–142
CrossRef
Google scholar
|
[96] |
Yue H, He Y, Fan E, Wang L, Lu S, Fu Z (2017). Label-free electrochemiluminescent biosensor for rapid and sensitive detection of pseudomonas aeruginosa using phage as highly specific recognition agent. Biosensors & Bioelectronics, 94: 429–432
CrossRef
Google scholar
|
[97] |
Zhang A, Call D R, Besser T E, Liu J, Jones L, Wang H, Davis M A (2019).β-lactam resistance genes in bacteriophage and bacterial DNA from wastewater, river water, and irrigation water in Washington State. Water Research, 161: 335–340
CrossRef
Google scholar
|
[98] |
Zhou Y, Marar A, Kner P, Ramasamy R P (2017). Charge-directed immobilization of bacteriophage on nanostructured electrode for whole-cell electrochemical biosensors. Analytical Chemistry, 89(11): 5734–5741
CrossRef
Google scholar
|
/
〈 | 〉 |