Applications of bacteriophages in precision engineering of the human gut microbiome

Xiaoxian Kuang , Juntao Shen , Linggang Zheng , Yi Duan , Yingfei Ma , Elaine Lai-Han Leung , Lei Dai

Engineering Microbiology ›› 2025, Vol. 5 ›› Issue (1) : 100189

PDF (3096KB)
Engineering Microbiology ›› 2025, Vol. 5 ›› Issue (1) : 100189 DOI: 10.1016/j.engmic.2025.100189
Review

Applications of bacteriophages in precision engineering of the human gut microbiome

Author information +
History +
PDF (3096KB)

Abstract

As our understanding of the role of the gut microbiome in human diseases deepens, precision engineering of the gut microbiome using bacteriophages has gained significant attention. Herein, we review the recent advances in bacteriophage-mediated modulation of the gut microbiome, discuss approaches at the ecological and genetic levels, and summarize the challenges and strategies pertinent to each level of intervention. Drawing on the structural attributes of bacteriophages in the context of precision engineering, we examined the latest developments in the field of phage administration. Gaining a nuanced understanding of microbiome manipulation will yield tailored strategies and technologies. This could revolutionize the prevention and treatment of diseases linked to gut pathogens and offer new avenues for the therapeutic use of bacteriophages.

Keywords

Bacteriophages / Microbiome engineering / Human gut microbiome

Cite this article

Download citation ▾
Xiaoxian Kuang, Juntao Shen, Linggang Zheng, Yi Duan, Yingfei Ma, Elaine Lai-Han Leung, Lei Dai. Applications of bacteriophages in precision engineering of the human gut microbiome. Engineering Microbiology, 2025, 5(1): 100189 DOI:10.1016/j.engmic.2025.100189

登录浏览全文

4963

注册一个新账户 忘记密码

Declaration of Competing Interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

CRediT authorship contribution statement

Xiaoxian Kuang: Writing - review & editing, Writing - original draft, Visualization. Juntao Shen: Writing - original draft, Funding acquisition, Conceptualization. Linggang Zheng: Writing - review & editing, Writing - original draft. Yi Duan: Writing - review & editing. Yingfei Ma: Writing - review & editing. Elaine Lai-Han Leung: Writing - review & editing. Lei Dai: Writing - review & editing, Funding acquisition, Conceptualization.

Acknowledgments

This study was funded by the Guangdong Basic and Applied Basic Research Foundation (2024A1515011872) and the National Key R&D Program of China (2019YFA0906700). All illustrations in this work were created using the BioRender platform (©BioRender: biorender.com), which we extend our appreciation for its user-friendly design tools.

References

[1]

P.J. Turnbaugh, R.E. Ley, M. Hamady, C.M. Fraser-Liggett, R. Knight, J.I. Gordon, The Human Microbiome Project, Nature 449(2007) 804-810, doi: 10.1038/nature06244.

[2]

X. Zhu, B. Li, P. Lou, T. Dai, Y. Chen, A. Zhuge, Y. Yuan, L. Li, The Relationship Between the Gut Microbiome and Neurodegenerative Diseases, Neurosci. Bull. 37(2021) 1510-1522, doi: 10.1007/s12264-021-00730-8.

[3]

J. Wu, K. Wang, X. Wang, Y. Pang, C. Jiang, The role of the gut microbiome and its metabolites in metabolic diseases, Protein Cell 12(2021) 360-373, doi: 10.1007/s13238-020-00814-7.

[4]

N. Kazemian, M. Mahmoudi, F. Halperin, J.C. Wu, S. Pakpour, Gut microbiota and cardiovascular disease: opportunities and challenges, Microbiome 8(2020) 36, doi: 10.1186/s40168-020-00821-0.

[5]

K. Fu, A.H.K. Cheung, C.C. Wong, W. Liu, Y. Zhou, F. Wang, P. Huang, K. Yuan, O.O. Coker, Y. Pan, D. Chen, N.M. Lam, M. Gao, X. Zhang, H. Huang, K.F. To, J.J.Y. Sung, J. Yu, Streptococcus anginosus promotes gastric inflammation, atrophy, and tumorigenesis in mice, Cell 187 (2024) 882-896.e17, doi: 10.1016/j.cell.2024.01.004.

[6]

R. Xie, Y. Gu, M. Li, L. Li, Y. Yang, Y. Sun, B. Zhou, T. Liu, S. Wang, W. Liu, R. Yang, X. Su, W. Zhong, B. Wang, H. Cao, Desulfovibrio vulgaris interacts with novel gut epithelial immune receptor LRRC19 and exacerbates colitis, Microbiome 12(2024) 4, doi: 10.1186/s40168-023-01722-8.

[7]

W. Cui, M. Guo, D. Liu, P. Xiao, C. Yang, H. Huang, C. Liang, Y. Yang, X. Fu, Y. Zhang, J. Liu, S. Shi, J. Cong, Z. Han, Y. Xu, L. Du, C. Yin, Y. Zhang, J. Sun, W. Gu, R. Chai, S. Zhu, B. Chu, Gut microbial metabolite facilitates colorectal cancer development via ferroptosis inhibition, Nat. Cell Biol. (2024), doi: 10.1038/s41556-023-01314-6.

[8]

Y. Cao, J. Oh, M. Xue, W.J. Huh, J. Wang, J.A. Gonzalez-Hernandez, T.A. Rice, A.L. Martin, D. Song, J.M. Crawford, S.B. Herzon, N.W. Palm, Commensal microbiota from patients with inflammatory bowel disease produce genotoxic metabolites, Science 378(2022) eabm3233, doi: 10.1126/science.abm3233.

[9]

Y. An, Z. Zhai, X. Wang, Y. Ding, L. He, L. Li, Q. Mo, C. Mu, R. Xie, T. Liu, W. Zhong, B. Wang, H. Cao, Targeting Desulfovibrio vulgaris flagellin-induced NAIP/NLRC4 inflammasome activation in macrophages attenuates ulcerative colitis, J. Adv. Res. 52 (2023) 219-232, doi: 10.1016/j.jare.2023.08.008.

[10]

J.C. Taylor, X. Gao, J. Xu, M. Holder, J. Petrosino, R. Kumar, W. Liu, M. Höök, C. Mackenzie, A. Hillhouse, W. Brashear, M.P. Nunez, Y. Xu, A type VII secretion system of Streptococcus gallolyticus subsp. gallolyticus contributes to gut colonization and the development of colon tumors, PLOS Pathog 17(2021) e1009182, doi: 10.1371/journal.ppat.1009182.

[11]

T.M.G. Dronkers, A.C. Ouwehand, G.T. Rijkers, Global analysis of clinical trials with probiotics, Heliyon 6 (2020) e04467, doi: 10.1016/j.heliyon.2020.e04467.

[12]

P. Panchal, S. Budree, A. Scheeler, G. Medina, M. Seng, W.F. Wong, R. Eliott, T. Mitchell, Z. Kassam, J.R. Allegretti, M. Osman, Scaling Safe Access to Fecal Microbiota Transplantation: Past, Present, and Future, Curr. Gastroenterol. Rep. 20(2018) 14, doi: 10.1007/s11894-018-0619-8.

[13]

J. Suez, N. Zmora, G. Zilberman-Schapira, U. Mor, M. Dori-Bachash, S. Bashiardes, M. Zur, D. Regev-Lehavi, R. Ben-Zeev Brik, S. Federici, M. Horn, Y. Cohen, A.E. Moor, D. Zeevi, T. Korem, E. Kotler, A. Harmelin, S. Itzkovitz, N. Maharshak, O. Shibolet, M. Pevsner-Fischer, H. Shapiro, I. Sharon, Z. Halpern, E. Segal, E. Elinav, Post-Antibiotic Gut Mucosal Microbiome Reconstitution Is Impaired by Probiotics and Improved by Autologous FMT, Cell 174 (2018) 1406-1423.e16, doi: 10.1016/j.cell.2018.08.047.

[14]

Y. Yu, W. Wang, F. Zhang, The Next Generation Fecal Microbiota Transplantation: To Transplant Bacteria or Virome, Adv. Sci. 10(2023) 2301097, doi: 10.1002/advs.202301097.

[15]

T. Zuo, S.H. Wong, K. Lam, R. Lui, K. Cheung, W. Tang, J.Y.L. Ching, P.K.S. Chan, M.C.W. Chan, J.C.Y. Wu, F.K.L. Chan, J. Yu, J.J.Y. Sung, S.C. Ng, Bacteriophage transfer during faecal microbiota transplantation in Clostridium difficile infection is associated with treatment outcome, Gut (2017) gutjnl-2017-313952, doi: 10.1136/gutjnl-2017-313952.

[16]

A. Megur, E.B.M. Daliri, D. Baltriukien ė, A. Burokas, Prebiotics as a Tool for the Prevention and Treatment of Obesity and Diabetes: Classification and Ability to Modulate the Gut Microbiota, Int. J. Mol. Sci. 23(2022) 6097, doi: 10.3390/ijms23116097.

[17]

A.K. Brödel, L.H. Charpenay, M. Galtier, F.J. Fuche, R. Terrasse, C. Poquet, J. Havránek, S. Pignotti, A. Krawczyk, M. Arraou, G. Prevot, D. Spadoni, M.T.N. Yarnall, E.M. Hessel, J. Fernandez-Rodriguez, X. Duportet, D. Bikard, situ targeted base editing of bacteria in the mouse gut, Nature (2024), doi: 10.1038/s41586-024-07681-w.

[18]

A. Bruttin, H. Brüssow, Human Volunteers Receiving Escherichia coli Phage T4 Orally: a Safety Test of Phage Therapy, Antimicrob. Agents Chemother. 49 (2005) 2874-2878, doi: 10.1128/AAC.49.7.2874-2878.2005.

[19]

E. Chain, H.W. Florey, A.D. Gardner, N.G. Heatley, M.A. Jennings, J. Orr-Ewing, A.G. Sanders, Penicillin as a chemotherapeutic agent, The Lancet 236(1940) 226-228.

[20]

R.J. Citorik, M. Mimee, T.K. Lu, Sequence-specific antimicrobials using efficiently delivered RNA-guided nucleases, Nat. Biotechnol. 32(2014) 1141-1145, doi: 10.1038/nbt.3011.

[21]

Y. Duan, C. Llorente, S. Lang, K. Brandl, H. Chu, L. Jiang, R.C. White, T.H. Clarke, K. Nguyen, M. Torralba, Y. Shao, J. Liu, A. Hernandez-Morales, L. Lessor, I.R. Rahman, Y. Miyamoto, M. Ly, B. Gao, W. Sun, R. Kiesel, F. Hutmacher, S. Lee, M. Ventura-Cots, F. Bosques-Padilla, E.C. Verna, J.G. Abraldes, R.S. Brown, V. Vargas, J. Altamirano, J. Caballería, D.L. Shawcross, S.B. Ho, A. Louvet, M.R. Lucey, P. Mathurin, G. Garcia-Tsao, R. Bataller, X.M. Tu, L. Eckmann, W.A. Van Der Donk, R. Young, T.D. Lawley, P. Stärkel, D. Pride, D.E. Fouts, B. Schnabl, Bacteriophage targeting of gut bacterium attenuates alcoholic liver disease, Nature 575(2019) 505-511, doi: 10.1038/s41586-019-1742-x.

[22]

S. Federici, S. Kredo-Russo, R. Valdés-Mas, D. Kviatcovsky, E. Weinstock, Y. Matiuhin, Y. Silberberg, K. Atarashi, M. Furuichi, A. Oka, B. Liu, M. Fibelman, I.N. Weiner, E. Khabra, N. Cullin, N. Ben-Yishai, D. Inbar, H. Ben-David, J. Nicenboim, N. Kowalsman, W. Lieb, E. Kario, T. Cohen, Y.F. Geffen, L. Zelcbuch, A. Cohen, U. Rappo, I. Gahali-Sass, M. Golembo, V. Lev, M. Dori-Bachash, H. Shapiro, C. Moresi, A. Cuevas-Sierra, G. Mohapatra, L. Kern, D. Zheng, S.P. Nobs, J. Suez, N. Stettner, A. Harmelin, N. Zak, S. Puttagunta, M. Bassan, K. Honda, H. Sokol, C. Bang, A. Franke, C. Schramm, N. Maharshak, R.B. Sartor, R. Sorek, E. Elinav, Targeted suppression of human IBD-associated gut microbiota commensals by phage consortia for treatment of intestinal inflammation, Cell 185 (2022) 2879-2898.e24, doi: 10.1016/j.cell.2022.07.003.

[23]

Y.E. Gencay, D. Jasinskyt ė, C. Robert, S. Semsey, V. Martínez, A.Ø. Petersen, K. Brunner, A. De Santiago Torio, A. Salazar, I.C. Turcu, M.K. Eriksen, L. Koval, A. Takos, R. Pascal, T.S. Schou, L. Bayer, T. Bryde, K.C. Johansen, E.G. Bak, F. Smrekar, T.B. Doyle, M.J. Satlin, A. Gram, J. Carvalho, L. Jessen, B. Hallström, J. Hink, B. Damholt, A. Troy, M. Grove, J. Clube, C. Grøndahl, J.K. Haaber, E. Van Der Helm, M. Zdravkovic, M.O.A. Sommer, Engineered phage with antibacterial CRISPR-Cas selectively reduce E. coli burden in mice, Nat. Biotechnol. 42(2024) 265-274, doi: 10.1038/s41587-023-01759-y.

[24]

F. de Herelle, Sur un microbe invisible antagoniste des bacilles dysentériques, C. r. Académie Sci 165(1917) 373-375.

[25]

B.B. Hsu, I.N. Plant, L. Lyon, F.M. Anastassacos, J.C. Way, P.A. Silver, In situ reprogramming of gut bacteria by oral delivery, Nat. Commun. 11(2020) 5030, doi: 10.1038/s41467-020-18614-2.

[26]

A.P. KRUEGER, E.J. SCRIBNER, THE BACTERIOPHAGE: ITS NATURE AND ITS THERAPEUTIC USE, J. Am. Med. Assoc. 116(1941) 2269-2277, doi: 10.1001/jama.1941.62820200013011.

[27]

E.B. McKINLEY, THE BACTERIOPHAGE IN THE TREATMENT OF INFECTIONS, Arch. Intern. Med. 32(1923) 899-910, doi: 10.1001/archinte.1923.00110240092005.

[28]

K.A. Monsur, M.A. Rahman, F. Huq, M.N. Islam, R.S. Northrup, N. Hirschhorn, Effect of massive doses of bacteriophage on excretion of vibrios, duration of diarrhoea and output of stools in acute cases of cholera, Bull. World Health Organ. 42(1970) 723-732.

[29]

H.W. Smith, M.B. Huggins, Successful treatment of experimental Escherichia coli infections in mice using phage: its general superiority over antibiotics, Microbiology 128(1982) 307-318.

[30]

F.W. Twort, AN INVESTIGATION ON THE NATURE OF ULTRAMICROSCOPIC VIRUSES, Orig. Publ. 2(4814) (1915) 1241-1243 Issue186, doi: 10.1016/S0140-6736(01)20383-3.

[31]

S.X. Zhou, L.P. Wang, M.Y. Liu, H.Y. Zhang, Q.B. Lu, L.S. Shi, X. Ren, Y.F. Wang, S.H. Lin, C.H. Zhang, M.J. Geng, X.A. Zhang, Y.L. Zhu, Z.J. Li, L.Q. Fang, W. Liu, W.Z. Yang, Characteristics of diarrheagenic Escherichia coli among patients with acute diarrhea in China, 2009-2018, J. Infect. 83(2021) 424-432, doi: 10.1016/j.jinf.2021.08.001.

[32]

J. Czepiel, M. Dróż d ż, H. Pituch, E.J. Kuijper, W. Perucki, A. Mielimonka, S. Goldman, D. Wulta ń ska, A. Garlicki, G. Biesiada, Clostridium difficile infection: review, Eur. J. Clin. Microbiol. Infect. Dis. 38(2019) 1211-1221, doi: 10.1007/s10096-019-03539-6.

[33]

N. Wang, J.Y. Fang, Fusobacterium nucleatum, a key pathogenic factor and microbial biomarker for colorectal cancer, Trends Microbiol 31(2023) 159-172, doi: 10.1016/j.tim.2022.08.010.

[34]

J.B. Kaper, J.P. Nataro, H.L.T. Mobley, Pathogenic Escherichia coli, Nat. Rev. Microbiol. 2(2004) 123-140, doi: 10.1038/nrmicro818.

[35]

J.G. Kusters, A.H.M. Van Vliet, E.J. Kuipers, Pathogenesis of Helicobacter pylori Infection, Clin. Microbiol. Rev. 19(2006) 449-490, doi: 10.1128/CMR.00054-05.

[36]

G.L. Popa, M.I. Popa, Salmonella spp. infection - a continuous threat worldwide, GERMS 11(2021) 88-96, doi: 10.18683/germs.2021.1244.

[37]

R.T. Schooley, B. Biswas, J.J. Gill, A. Hernandez-Morales, J. Lancaster, L. Lessor, J.J. Barr, S.L. Reed, F. Rohwer, S. Benler, A.M. Segall, R. Taplitz, D.M. Smith, K. Kerr, M. Kumaraswamy, V. Nizet, L. Lin, M.D. McCauley, S.A. Strathdee, C.A. Benson, R.K. Pope, B.M. Leroux, A.C. Picel, A.J. Mateczun, K.E. Cilwa, J.M. Regeimbal, L.A. Estrella, D.M. Wolfe, M.S. Henry, J. Quinones, S. Salka, K.A. Bishop-Lilly, R. Young, T. Hamilton, Development and Use of Personalized Bacteriophage-Based Therapeutic Cocktails To Treat a Patient with a Disseminated Resistant Acinetobacter baumannii Infection, Antimicrob. Agents Chemother 61 (2017) e00954 -17, doi: 10.1128/AAC.00954-17.

[38]

S. Jennes, M. Merabishvili, P. Soentjens, K.W. Pang, T. Rose, E. Keersebilck, O. Soete, P.M. François, S. Teodorescu, G. Verween, G. Verbeken, D. De Vos, J.P. Pirnay, Use of bacteriophages in the treatment of colistin-only-sensitive Pseudomonas aeruginosa septicaemia in a patient with acute kidney injury —a case report, Crit. Care 21(2017) 129, doi: 10.1186/s13054-017-1709-y.

[39]

J.A. Nick, R.M. Dedrick, A.L. Gray, E.K. Vladar, B.E. Smith, K.G. Freeman, K.C. Malcolm, L.E. Epperson, N.A. Hasan, J. Hendrix, K. Callahan, K. Walton, B. Vestal, E. Wheeler, N.M. Rysavy, K. Poch, S. Caceres, V.K. Lovell, K.B. Hisert, V.C. De Moura, D. Chatterjee, P. De, N. Weakly, S.L. Martiniano, D.A. Lynch, C.L. Daley, M. Strong, F. Jia, G.F. Hatfull, R.M. Davidson, Host and pathogen response to bacteriophage engineered against Mycobacterium abscessus lung infection, Cell 185(2022) 1860-1874.e12. https://doi.org/10.1016/j.cell.2022.04.024.

[40]

R.M. Dedrick, C.A. Guerrero-Bustamante, R.A. Garlena, D.A. Russell, K. Ford, K. Harris, K.C. Gilmour, J. Soothill, D. Jacobs-Sera, R.T. Schooley, G.F. Hatfull, H. Spencer, Engineered bacteriophages for treatment of a patient with a disseminated drug-resistant Mycobacterium abscessus, Nat. Med. 25(2019) 730-733, doi: 10.1038/s41591-019-0437-z.

[41]

J. Chow, S.K. Mazmanian, A Pathobiont of the Microbiota Balances Host Colonization and Intestinal Inflammation, Cell Host Microbe 7(2010) 265-276, doi: 10.1016/j.chom.2010.03.004.

[42]

L. Osbelt, M. Wende, É. Almási, E. Derksen, U. Muthukumarasamy, T.R. Lesker, E.J.C. Galvez, M.C. Pils, E. Schalk, P. Chhatwal, J. Färber, M. Neumann- Schaal, T. Fischer, D. Schlüter, T. Strowig, Klebsiella oxytoca causes colonization resistance against multidrug-resistant K. pneumoniae in the gut via cooperative carbohydrate competition, Cell Host Microbe 29 (2021) 1663-1679.e7, doi: 10.1016/j.chom.2021.09.003.

[43]

S.A. Pötgens, H. Brossel, M. Sboarina, E. Catry, P.D. Cani, A.M. Neyrinck, N.M. Delzenne, L.B. Bindels, Klebsiella oxytoca expands in cancer cachexia and acts as a gut pathobiont contributing to intestinal dysfunction, Sci. Rep. 8(2018) 12321, doi: 10.1038/s41598-018-30569-5.

[44]

B.B. Finlay, CIFAR Humans, the Microbiome, Are noncommunicable diseases communicable? Science 367(2020) 250-251, doi: 10.1126/science.aaz3834.

[45]

D. Kviatcovsky, R. Valdés-Mas, S. Federici, E. Elinav, Phage therapy in noncommunicable diseases, Science 382(2023) 266-267, doi: 10.1126/science.adh2718.

[46]

C. Ramakrishna, M. Kujawski, H. Chu, L. Li, S.K. Mazmanian, E.M. Cantin, Bacteroides fragilis polysaccharide A induces IL-10 secreting B and T cells that prevent viral encephalitis, Nat. Commun. 10(2019) 2153, doi: 10.1038/s41467-019-09884-6.

[47]

E. Valguarnera, J.B. Wardenburg, Good Gone Bad: One Toxin Away From Disease for Bacteroides fragilis, J. Mol. Biol. 432(2020) 765-785, doi: 10.1016/j.jmb.2019.12.003.

[48]

L. Sun, Y. Zhang, J. Cai, B. Rimal, E.R. Rocha, J.P. Coleman, C. Zhang, R.G. Nichols, Y. Luo, B. Kim, Y. Chen, K.W. Krausz, C.C. Harris, A.D. Patterson, Z. Zhang, S. Takahashi, F.J. Gonzalez, Bile salt hydrolase in nonenterotoxigenic Bacteroides potentiates colorectal cancer, Nat. Commun. 14(2023) 755, doi: 10.1038/s41467-023-36089-9.

[49]

J. Yang, Y. Li, N. Tang, J. Li, J. Zhou, S. Lu, G. Zhang, Y. Song, C. Wang, J. Zhong, J. Xu, J. Feng, The human gut serves as a reservoir of hypervirulent Klebsiella pneumoniae, Gut Microbes 14(2022) 2114739, doi: 10.1080/19490976.2022.2114739.

[50]

N. Nakamoto, N. Sasaki, R. Aoki, K. Miyamoto, W. Suda, T. Teratani, T. Suzuki, Y. Koda, P.S. Chu, N. Taniki, A. Yamaguchi, M. Kanamori, N. Kamada, M. Hattori, H. Ashida, M. Sakamoto, K. Atarashi, S. Narushima, A. Yoshimura, K. Honda, T. Sato, T. Kanai, Gut pathobionts underlie intestinal barrier dysfunction and liver T helper 17 cell immune response in primary sclerosing cholangitis, Nat. Microbiol. 4 (2019) 492-503, doi: 10.1038/s41564-018-0333-1.

[51]

J. Yuan, C. Chen, J. Cui, J. Lu, C. Yan, X. Wei, X. Zhao, N. Li, S. Li, G. Xue, W. Cheng, B. Li, H. Li, W. Lin, C. Tian, J. Zhao, J. Han, D. An, Q. Zhang, H. Wei, M. Zheng, X. Ma, W. Li, X. Chen, Z. Zhang, H. Zeng, S. Ying, J. Wu, R. Yang, D. Liu, Fatty Liver Disease Caused by High-Alcohol-Producing Klebsiella pneumoniae, Cell Metab 30 (2019) 675-688.e7, doi: 10.1016/j.cmet.2019.08.018.

[52]

L. Jochum, B. Stecher, Label or Concept - What Is a Pathobiont? Trends Microbiol 28(2020) 789-792, doi: 10.1016/j.tim.2020.04.011.

[53]

B.K. Chan, S.T. Abedon, C. Loc-Carrillo, Phage cocktails and the future of phage therapy, Future Microbiol 8(2013) 769-783, doi: 10.2217/fmb.13.47.

[54]

J. Ye, Q. Meng, K. Jin, Y. Luo, T. Yue, Phage cocktail alleviated type 2 diabetes by reshaping gut microbiota and decreasing proinflammatory cytokines, Appl. Microbiol. Biotechnol. 108 (2024) 9, doi: 10.1007/s00253-023-12912-7.

[55]

C. Buttimer, T. Sutton, J. Colom, E. Murray, P.H. Bettio, L. Smith, A.S. Bolocan, A. Shkoporov, A. Oka, B. Liu, J.W. Herzog, R.B. Sartor, L.A. Draper, R.P. Ross, C. Hill, Impact of a phage cocktail targeting Escherichia coli and Enterococcus faecalis as members of a gut bacterial consortium in vitro and in vivo, Front. Microbiol. 13(2022) 936083, doi: 10.3389/fmicb.2022.936083.

[56]

T.R. Callaway, T.S. Edrington, A.D. Brabban, R.C. Anderson, M.L. Rossman, M.J. Engler, M.A. Carr, K.J. Genovese, J.E. Keen, M.L. Looper, E.M. Kutter, D.J. Nisbet, Bacteriophage Isolated from Feedlot Cattle Can Reduce Escherichia coli O157:H 7 Populations in Ruminant Gastrointestinal Tracts, Foodborne Pathog. Dis. 5 (2008) 183-191, doi: 10.1089/fpd.2007.0057.

[57]

V. Clavijo, M.J.V. Flórez, The gastrointestinal microbiome and its association with the control of pathogens in broiler chicken production: A review, Poult. Sci. 97(2018) 1006-1021, doi: 10.3382/ps/pex359.

[58]

X. Mao, Y. Wu, R. Ma, L. Li, L. Wang, Y. Tan, Z. Li, H. Liu, K. Han, Y. Cao, Y. Li, H. Peng, X. Li, C. Hu, X. Wang, Oral phage therapy with microencapsulated phage A221 against Escherichia coli infections in weaned piglets, BMC Vet. Res. 19 (2023) 165, doi: 10.1186/s12917-023-03724-y.

[59]

Q. Lamy-Besnier, L. Chaffringeon, M. Lourenço, R.B. Payne, J.T. Trinh, J.A. Schwartz, A. Sulakvelidze, L. Debarbieux, Prophylactic Administration of a Bacteriophage Cocktail Is Safe and Effective in Reducing Salmonella enterica Serovar Typhimurium Burden in Vivo, Microbiol. Spectr. 9(2021) e00497 -21, doi: 10.1128/Spectrum.00497-21.

[60]

A.M. Thanki, G. Mignard, R.J. Atterbury, P. Barrow, A.D. Millard, M.R.J. Clokie, Prophylactic Delivery of a Bacteriophage Cocktail in Feed Significantly Reduces Salmonella Colonization in Pigs, Microbiol. Spectr. 10 (2022) e00422 -22, doi: 10.1128/spectrum.00422-22.

[61]

R.P. Johnson, C.L. Gyles, W.E. Huff, S. Ojha, G.R. Huff, N.C. Rath, A.M. Donoghue, Bacteriophages for prophylaxis and therapy in cattle, poultry and pigs, Anim. Health Res. Rev. 9(2008) 201-215, doi: 10.1017/S1466252308001576.

[62]

V.L. Donati, L. Madsen, M. Middelboe, M.L. Strube, I. Dalsgaard, The Gut Microbiota of Healthy and Flavobacterium psychrophilum-Infected Rainbow Trout Fry Is Shaped by Antibiotics and Phage Therapies, Front. Microbiol. 13(2022) 771296, doi: 10.3389/fmicb.2022.771296.

[63]

Md. S. Ahasan, R. Kinobe, L. Elliott, L. Owens, J. Scott, J. Picard, R. Huerlimann, E. Ariel, Bacteriophage versus antibiotic therapy on gut bacterial communities of juvenile green turtle, Chelonia mydas, Environ. Microbiol. 21(2019) 2871-2885, doi: 10.1111/1462-2920.14644.

[64]

Y. Choi, W. Lee, J.G. Kwon, A. Kang, M.J. Kwak, J.Y. Eor, Y. Kim, The current state of phage therapy in livestock and companion animals, J. Anim. Sci. Technol. 66(2024) 57-78, doi: 10.5187/jast.2024.e5.

[65]

European Medicines Agency, Guideline on quality, safety and efficacy of veterinary medicinal products specifically designed for phage therapy, (2023). https://www.ema.europa.eu/en/quality-safety-and-efficacy-bacteriophages-veterinary-medicines-scientific-guideline.

[66]

C. Tartera, F. Lucena, J. Jofre, Human origin of Bacteroides fragilis bacteriophages present in the environment, Appl. Environ. Microbiol. 55(1989) 2696-2701, doi: 10.1128/aem.55.10.2696-2701.1989.

[67]

M. Kai, S. Watanabe, K. Furuse, A. Ozawa, Bacteroides Bacteriophages Isolated from Human Feces, Microbiol. Immunol. 29(1985) 895-899, doi: 10.1111/j.1348-0421.1985.tb00891.x.

[68]

A.J. Hryckowian, B.D. Merrill, N.T. Porter, W. Van Treuren, E.J. Nelson, R.A. Garlena, D.A. Russell, E.C. Martens, J.L. Sonnenburg, Bacteroides thetaiotaomicron- Infecting Bacteriophage Isolates Inform Sequence-Based Host Range Predictions, Cell Host Microbe 28 (2020) 371-379.e5, doi: 10.1016/j.chom.2020.06.011.

[69]

J. Shen, J. Zhang, L. Mo, Y. Li, Y. Li, C. Li, X. Kuang, Z. Tao, Z. Qu, L. Wu, J. Chen, S. Liu, L. Zeng, Z. He, Z. Chen, Y. Deng, T. Zhang, B. Li, L. Dai, Y. Ma, Large-scale phage cultivation for commensal human gut bacteria, Cell Host Microbe 31 (2023) 665-677.e7, doi: 10.1016/j.chom.2023.03.013.

[70]

A.C. Gregory, O. Zablocki, A.A. Zayed, A. Howell, B. Bolduc, M.B. Sullivan, The Gut Virome Database Reveals Age-Dependent Patterns of Virome Diversity in the Human Gut, Cell Host Microbe 28 (2020) 724-740.e8, doi: 10.1016/j.chom.2020.08.003.

[71]

M.A. Nethery, C. Hidalgo-Cantabrana, A. Roberts, R. Barrangou, CRISPR-based engineering of phages for in situ bacterial base editing, Proc. Natl. Acad. Sci. 119(2022) e2206744119, doi: 10.1073/pnas.2206744119.

[72]

E. Pfeifer, R.A. Bonnin, E.P.C. Rocha, Phage-Plasmids Spread Antibiotic Resistance Genes through Infection and Lysogenic Conversion, mBio 13 (2022) e01851 -22, doi: 10.1128/mbio.01851-22.

[73]

K. Selle, J.R. Fletcher, H. Tuson, D.S. Schmitt, L. McMillan, G.S. Vridhambal, A.J. Rivera, S.A. Montgomery, L.C. Fortier, R. Barrangou, C.M. Theriot, D.G. Ousterout, Vivo Targeting of Clostridioides difficile Using Phage-Delivered CRISPRCas3 Antimicrobials, mBio 11 (2020) e00019-20, doi: 10.1128/mBio.00019-20.

[74]

F.L. Nobrega, M. Vlot, P.A. De Jonge, L.L. Dreesens, H.J.E. Beaumont, R. Lavigne, B.E. Dutilh, S.J.J. Brouns, Targeting mechanisms of tailed bacteriophages, Nat. Rev. Microbiol. 16(2018) 760-773, doi: 10.1038/s41579-018-0070-8.

[75]

J.T. Rostøl, L. Marraffini, (Ph)ighting Phages: How Bacteria Resist Their Parasites, Cell Host Microbe 25(2019) 184-194, doi: 10.1016/j.chom.2019.01.009.

[76]

N. Madi, E.T. Cato, Md.Abu Sayeed, A. Creasy-Marrazzo, A. Cuénod, K. Islam, Md.I.U. Khabir, Md.T.R. Bhuiyan, Y.A. Begum, E. Freeman, A. Vustepalli, L. Brinkley, M. Kamat, L.S. Bailey, K.B. Basso, F. Qadri, A.I. Khan, B.J. Shapiro, E.J. Nelson, Phage predation, disease severity, and pathogen genetic diversity in cholera patients, Science 384(2024) eadj3166, doi: 10.1126/science.adj3166.

[77]

M. Jin, J. Chen, X. Zhao, G. Hu, H. Wang, Z. Liu, W.H. Chen, An Engineered 𝜆 Phage Enables Enhanced and Strain-Specific Killing of Enterohemorrhagic Escherichia coli, Microbiol. Spectr. 10 (2022) e01271 -22, doi: 10.1128/spectrum.01271-22.

[78]

S. Doron, S. Melamed, G. Ofir, A. Leavitt, A. Lopatina, M. Keren, G. Amitai, R. Sorek, Systematic discovery of antiphage defense systems in the microbial pangenome, Science 359(2018) eaar4120, doi: 10.1126/science.aar4120.

[79]

L. Gao, H. Altae-Tran, F. Böhning, K.S. Makarova, M. Segel, J.L. Schmid-Burgk, J. Koob, Y.I. Wolf, E.V. Koonin, F. Zhang, Diverse enzymatic activities mediate antiviral immunity in prokaryotes, Science 369(2020) 1077-1084, doi: 10.1126/science.aba0372.

[80]

A. Millman, S. Melamed, A. Leavitt, S. Doron, A. Bernheim, J. Hör, J. Garb, N. Bechon, A. Brandis, A. Lopatina, G. Ofir, D. Hochhauser, A. Stokar-Avihail, N. Tal, S. Sharir, M. Voichek, Z. Erez, J.L.M. Ferrer, D. Dar, A. Kacen, G. Amitai, R. Sorek, An expanded arsenal of immune systems that protect bacteria from phages, Cell Host Microbe 30 (2022) 1556-1569.e5, doi: 10.1016/j.chom.2022.09.017.

[81]

M. Landsberger, S. Gandon, S. Meaden, C. Rollie, A. Chevallereau, H. Chabas, A. Buckling, E.R. Westra, S. Van Houte, Anti-CRISPR Phages Cooperate to Overcome CRISPR-Cas Immunity, Cell 174 (2018) 908-916.e12, doi: 10.1016/j.cell.2018.05.058.

[82]

M. Lourenço, L. Chaffringeon, Q. Lamy-Besnier, T. Pédron, P. Campagne, C. Eberl, M. Bérard, B. Stecher, L. Debarbieux, L. De Sordi, The Spatial Heterogeneity of the Gut Limits Predation and Fosters Coexistence of Bacteria and Bacteriophages, Cell Host Microbe 28 (2020) 390-401.e5, doi: 10.1016/j.chom.2020.06.002.

[83]

X. Zou, X. Xiao, Z. Mo, Y. Ge, X. Jiang, R. Huang, M. Li, Z. Deng, S. Chen, L. Wang, S.Y. Lee, Systematic strategies for developing phage resistant Escherichia coli strains, Nat. Commun. 13(2022) 4491, doi: 10.1038/s41467-022-31934-9.

[84]

S. Meile, J. Du, M. Dunne, S. Kilcher, M.J. Loessner, Engineering therapeutic phages for enhanced antibacterial efficacy, Curr. Opin. Virol. 52(2022) 182-191, doi: 10.1016/j.coviro.2021.12.003.

[85]

T.K. Lu, J.J. Collins, Dispersing biofilms with engineered enzymatic bacteriophage, Proc. Natl. Acad. Sci. 104(2007) 11197-11202, doi: 10.1073/pnas.0704624104.

[86]

J. Du, S. Meile, J. Baggenstos, T. Jäggi, P. Piffaretti, L. Hunold, C.I. Matter, L. Leitner, T.M. Kessler, M.J. Loessner, S. Kilcher, M. Dunne, Enhancing bacteriophage therapeutics through in situ production and release of heterologous antimicrobial effectors, Nat. Commun. 14(2023) 4337, doi: 10.1038/s41467-023-39612-0.

[87]

M.A.M. Shaufi, C.C. Sieo, C.W. Chong, T. Geok Hun, A.R. Omar, G. Han Ming, Y.Wan Ho, Effects of Phage Cocktail, Probiotics, and Their Combination on Growth Performance and Gut Microbiota of Broiler Chickens, Animals 13(2023) 1328, doi: 10.3390/ani13081328.

[88]

A.M. Comeau, F. Tétart, S.N. Trojet, M.F. Prère, H.M. Krisch, Phage-Antibiotic Synergy (PAS): β-Lactam and Quinolone Antibiotics Stimulate Virulent Phage Growth, PLoS ONE 2(2007) e799, doi: 10.1371/journal.pone.0000799.

[89]

F. Gordillo Altamirano, J.H. Forsyth, R. Patwa, X. Kostoulias, M. Trim, D. Subedi, S.K. Archer, F.C. Morris, C. Oliveira, L. Kielty, D. Korneev, M.K. O’Bryan, T.J. Lithgow, A.Y. Peleg, J.J. Barr, Bacteriophage-resistant Acinetobacter baumannii are resensitized to antimicrobials, Nat. Microbiol. 6(2021) 157-161, doi: 10.1038/s41564-020-00830-7.

[90]

D.W. Zheng, X. Dong, P. Pan, K.W. Chen, J.X. Fan, S.X. Cheng, X.Z. Zhang, Phageguided modulation of the gut microbiota of mouse models of colorectal cancer augments their responses to chemotherapy, Nat. Biomed. Eng. 3(2019) 717-728, doi: 10.1038/s41551-019-0423-2.

[91]

F. Laforêt, C. Antoine, S. Lebrun, I. Gonza, E. Goya-Jorge, C. Douny, J.N. Duprez, M.L. Scippo, B. Taminiau, G. Daube, A. Fall, D. Thiry, V. Delcenserie, Impact Assessment of vB_KpnP_K1-ULIP33 Bacteriophage on the Human Gut Microbiota Using a Dynamic In Vitro Model, Viruses 15 (2023) 719, doi: 10.3390/v15030719.

[92]

L. Gan, Y. Feng, B. Du, H. Fu, Z. Tian, G. Xue, C. Yan, X. Cui, R. Zhang, J. Cui, H. Zhao, J. Feng, Z. Xu, Z. Fan, T. Fu, S. Du, S. Liu, Q. Zhang, Z. Yu, Y. Sun, J. Yuan, Bacteriophage targeting microbiota alleviates non-alcoholic fatty liver disease induced by high alcohol-producing Klebsiella pneumoniae, Nat. Commun. 14(2023) 3215, doi: 10.1038/s41467-023-39028-w.

[93]

G. Pinto, S.A. Shetty, E.G. Zoetendal, R.F.S. Gonçalves, A.C. Pinheiro, C. Almeida, J. Azeredo, H. Smidt, An in vitro fermentation model to study the impact of bacteriophages targeting Shiga toxin-encoding Escherichia coli on the colonic microbiota, Npj Biofilms Microbiomes 8(2022) 74, doi: 10.1038/s41522-022-00334-8.

[94]

L. Ping, L. Zhuoya, J. Pei, C. Jingchao, L. Yi, L. Guosheng, W. Hailei, Editing of a Specific Strain of Escherichia coli in the Mouse Gut Using Native Phages, Microbiol. Spectr. 10(2022) e01804-e01822, doi: 10.1128/spectrum.01804-22.

[95]

K. Kosznik-Kwaśnicka, M. Podlacha, Ł. Grabowski, M. Stasi ł oj ć, A. Nowak- Zaleska, K. Ciemi ń ska, Z. Cyske, A. Dydecka, L. Gaffke, J. Mantej, D. My ś li ń ska, A. Necel, K. Pierzynowska, E. Piotrowska, E. Radzanowska-Alenowicz, E. Rintz, K. Sitko, G. Topka-Bielecka, G. W ęgrzyn, A. W ęgrzyn, Biological aspects of phage therapy versus antibiotics against Salmonella enterica serovar Typhimurium infection of chickens, Front. Cell. Infect. Microbiol. 12(2022) 941867, doi: 10.3389/fcimb.2022.941867.

[96]

R.R. Jakobsen, J.T. Trinh, L. Bomholtz, S.K. Brok-Lauridsen, A. Sulakvelidze, D.S. Nielsen, A Bacteriophage Cocktail Significantly Reduces Listeria monocytogenes without Deleterious Impact on the Commensal Gut Microbiota under Simulated Gastrointestinal Conditions, Viruses 14(2022) 190, doi: 10.3390/v14020190.

[97]

J. Huang, L. Liang, K. Cui, P. Li, G. Hao, S. Sun, Salmonella phage CKT1 significantly relieves the body weight loss of chicks by normalizing the abnormal intestinal microbiome caused by hypervirulent Salmonella Pullorum, Poult. Sci. 101 (2022) 101668, doi: 10.1016/j.psj.2021.101668.

[98]

V. Clavijo, T. Morales, M.J. Vives-Flores, A.Reyes Muñoz, The gut microbiota of chickens in a commercial farm treated with a Salmonella phage cocktail, Sci. Rep. 12(2022) 991, doi: 10.1038/s41598-021-04679-6.

[99]

M. Corbellino, N. Kieffer, M. Kutateladze, N. Balarjishvili, L. Leshkasheli, L. Askilashvili, G. Tsertsvadze, S.G. Rimoldi, D. Nizharadze, N. Hoyle, L. Nadareishvili, S. Antinori, C. Pagani, D.G. Scorza, A.L.L. Romanò, S. Ardizzone, P. Danelli, M.R. Gismondo, M. Galli, P. Nordmann, L. Poirel, Eradication of a Multidrug- Resistant, Carbapenemase-Producing Klebsiella pneumoniae Isolate Following Oral and Intra-rectal Therapy With a Custom Made, Lytic Bacteriophage Preparation, Clin. Infect. Dis. 70(2020) 1998-2001, doi: 10.1093/cid/ciz782.

[100]

P.J. Richards, P.L. Connerton, I.F. Connerton, Phage Biocontrol of Campylobacter jejuni in Chickens Does Not Produce Collateral Effects on the Gut Microbiota, Front. Microbiol. 10(2019) 476, doi: 10.3389/fmicb.2019.00476.

[101]

Z.D. Moye, J. Woolston, P.V.D. Abbeele, C. Duysburgh, L. Verstrepen, C.R. Das, M. Marzorati, A. Sulakvelidze, A Bacteriophage Cocktail Eliminates Salmonella Typhimurium from the Human Colonic Microbiome while Preserving Cytokine Signaling and Preventing Attachment to and Invasion of Human Cells by Salmonella In Vitro, J. Food Prot. 82(2019) 1336-1349, doi: 10.4315/0362-028X.JFP-18-587.

[102]

U. Dissanayake, M. Ukhanova, Z.D. Moye, A. Sulakvelidze, V. Mai, Bacteriophages Reduce Pathogenic Escherichia coli Counts in Mice Without Distorting Gut Microbiota, Front. Microbiol. 10(2019) 1984, doi: 10.3389/fmicb.2019.01984.

[103]

H. Bao, M. Pang, A. Olaniran, X. Zhang, H. Zhang, Y. Zhou, L. Sun, S. Schmidt, R. Wang, Alterations in the diversity and composition of mice gut microbiota by lytic or temperate gut phage treatment, Appl. Microbiol. Biotechnol. 102(2018) 10219-10230, doi: 10.1007/s00253-018-9378-6.

[104]

S.A. Sarker, B. Berger, Y. Deng, S. Kieser, F. Foata, D. Moine, P. Descombes, S. Sultana, S. Huq, P.K. Bardhan, V. Vuillet, F. Praplan, H. Brüssow, Oral application of E scherichia coli bacteriophage: safety tests in healthy and diarrheal children from B angladesh, Environ. Microbiol. 19(2017) 237-250, doi: 10.1111/1462-2920.13574.

[105]

S.A. Sarker, S. Sultana, G. Reuteler, D. Moine, P. Descombes, F. Charton, G. Bourdin, S. McCallin, C. Ngom-Bru, T. Neville, M. Akter, S. Huq, F. Qadri, K. Talukdar, M. Kassam, M. Delley, C. Loiseau, Y. Deng, S. El Aidy, B. Berger, H. Brüssow, Oral Phage Therapy of Acute Bacterial Diarrhea With Two Coliphage Preparations: A Randomized Trial in Children From Bangladesh, EBioMedicine 4(2016) 124-137, doi: 10.1016/j.ebiom.2015.12.023.

[106]

J.Y. Nale, J. Spencer, K.R. Hargreaves, A.M. Buckley, P. Trzepi ń ski, G.R. Douce, M.R.J. Clokie, Bacteriophage Combinations Significantly Reduce Clostridium difficile Growth In Vitro and Proliferation In Vivo, Antimicrob. Agents Chemother. 60(2016) 968-981, doi: 10.1128/AAC.01774-15.

[107]

V. Mai, M. Ukhanova, M.K. Reinhard, M. Li, A. Sulakvelidze, Bacteriophage administration significantly reduces Shigella colonization and shedding by Shigella -challenged mice without deleterious side effects and distortions in the gut microbiota, Bacteriophage 5(2015) e1088124, doi: 10.1080/21597081.2015.1088124.

[108]

J. Fa-arun, Y.W. Huan, E. Darmon, B. Wang, Tail-Engineered Phage P2 Enables Delivery of Antimicrobials into Multiple Gut Pathogens, ACS Synth. Biol. 12 (2023) 596-607, doi: 10.1021/acssynbio.2c00615.

[109]

K.N. Lam, P. Spanogiannopoulos, P. Soto-Perez, M. Alexander, M.J. Nalley, J.E. Bisanz, R.R. Nayak, A.M. Weakley, F.B. Yu, P.J. Turnbaugh, Phage-delivered CRISPR-Cas9 for strain-specific depletion and genomic deletions in the gut microbiome, Cell Rep 37 (2021) 109930, doi: 10.1016/j.celrep.2021.109930.

[110]

B.B. Hsu, J.C. Way, P.A. Silver, Stable Neutralization of a Virulence Factor in Bacteria Using Temperate Phage in the Mammalian Gut, mSystems 5(2020) e00013- e00020, doi: 10.1128/mSystems.00013-20.

[111]

A. Reyes, M. Wu, N.P. McNulty, F.L. Rohwer, J.I. Gordon, Gnotobiotic mouse model of phage-bacterial host dynamics in the human gut, Proc. Natl. Acad. Sci. 110(2013) 20236-20241, doi: 10.1073/pnas.1319470110.

[112]

B.B. Hsu, T.E. Gibson, V. Yeliseyev, Q. Liu, L. Lyon, L. Bry, P.A. Silver, G.K. Gerber, Dynamic Modulation of the Gut Microbiota and Metabolome by Bacteriophages in a Mouse Model, Cell Host Microbe 25 (2019) 803-814.e5, doi: 10.1016/j.chom.2019.05.001.

[113]

D. Wang, P.W.L. Tai, G. Gao, Adeno-associated virus vector as a platform for gene therapy delivery, Nat. Rev. Drug Discov. 18(2019) 358-378, doi: 10.1038/s41573-019-0012-9.

[114]

C. Ronda, S.P. Chen, V. Cabral, S.J. Yaung, H.H. Wang, Metagenomic engineering of the mammalian gut microbiome in situ, Nat. Methods 16(2019) 167-170, doi: 10.1038/s41592-018-0301-y.

[115]

R. Ghosh, M. De, Liposome-Based Antibacterial Delivery: An Emergent Approach to Combat Bacterial Infections, ACS Omega 8(2023) 35442-35451, doi: 10.1021/acsomega.3c04893.

[116]

D. Bikard, C.W. Euler, W. Jiang, P.M. Nussenzweig, G.W. Goldberg, X. Duportet, V.A. Fischetti, L.A. Marraffini, Exploiting CRISPR-Cas nucleases to produce sequence-specific antimicrobials, Nat. Biotechnol. 32(2014) 1146-1150, doi: 10.1038/nbt.3043.

[117]

B. Csörgő, L.M. León, I.J. Chau-Ly, A. Vasquez-Rifo, J.D. Berry, C. Mahendra, E.D. Crawford, J.D. Lewis, J. Bondy-Denomy, A compact Cascade-Cas3 system for targeted genome engineering, Nat. Methods 17 (2020) 1183-1190, doi: 10.1038/s41592-020-00980-w.

[118]

R. Yao, D. Liu, X. Jia, Y. Zheng, W. Liu, Y. Xiao, CRISPR-Cas9/Cas12a biotechnology and application in bacteria, Synth. Syst. Biotechnol. 3(2018) 135-149, doi: 10.1016/j.synbio.2018.09.004.

[119]

K.S. Pawelczak, N.S. Gavande, P.S. VanderVere-Carozza, J.J. Turchi, Modulating DNA Repair Pathways to Improve Precision Genome Engineering, ACS Chem. Biol. 13(2018) 389-396, doi: 10.1021/acschembio.7b00777.

[120]

Y. Liang, F. Chen, K. Wang, L. Lai, Base editors: development and applications in biomedicine, Front. Med. 17(2023) 359-387, doi: 10.1007/s11684-023-1013-y.

[121]

S.D. Rodrigues, M. Karimi, L. Impens, E. Van Lerberge, G. Coussens, S. Aesaert, D. Rombaut, D. Holtappels, H.M.M. Ibrahim, M. Van Montagu, J. Wagemans, T.B. Jacobs, B. De Coninck, L. Pauwels, Efficient CRISPR-mediated base editing in Agrobacterium spp, Proc. Natl. Acad. Sci. 118(2021) e2013338118, doi: 10.1073/pnas.2013338118.

[122]

D.C. Volke, R.A. Martino, E. Kozaeva, A.M. Smania, P.I. Nikel, Modular (de)construction of complex bacterial phenotypes by CRISPR/nCas9- assisted, multiplex cytidine base-editing, Nat. Commun. 13(2022) 3026, doi: 10.1038/s41467-022-30780-z.

[123]

Y. Wei, L.J. Feng, X.Z. Yuan, S.G. Wang, P.F. Xia, Developing a Base Editing System for Marine Roseobacter Clade Bacteria, ACS Synth. Biol. 12(2023) 2178-2186, doi: 10.1021/acssynbio.3c00259.

[124]

L. Zheng, J. Shen, R. Chen, Y. Hu, W. Zhao, E.L.H. Leung, L. Dai, Genome engineering of the human gut microbiome, J. Genet. Genomics (2024) S1673852724000031, doi: 10.1016/j.jgg.2024.01.002.

[125]

M. Mahler, A.R. Costa, S.P.B. Van Beljouw, P.C. Fineran, S.J.J. Brouns, Approaches for bacteriophage genome engineering, Trends Biotechnol 41(2023) 669-685, doi: 10.1016/j.tibtech.2022.08.008.

[126]

D.P. Pires, R. Monteiro, D. Mil-Homens, A. Fialho, T.K. Lu, J. Azeredo, Designing P. aeruginosa synthetic phages with reduced genomes, Sci. Rep. 11(2021) 2164, doi: 10.1038/s41598-021-81580-2.

[127]

E.M. Pulkkinen, T.C. Hinkley, S.R. Nugen, Utilizing in vitro DNA assembly to engineer a synthetic T7 Nanoluc reporter phage for Escherichia coli detection, Integr. Biol. 11 (2019) 63-68, doi: 10.1093/intbio/zyz005.

[128]

M.S. Faber, J.T. Van Leuven, M.M. Ederer, Y. Sapozhnikov, Z.L. Wilson, H.A. Wichman, T.A. Whitehead, C.R. Miller, Saturation Mutagenesis Genome Engineering of Infective ΦX174 Bacteriophage via Unamplified Oligo Pools and Golden Gate Assembly, ACS Synth. Biol. 9(2020) 125-131, doi: 10.1021/acssynbio.9b00411.

[129]

L. Cheng, Z. Deng, H. Tao, W. Song, B. Xing, W. Liu, L. Kong, S. Yuan, Y. Ma, Y. Wu, X. Huang, Y. Peng, N.K. Wong, Y. Liu, Y. Wang, Y. Shen, J. Li, M. Xiao, Harnessing stepping-stone hosts to engineer, select, and reboot synthetic bacteriophages in one pot, Cell Rep. Methods 2 (2022) 100217, doi: 10.1016/j.crmeth.2022.100217.

[130]

S. Kilcher, P. Studer, C. Muessner, J. Klumpp, M.J. Loessner, Cross-genus rebooting of custom-made, synthetic bacteriophage genomes in L-form bacteria, Proc. Natl. Acad. Sci. 115(2018) 567-572, doi: 10.1073/pnas.1714658115.

[131]

S. Yuan, J. Shi, J. Jiang, Y. Ma, Genome-scale top-down strategy to generate viable genome-reduced phages, Nucleic Acids Res 50(2022) 13183-13197, doi: 10.1093/nar/gkac1168.

[132]

P.J. Voorhees, C. Cruz-Teran, J. Edelstein, S.K. Lai, Challenges & opportunities for phage-based in situ microbiome engineering in the gut, J. Controlled Release 326(2020) 106-119, doi: 10.1016/j.jconrel.2020.06.016.

[133]

J.N. Chu, G. Traverso, Foundations of gastrointestinal-based drug delivery and future developments, Nat. Rev. Gastroenterol. Hepatol. 19(2022) 219-238, doi: 10.1038/s41575-021-00539-w.

[134]

N. Procházková, G. Falony, L.O. Dragsted, T.R. Licht, J. Raes, H.M. Roager, Advancing human gut microbiota research by considering gut transit time, Gut 72(2023) 180-191. https://doi.org/10.1136/gutjnl-2022-328166.

[135]

D. Shalon, R.N. Culver, J.A. Grembi, J. Folz, P.V. Treit, H. Shi, F.A. Rosenberger, L. Dethlefsen, X. Meng, E. Yaffe, A. Aranda-Díaz, P.E. Geyer, J.B. Mueller-Reif, S. Spencer, A.D. Patterson, G. Triadafilopoulos, S.P. Holmes, M. Mann, O. Fiehn, D.A. Relman, K.C. Huang, Profiling the human intestinal environment under physiological conditions, Nature 617(2023) 581-591, doi: 10.1038/s41586-023-05989-7.

[136]

M. Koziolek, M. Grimm, F. Schneider, P. Jedamzik, M. Sager, J.P. Kühn, W. Siegmund, W. Weitschies, Navigating the human gastrointestinal tract for oral drug delivery: Uncharted waters and new frontiers, Adv. Drug Deliv. Rev. 101(2016) 75-88, doi: 10.1016/j.addr.2016.03.009.

[137]

A.M. Vargason, A.C. Anselmo, S. Mitragotri, The evolution of commercial drug delivery technologies, Nat. Biomed. Eng. 5(2021) 951-967, doi: 10.1038/s41551-021-00698-w.

[138]

C.R. Merril, B. Biswas, R. Carlton, N.C. Jensen, G.J. Creed, S. Zullo, S. Adhya, Longcirculating bacteriophage as antibacterial agents., Proc. Natl. Acad. Sci. 93(1996) 3188-3192, doi: https://doi.org/10.1073/pnas.93.8.3188.

[139]

S.B.W. Liyanagedera, J. Williams, J.P. Wheatley, A.Y. Biketova, M. Hasan, A.P. Sagona, K.J. Purdy, R.J. Puxty, T. Feher, V. Kulkarni, SpyPhage: A Cell-Free TXTL Platform for Rapid Engineering of Targeted Phage Therapies, ACS Synth. Biol. 11(2022) 3330-3342, doi: https://doi.org/10.1021/acssynbio.2c00244.

[140]

M. Durán-Lobato, Z. Niu, M.J. Alonso, Oral Delivery of Biologics for Precision Medicine, Adv. Mater. 32(2020) 1901935, doi: 10.1002/adma.201901935.

[141]

Y. Yang, H. Du, G. Zou, Z. Song, Y. Zhou, H. Li, C. Tan, H. Chen, V.A. Fischetti, J. Li, Encapsulation and delivery of phage as a novel method for gut flora manipulation in situ: A review, J. Controlled Release 353(2023) 634-649, doi: 10.1016/j.jconrel.2022.11.048.

[142]

L. Meng, F. Yang, Y. Pang, Z. Cao, F. Wu, D. Yan, J. Liu, Nanocapping-enabled charge reversal generates cell-enterable endosomal-escapable bacteriophages for intracellular pathogen inhibition, Sci. Adv. 8 (2022) eabq2005, doi: 10.1126/sciadv.abq2005.

[143]

J.M. Andriolo, N.J. Sutton, J.P. Murphy, L.G. Huston, E.A. Kooistra-Manning, R.F. West, M.L. Pedulla, M.K. Hailer, J.L. Skinner, Electrospun Fibers for Controlled Release of Nanoparticle-Assisted Phage Therapy Treatment of Topical Wounds, MRS Adv 3(2018) 3019-3025, doi: 10.1557/adv.2018.483.

[144]

K. Richards, D.J. Malik, Microencapsulation of Bacteriophages Using Membrane Emulsification in Different pH-Triggered Controlled Release Formulations for Oral Administration, Pharmaceuticals 14(2021) 424, doi: 10.3390/ph14050424.

[145]

G.K. Vinner, K. Richards, M. Leppanen, A.P. Sagona, D.J. Malik, Microencapsulation of Enteric Bacteriophages in a pH-Responsive Solid Oral Dosage Formulation Using a Scalable Membrane Emulsification Process, Pharmaceutics 11(2019) 475, doi: 10.3390/pharmaceutics11090475.

[146]

J. Li, H. Zheng, S.S.Y. Leung, Investigating the effectiveness of liposomebacteriophage nanocomplex in killing Staphylococcus aureus using epithelial cell coculture models, Int. J. Pharm. 657 (2024) 124146, doi: 10.1016/j.ijpharm.2024.124146.

[147]

R. Międzybrodzki, M. K ł ak, E. Jończyk-Matysiak, B. Bubak, A. Wójcik, M. Kaszowska, B. Weber-D ąbrowska, M. Ł obocka, A. Górski, Means to Facilitate the Overcoming of Gastric Juice Barrier by a Therapeutic Staphylococcal Bacteriophage A5/80, Front. Microbiol. (2017) 08, doi: 10.3389/fmicb.2017.00467.

AI Summary AI Mindmap
PDF (3096KB)

401

Accesses

0

Citation

Detail

Sections
Recommended

AI思维导图

/