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Characterization and genomic analysis of a novel bacteriophage BUCT_49532 lysing Klebsiella pneumoniae

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Abstract

Bacteriophages are a type of virus widely distributed in nature that demonstrates a remarkable aptitude for selectively recognizing and infecting bacteria. In particular, Klebsiella pneumoniae is acknowledged as a clinical pathogen responsible for nosocomial infections and frequently develops multidrug resistance. Considering the increasing prevalence of antibiotic-resistant bacteria, bacteriophages have emerged as a compelling alternative therapeutic approach. In this study, a novel phage named BUCT_49532 was isolated from sewage using K. pneumoniae K1119 as the host. Electron microscopy revealed that BUCT_49532 belongs to the Caudoviricetes class. Further analysis through whole genome sequencing demonstrated that BUCT_49532 is a Jedunavirus comprised of linear double-stranded DNA with a length of 49,532 bp. Comparative genomics analysis based on average nucleotide identity (ANI) values revealed that BUCT_49532 should be identified as a novel species. Characterized by a good safety profile, high environmental stability, and strong lytic performance, phage BUCT_49532 presents an interesting case for consideration. Although its host range is relatively narrow, its application potential can be expanded by utilizing phage cocktails, making it a promising candidate for biocontrol approaches.

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Data availability

All data generated for this study is included in the article and supplement materials. The genome sequence data reported here are available in the GenBank database under accession number MZ374361.1.

References

  1. Latka A, Drulis-Kawa Z (2020) Advantages and limitations of microtiter biofilm assays in the model of antibiofilm activity of Klebsiella phage KP34 and its depolymerase. Sci Rep 10:20338. https://doi.org/10.1038/s41598-020-77198-5

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. V. Volozhantsev N, M. Shpirt A, I. Borzilov A, V. Komisarova E, M. Krasilnikova V, S. Shashkov A, V. Verevkin V, A. Knirel Y, (2020) Characterization and therapeutic potential of bacteriophage-encoded polysaccharide depolymerases with β galactosidase activity against Klebsiella pneumoniae K57 capsular type. Antibiotics 9:732. https://doi.org/10.3390/antibiotics9110732

    Article  CAS  PubMed  Google Scholar 

  3. Zurabov F, Zhilenkov E (2021) Characterization of four virulent Klebsiella pneumoniae bacteriophages, and evaluation of their potential use in complex phage preparation. Virol J 18:9. https://doi.org/10.1186/s12985-020-01485-w

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Turton JF, Perry C, Elgohari S, Hampton CV (2010) PCR characterization and typing of Klebsiella pneumoniae using capsular type-specific, variable number tandem repeat and virulence gene targets. J Med Microbiol 59:541–547. https://doi.org/10.1099/jmm.0.015198-0

    Article  CAS  PubMed  Google Scholar 

  5. Hsu C-R, Liao C-H, Lin T-L, Yang H-R, Yang F-L, Hsieh P-F, Wu S-H, Wang J-T (2016) Identification of a capsular variant and characterization of capsular acetylation in Klebsiella pneumoniae PLA-associated type K57. Sci Rep 6:31946. https://doi.org/10.1038/srep31946

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Townsend EM, Kelly L, Gannon L, Muscatt G, Dunstan R, Michniewski S, Sapkota H, Kiljunen SJ, Kolsi A, Skurnik M, Lithgow T, Millard AD, Jameson E (2021) Isolation and characterization of Klebsiella phages for phage therapy. PHAGE 2:26–42. https://doi.org/10.1089/phage.2020.0046

    Article  PubMed  PubMed Central  Google Scholar 

  7. Zhang C, Yuan J, Guo C, Ge C, Wang X, Wei D, Li X, Si H, Hu C (2021) Identification and complete genome of lytic “Kp34likevirus” phage vB_KpnP_Bp5 and therapeutic potency in the treatment of lethal Klebsiella pneumoniae infections in mice. Virus Res 297:198348. https://doi.org/10.1016/j.virusres.2021.198348

    Article  CAS  PubMed  Google Scholar 

  8. Kim MH, Lee HJ, Park KS, Suh JT (2010) Molecular characteristics of extended spectrum β-lactamases in Escherichia coli and Klebsiella pneumoniae and the prevalence of qnr in extended spectrum β-lactamase isolates in a Tertiary Care Hospital in Korea. Yonsei Med J 51:768. https://doi.org/10.3349/ymj.2010.51.5.768

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Park E-A, Kim Y-T, Cho J-H, Ryu S, Lee J-H (2017) Characterization and genome analysis of novel bacteriophages infecting the opportunistic human pathogens Klebsiella oxytoca and K. pneumoniae. Arch Virol 162:1129–1139. https://doi.org/10.1007/s00705-016-3202-3

    Article  CAS  PubMed  Google Scholar 

  10. Guo Y, Chen P, Lin Z, Wang T (2019) Characterization of two pseudomonas aeruginosa viruses vB_PaeM_SCUT-S1 and vB_PaeM_SCUT-S2. Viruses 11:318

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Tan D, Zhang Y, Cheng M, Le S, Gu J, Bao J, Qin J, Guo X, Zhu T (2019) Characterization of Klebsiella pneumoniae ST11 isolates and their interactions with lytic phages. Viruses 11:1080. https://doi.org/10.3390/v11111080

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Dunne M, Denyes JM, Arndt H, Loessner MJ, Leiman PG, Klumpp J (2018) Salmonella phage S16 tail fiber Adhesin features a rare polyglycine rich domain for host recognition. Structure 26:1573-1582.e4. https://doi.org/10.1016/j.str.2018.07.017

    Article  CAS  PubMed  Google Scholar 

  13. Dams D, Brøndsted L, Drulis-Kawa Z, Briers Y (2019) Engineering of receptor-binding proteins in bacteriophages and phage tail-like bacteriocins. Biochem Soc Trans 47:449–460. https://doi.org/10.1042/BST20180172

    Article  CAS  PubMed  Google Scholar 

  14. Kortright KE, Chan BK, Koff JL, Turner PE (2019) Phage therapy: a renewed approach to combat antibiotic-resistant bacteria. Cell Host Microbe 25:219–232. https://doi.org/10.1016/j.chom.2019.01.014

    Article  CAS  PubMed  Google Scholar 

  15. 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. Res Microbiol 168:194–207. https://doi.org/10.1016/j.resmic.2016.10.009

    Article  PubMed  Google Scholar 

  16. Hsieh P-F, Lin H-H, Lin T-L, Chen Y-Y, Wang J-T (2017) Two T7-like bacteriophages, K5–2 and K5–4, each encodes two capsule depolymerases: isolation and functional characterization. Sci Rep 7:4624. https://doi.org/10.1038/s41598-017-04644-2

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Wintachai P, Naknaen A, Thammaphet J, Pomwised R, Phaonakrop N, Roytrakul S, Smith DR (2020) Characterization of extended-spectrum-β-lactamase producing Klebsiella pneumoniae phage KP1801 and evaluation of therapeutic efficacy in vitro and in vivo. Sci Rep 10:11803. https://doi.org/10.1038/s41598-020-68702-y

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Cano EJ, Caflisch KM, Bollyky PL, Van Belleghem JD, Patel R, Fackler J, Brownstein MJ, Horne B, Biswas B, Henry M, Malagon F, Lewallen DG, Suh GA (2021) Phage therapy for limb-threatening prosthetic knee Klebsiella pneumoniae infection: case report and in vitro characterization of anti-biofilm activity. Clin Infect Dis 73:e144–e151. https://doi.org/10.1093/cid/ciaa705

    Article  PubMed  Google Scholar 

  19. Pan Y-J, Lin T-L, Chen C-C, Tsai Y-T, Cheng Y-H, Chen Y-Y, Hsieh P-F, Lin Y-T, Wang J-T (2017) Klebsiella phage ΦK64-1 encodes multiple depolymerases for multiple host capsular types. J Virol 91:e02457-e2516. https://doi.org/10.1128/JVI.02457-16

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Pu M, Han P, Zhang G, Liu Y, Li Y, Li F, Li M, An X, Song L, Chen Y, Fan H, Tong Y (2022) Characterization and comparative genomics analysis of a new bacteriophage BUCT610 against Klebsiella pneumoniae and efficacy assessment in galleria mellonella larvae. Int J Mol Sci 23:8040

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Zhao F, Sun H, Zhou X, Liu G, Li M, Wang C, Liu S, Zhuang Y, Tong Y, Ren H (2019) Characterization and genome analysis of a novel bacteriophage vB_SpuP_Spp16 that infects Salmonella enterica serovar pullorum. Virus Genes 55:532–540. https://doi.org/10.1007/s11262-019-01664-0

    Article  CAS  PubMed  Google Scholar 

  22. Domingo-Calap P, Beamud B, Mora-Quilis L, González-Candelas F, Sanjuán R (2020) Isolation and characterization of two Klebsiella pneumoniae phages encoding divergent depolymerases. IJMS 21:3160. https://doi.org/10.3390/ijms21093160

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Feng J, Gao L, Li L, Zhang Z, Wu C, Li F, Tong Y (2021) Characterization and genome analysis of novel Klebsiella phage BUCT556A with lytic activity against carbapenemase-producing Klebsiella pneumoniae. Virus Res 303:198506. https://doi.org/10.1016/j.virusres.2021.198506

    Article  CAS  PubMed  Google Scholar 

  24. Lu L, Cai L, Jiao N, Zhang R (2017) Isolation and characterization of the first phage infecting ecologically important marine bacteria Erythrobacter. Virol J 14:104. https://doi.org/10.1186/s12985-017-0773-x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Xing S, Ma T, Zhang X, Huang Y, Mi Z, Sun Q, An X, Fan H, Wu S, Wei L, Tong Y (2017) First complete genome sequence of a virulent bacteriophage infecting the opportunistic pathogen Serratia rubidaea. Arch Virol 162:2021–2028. https://doi.org/10.1007/s00705-017-3300-x

    Article  CAS  PubMed  Google Scholar 

  26. Han P, Hu Y, An X, Song L, Fan H, Tong Y (2021) Biochemical and genomic characterization of a novel bacteriophage BUCT555 lysing Stenotrophomonas maltophilia. Virus Res 301:198465. https://doi.org/10.1016/j.virusres.2021.198465

    Article  CAS  PubMed  Google Scholar 

  27. Madaha EL, Mienie C, Gonsu HK, Bughe RN, Fonkoua MC, Mbacham WF, Alayande KA, Bezuidenhout CC, Ateba CN (2020) Whole-genome sequence of multi-drug resistant Pseudomonas aeruginosa strains UY1PSABAL and UY1PSABAL2 isolated from human broncho-alveolar lavage, Yaoundé. Cameroon PLoS ONE 15:e0238390. https://doi.org/10.1371/journal.pone.0238390

    Article  CAS  PubMed  Google Scholar 

  28. Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M, Kulikov AS, Lesin VM, Nikolenko SI, Pham S, Prjibelski AD, Pyshkin AV, Sirotkin AV, Vyahhi N, Tesler G, Alekseyev MA, Pevzner PA (2012) SPAdes: A new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 19:455–477. https://doi.org/10.1089/cmb.2012.0021

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Overbeek R, Olson R, Pusch GD, Olsen GJ, Davis JJ, Disz T, Edwards RA, Gerdes S, Parrello B, Shukla M, Vonstein V, Wattam AR, Xia F, Stevens R (2014) The SEED and the Rapid Annotation of microbial genomes using Subsystems Technology (RAST). Nucl Acids Res 42:D206–D214. https://doi.org/10.1093/nar/gkt1226

    Article  CAS  PubMed  Google Scholar 

  30. Finn RD, Clements J, Eddy SR (2011) HMMER web server: interactive sequence similarity searching. Nucleic Acids Res 39:W29–W37. https://doi.org/10.1093/nar/gkr367

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Zimmermann L, Stephens A, Nam S-Z, Rau D, Kübler J, Lozajic M, Gabler F, Söding J, Lupas AN, Alva V (2018) A completely reimplemented MPI bioinformatics toolkit with a New HHpred server at its core. J Mol Biol 430:2237–2243. https://doi.org/10.1016/j.jmb.2017.12.007

    Article  CAS  PubMed  Google Scholar 

  32. Saier MH, Reddy VS, Moreno-Hagelsieb G, Hendargo KJ, Zhang Y, Iddamsetty V, Lam KJK, Tian N, Russum S, Wang J, Medrano-Soto A (2021) The transporter classification database (TCDB): 2021 update. Nucleic Acids Res 49:D461–D467. https://doi.org/10.1093/nar/gkaa1004

    Article  CAS  PubMed  Google Scholar 

  33. Chan PP, Lowe TM (2019) tRNAscan-SE: Searching for tRNA Genes in Genomic Sequences. In: Kollmar M (ed) Gene Prediction. Springer, New York, New York, NY, pp 1–14

    Google Scholar 

  34. Grant JR, Enns E, Marinier E, Mandal A, Herman EK, Chen C, Graham M, Van Domselaar G, Stothard P (2023) Proksee: in-depth characterization and visualization of bacterial genomes. Nucleic Acids Res 51:W484–W492. https://doi.org/10.1093/nar/gkad326

    Article  PubMed  PubMed Central  Google Scholar 

  35. Chen L (2004) VFDB: a reference database for bacterial virulence factors. Nucleic Acids Res 33:D325–D328. https://doi.org/10.1093/nar/gki008

    Article  CAS  PubMed Central  Google Scholar 

  36. McArthur AG, Waglechner N, Nizam F, Yan A, Azad MA, Baylay AJ, Bhullar K, Canova MJ, De Pascale G, Ejim L, Kalan L, King AM, Koteva K, Morar M, Mulvey MR, O’Brien JS, Pawlowski AC, Piddock LJV, Spanogiannopoulos P, Sutherland AD, Tang I, Taylor PL, Thaker M, Wang W, Yan M, Yu T, Wright GD (2013) The comprehensive antibiotic resistance database. Antimicrob Agents Chemother 57:3348–3357. https://doi.org/10.1128/AAC.00419-13

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Florensa AF, Kaas RS, Clausen PTLC, Aytan-Aktug D, Aarestrup FM (2022) ResFinder – an open online resource for identification of antimicrobial resistance genes in next-generation sequencing data and prediction of phenotypes from genotypes. Microbial Geno. https://doi.org/10.1099/mgen.0.000748

    Article  Google Scholar 

  38. Hallgren J, Tsirigos KD, Pedersen MD, Almagro Armenteros JJ, Marcatili P, Nielsen H, Krogh A, Winther O (2022) DeepTMHMM predicts alpha and beta transmembrane proteins using deep neural networks. Bioinformatics. https://doi.org/10.1101/2022.04.08.487609

    Article  Google Scholar 

  39. Teufel F, Almagro Armenteros JJ, Johansen AR, Gíslason MH, Pihl SI, Tsirigos KD, Winther O, Brunak S, von Heijne G, Nielsen H (2022) SignalP 6.0 predicts all five types of signal peptides using protein language models. Nat Biotechnol. https://doi.org/10.1038/s41587-021-01156-3

    Article  PubMed  PubMed Central  Google Scholar 

  40. Tynecki P, Guziński A, Kazimierczak J, Jadczuk M, Dastych J, Onisko A (2020) PhageAI—bacteriophage life cycle recognition with machine learning and natural language processing. Bioinformatics. https://doi.org/10.1101/2020.07.11.198606

    Article  Google Scholar 

  41. Sullivan MJ, Petty NK, Beatson SA (2011) Easyfig: a genome comparison visualizer. Bioinformatics 27:1009–1010. https://doi.org/10.1093/bioinformatics/btr039

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Darling ACE, Mau B, Blattner FR, Perna NT (2004) Mauve: multiple alignment of conserved genomic sequence with rearrangements. Genome Res 14:1394–1403. https://doi.org/10.1101/gr.2289704

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Robert X, Gouet P (2014) Deciphering key features in protein structures with the new ENDscript server. Nucleic Acids Res 42:W320–W324. https://doi.org/10.1093/nar/gku316

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Richter M, Rosselló-Móra R, Oliver Glöckner F, Peplies J (2016) JSpeciesWS: a web server for prokaryotic species circumscription based on pairwise genome comparison. Bioinformatics 32:929–931. https://doi.org/10.1093/bioinformatics/btv681

    Article  CAS  PubMed  Google Scholar 

  45. Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874. https://doi.org/10.1093/molbev/msw054

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Gao Y, Liu Q, Wang M, Zhao G, Jiang Y, Malin G, Gong Z, Meng X, Liu Z, Lin T, Li Y, Shao H (2017) Characterization and genome sequence of marine alteromonas gracilis phage PB15 isolated from the Yellow Sea, China. Curr Microbiol 74:821–826. https://doi.org/10.1007/s00284-017-1251-9

    Article  CAS  PubMed  Google Scholar 

  47. Kyrkou I, Carstens AB, Ellegaard-Jensen L, Kot W, Zervas A, Djurhuus AM, Neve H, Franz CMAP, Hansen M, Hansen LH (2020) Isolation and characterisation of novel phages infecting Lactobacillus plantarum and proposal of a new genus, “Silenusvirus.” Sci Rep 10:8763. https://doi.org/10.1038/s41598-020-65366-6

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Gao M, Yi L, Wang Y, Gao J, Liu H, Zhang X, Pei G, Tong Y, Bai C (2022) Characterization and genomic analysis of bacteriophage vB_KpnM_IME346 targeting clinical Klebsiella pneumoniae strain of the K63 capsular type. Curr Microbiol 79:160. https://doi.org/10.1007/s00284-022-02834-4

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Shi Y, Yan Y, Ji W, Du B, Meng X, Wang H, Sun J (2012) Characterization and determination of holin protein of Streptococcus suis bacteriophage SMP in heterologous host. Virol J 9:70. https://doi.org/10.1186/1743-422X-9-70

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Reddy BL, Saier MH (2013) Topological and phylogenetic analyses of bacterial holin families and superfamilies. Biochimica et Biophysica Acta (BBA) Biomembranes 1828:2654–2671

    Article  CAS  PubMed  Google Scholar 

  51. Adamczyk-Popławska M, Tracz-Gaszewska Z, Lasota P, Kwiatek A, Piekarowicz A (2020) Haemophilus influenzae HP1 bacteriophage encodes a lytic cassette with a pinholin and a signal-arrest-release endolysin. IJMS 21:4013. https://doi.org/10.3390/ijms21114013

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Cahill J, Young R (2019) Phage Lysis: Multiple Genes for Multiple Barriers. In: Advances in Virus Research. Elsevier, pp 33–70

  53. Kongari R, Rajaure M, Cahill J, Rasche E, Mijalis E, Berry J, Young R (2018) Phage spanins: diversity, topological dynamics and gene convergence. BMC Bioinformatics 19:326. https://doi.org/10.1186/s12859-018-2342-8

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Loh B, Zhang L, Hua X, Yu Y, Ma L, Wang X, Manohar P, Nachimuthu R, Martins WMBS, Toleman MA, Leptihn S (2021) Complete genome sequence of the virulent Klebsiella pneumoniae phage geezett infecting multidrug-resistant clinical strains. Microbiol Resour Announc 10:e00685-e721. https://doi.org/10.1128/MRA.00685-21

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Peng W, Zeng F, Wu Z, Jin Z, Li W, Zhu M, Wang Q, Tong Y, Chen L, Bai Q (2022) Isolation and genomic analysis of temperate phage 5W targeting multidrug-resistant Acinetobacter baumannii. Arch Microbiol 204:58. https://doi.org/10.1007/s00203-021-02618-7

    Article  CAS  Google Scholar 

  56. Pires DP, Oliveira H, Melo LDR, Sillankorva S, Azeredo J (2016) Bacteriophage-encoded depolymerases: their diversity and biotechnological applications. Appl Microbiol Biotechnol 100:2141

    Article  CAS  PubMed  Google Scholar 

  57. Gatea Kaabi SA, Musafer HK (2020) New Phage cocktail against infantile Sepsis bacteria. Microb Pathog 148:104447. https://doi.org/10.1016/j.micpath.2020.104447

    Article  CAS  PubMed  Google Scholar 

  58. Kim S-G, Lee S-B, Jo S-J, Cho K, Park J-K, Kwon J, Giri SS, Kim S-W, Kang J-W, Jung W-J, Lee Y-M, Roh E, Park S-C (2022) Phage cocktail in combination with Kasugamycin as a potential treatment for fire blight caused by Erwinia amylovora. Antibiotics 11:1566. https://doi.org/10.3390/antibiotics11111566

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Rydman PS, Bamford DH (2002) The lytic enzyme of bacteriophage PRD1 is associated with the viral membrane. J BACTERIOL 184:7

    Article  Google Scholar 

  60. Ragab S, Gouda SM, Abdelmoteleb M (2023) El-Shibiny A (2023) The role of identified and characterized bacteriophage ZCEC13 in controlling pathogenic and multidrug-resistant Escherichia coli in wastewater: in vitro study. Environ Technol. https://doi.org/10.1080/09593330.2023.2220886

    Article  PubMed  Google Scholar 

  61. Peng Q, Ma Z, Han Q, Xiang F, Wang L, Zhang Y, Zhao Y, Li J, Xian Y, Yuan Y (2023) Characterization of bacteriophage vB_KleM_KB2 possessing high control ability to pathogenic Klebsiella pneumoniae. Sci Rep 13:9815. https://doi.org/10.1038/s41598-023-37065-5

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Caldeira JC, Peabody DS (2007) Stability and assembly in vitro of bacteriophage PP7 virus-like particles. J Nanobiotechnol 5:10

    Article  Google Scholar 

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Acknowledgements

We are very grateful to Pengjun Han for his instruction in sequencing and depositing the phage genomes.

Funding

This study was funded by Key Research and Development Program of Hebei Province (22322908D), China Postdoctoral Science Foundation (2022M710330), Special Research Project on Education of Beijing University of Chemical Technology (2021BHDJGZD05) and Mechanism Construction and Practice of Collaboration on Innovation-entrepreneurship and Labor Education under the Background of New Engineering (2022).

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  1. Guangye Zhang and Yucong Liu have contributed equally to this study.

Authors and Affiliations

  1. College of Life Science and Technology, Beijing University of Chemical Technology, Beijing, 100029, China

    Guangye Zhang, Yucong Liu, Jinhong Wang, Nan Li, Pengjun Han, Yiming Chen, Weijian Xu & Changxia Liu

  2. State Key Laboratory of Biocontrol, School of Ecology, Sun Yat-Sen University, Guangzhou, 510275, China

    Yucong Liu

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All authors contributed to the study’s conception and design. Material preparation, data collection, and analysis were performed by Guangye Zhang, Yucong Liu, Jinhong Wang, and Nan Li. The first draft of the manuscript was written by Guangye Zhang and Yucong Liu. All authors commented on previous versions of the manuscript and made some revisions. All authors read and approved the final manuscript.

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Zhang, G., Liu, Y., Wang, J. et al. Characterization and genomic analysis of a novel bacteriophage BUCT_49532 lysing Klebsiella pneumoniae. Virus Genes 59, 852–867 (2023). https://doi.org/10.1007/s11262-023-02033-8

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