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Isolation and characterization of the novel bacteriophage vB_SmaS_BUCT626 against Stenotrophomonas maltophilia

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Abstract

Stenotrophomonas maltophilia has been recognized as an emerging global opportunistic pathogen, and it is intrinsically resistant to most antibiotics, which makes the limited choice for treating S. maltophilia infections. Bacteriophage with the proper characterization is considered as a promising alternative treatment option to control S. maltophilia infections. In this study, we isolated a novel Siphoviridae bacteriophage vB_SmaS_BUCT626 with lytic activity against S. maltophilia. Phage vB_SmaS_BUCT626 can lysis 10 of 20 S. maltophilia and was relatively stable at a wide range of temperatures (4–70 °C) and pH values (3.0–13.0) and exhibited good tolerance to chloroform. The genome of phage vB_SmaS_BUCT626 was a 61,662-bp linear double-stranded DNA molecule with a GC content of 56.2%, and contained 100 open-reading frames. It carried no antibiotic resistance, toxin, virulence-related genes, or lysogen-formation gene clusters. Together, these characteristics make phage vB_SmaS_BUCT626, a viable candidate as a biocontrol agent against S. maltophilia infection.

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References

  1. Brooke JS (2012) Stenotrophomonas maltophilia: an emerging global opportunistic pathogen. Clin Microbiol Rev 25:2–41. https://doi.org/10.1128/cmr.00019-11

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Baumrin E, Piette EW, Micheletti RG (2017) Stenotrophomonas maltophilia: an emerging multidrug-resistant opportunistic pathogen in the immunocompromised host. BMJ Case Rep. https://doi.org/10.1136/bcr-2017-221053

    Article  PubMed  PubMed Central  Google Scholar 

  3. Jeon YD, Jeong WY, Kim MH, Jung IY, Ahn MY, Ann HW, Ahn JY, Han SH, Choi JY, Song YG, Kim JM, Ku NS (2016) Risk factors for mortality in patients with Stenotrophomonas maltophilia bacteremia. Medicine 95:e4375. https://doi.org/10.1097/md.0000000000004375

    Article  PubMed  PubMed Central  Google Scholar 

  4. Gil-Gil T, Martínez JL, Blanco P (2020) Mechanisms of antimicrobial resistance in Stenotrophomonas maltophilia: a review of current knowledge. Expert Rev Anti Infect Ther 18:335–347. https://doi.org/10.1080/14787210.2020.1730178

    Article  CAS  PubMed  Google Scholar 

  5. Keen EC (2015) A century of phage research: bacteriophages and the shaping of modern biology. BioEssays : news and reviews in molecular, cellular and developmental biology 37:6–9. https://doi.org/10.1002/bies.201400152

    Article  Google Scholar 

  6. McCutcheon JG, Dennis JJ (2021) The potential of phage therapy against the emerging opportunistic pathogen stenotrophomonas maltophilia. Viruses. https://doi.org/10.3390/v13061057

    Article  PubMed  PubMed Central  Google Scholar 

  7. Chang HC, Chen CR, Lin JW, Shen GH, Chang KM, Tseng YH, Weng SF (2005) Isolation and characterization of novel giant Stenotrophomonas maltophilia phage phiSMA5. Appl Environ Microbiol 71:1387–1393. https://doi.org/10.1128/aem.71.3.1387-1393.2005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Chen CR, Lin CH, Lin JW, Chang CI, Tseng YH, Weng SF (2007) Characterization of a novel T4-type Stenotrophomonas maltophilia virulent phage Smp14. Arch Microbiol 188:191–197. https://doi.org/10.1007/s00203-007-0238-5

    Article  CAS  PubMed  Google Scholar 

  9. García P, Monjardín C, Martín R, Madera C, Soberón N, Garcia E, Meana A, Suárez JE (2008) Isolation of new Stenotrophomonas bacteriophages and genomic characterization of temperate phage S1. Appl Environ Microbiol 74:7552–7560. https://doi.org/10.1128/aem.01709-08

    Article  PubMed  PubMed Central  Google Scholar 

  10. Fan H, Huang Y, Mi Z, Yin X, Wang L, Fan H, Zhang Z, An X, Chen J, Tong Y (2012) Complete genome sequence of IME13, a Stenotrophomonas maltophilia bacteriophage with large burst size and unique plaque polymorphism. J Virol 86:11392–11393. https://doi.org/10.1128/jvi.01908-12

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Huang Y, Fan H, Pei G, Fan H, Zhang Z, An X, Mi Z, Shi T, Tong Y (2012) Complete genome sequence of IME15, the first T7-like bacteriophage lytic to pan-antibiotic-resistant Stenotrophomonas maltophilia. J Virol 86:13839–13840. https://doi.org/10.1128/jvi.02661-12

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Peters DL, Lynch KH, Stothard P, Dennis JJ (2015) The isolation and characterization of two Stenotrophomonas maltophilia bacteriophages capable of cross-taxonomic order infectivity. BMC Genomics 16:664. https://doi.org/10.1186/s12864-015-1848-y

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Peters DL, Stothard P, Dennis JJ (2017) The isolation and characterization of Stenotrophomonas maltophilia T4-like bacteriophage DLP6. PLoS ONE 12:e0173341. https://doi.org/10.1371/journal.pone.0173341

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. McCutcheon JG, Lin A, Dennis JJ (2020) Isolation and characterization of the novel bacteriophage AXL3 against Stenotrophomonas maltophilia. Int J Mol Sci. https://doi.org/10.3390/ijms21176338

    Article  PubMed  PubMed Central  Google Scholar 

  15. Frank JA, Reich CI, Sharma S, Weisbaum JS, Wilson BA, Olsen GJ (2008) Critical evaluation of two primers commonly used for amplification of bacterial 16S rRNA genes. Appl Environ Microbiol 74:2461–2470. https://doi.org/10.1128/aem.02272-07

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Kaiser S, Biehler K, Jonas D (2009) A Stenotrophomonas maltophilia multilocus sequence typing scheme for inferring population structure. J Bacteriol 191:2934–2943. https://doi.org/10.1128/jb.00892-08

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. 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 

  18. Zhang W, Zhang R, Hu Y, Liu Y, Wang L, An X, Song L, Shi T, Fan H, Tong Y, Liu H (2021) Biological characteristics and genomic analysis of a Stenotrophomonas maltophilia phage vB_SmaS_BUCT548. Virus Genes 57:205–216. https://doi.org/10.1007/s11262-020-01818-5

    Article  CAS  PubMed  Google Scholar 

  19. Li F, Xing S, Fu K, Zhao S, Liu J, Tong Y, Zhou L (2019) Genomic and biological characterization of the Vibrio alginolyticus-infecting “Podoviridae” bacteriophage, vB_ValP_IME271. Virus Genes 55:218–226. https://doi.org/10.1007/s11262-018-1622-8

    Article  CAS  PubMed  Google Scholar 

  20. Aziz RK, Bartels D, Best AA, DeJongh M, Disz T, Edwards RA, Formsma K, Gerdes S, Glass EM, Kubal M, Meyer F, Olsen GJ, Olson R, Osterman AL, Overbeek RA, McNeil LK, Paarmann D, Paczian T, Parrello B, Pusch GD, Reich C, Stevens R, Vassieva O, Vonstein V, Wilke A, Zagnitko O (2008) The RAST server: rapid annotations using subsystems technology. BMC Genomics 9:75. https://doi.org/10.1186/1471-2164-9-75

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Bateman A et al (2021) UniProt: the universal protein knowledgebase in 2021. Nucleic acids research 49:D480–D489. https://doi.org/10.1093/nar/gkaa1100

    Article  CAS  Google Scholar 

  22. Lowe TM, Chan PP (2016) tRNAscan-SE On-line: integrating search and context for analysis of transfer RNA genes. Nucleic Acids Res 44:W54-57. https://doi.org/10.1093/nar/gkw413

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797. https://doi.org/10.1093/nar/gkh340

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Alikhan NF, Petty NK, Ben Zakour NL, Beatson SA (2011) BLAST Ring Image Generator (BRIG): simple prokaryote genome comparisons. BMC Genomics 12:402. https://doi.org/10.1186/1471-2164-12-402

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. 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 

  26. Feiss M, Rao VB (2012) The bacteriophage DNA packaging machine. Adv Exp Med Biol 726:489–509. https://doi.org/10.1007/978-1-4614-0980-9_22

    Article  CAS  PubMed  Google Scholar 

  27. Rao VB, Feiss M (2015) Mechanisms of DNA packaging by large double-stranded DNA viruses. Annual review of virology 2:351–378. https://doi.org/10.1146/annurev-virology-100114-055212

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Weiditch SA, Seraphim TV, Houry WA, Kanelis V (2019) Strategies for purification of the bacteriophage HK97 small and large terminase subunits that yield pure and homogeneous samples that are functional. Protein Expr Purif 160:45–55. https://doi.org/10.1016/j.pep.2019.03.017

    Article  CAS  PubMed  Google Scholar 

  29. Cahill J, Young R (2019) Phage lysis: multiple genes for multiple barriers. Adv Virus Res 103:33–70. https://doi.org/10.1016/bs.aivir.2018.09.003

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

This work was supported by the National Natural Science Foundation of China (82002207), the Natural Science Foundation of Shanxi Province (201901D211136), Shanxi Province Science Foundation for Youths (201801D221285), National Key Research and Development Program of China (2018YFA0903000), and Technology Research and Development Program of Taian (2018NS0140).

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Author notes

  1. Fei Li, Lingxing Li, and Yong Zhang have contributed equally to this work.

Authors and Affiliations

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

    Fei Li & Yigang Tong

  2. Taian City Central Hospital, Taian, 271000, China

    Fei Li, Lingxing Li, Yong Zhang, Shiyu Bai, Jingli Guan & Wangmeng Zhang

  3. Institutes of Biomedical Sciences, Shanxi University, Taiyuan, 030006, China

    Li Sun, Xiaogang Cui & Jiao Feng

Authors
  1. Fei Li
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  2. Lingxing Li
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  3. Yong Zhang
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  4. Shiyu Bai
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  5. Li Sun
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Contributions

YT, JF, XC, and WZ conceived and designed experiments and critically evaluated the manuscript. FL, LL, YZ, and JF drafted the manuscript, LF extracted the phage nucleotide and conducted the sequencing experiments. FL and YZ isolated and identified the phage and conducted the biological characterization experiments. SB, LS, and JG were involved in the phage bio-informatics analysis. However, the sequence submission author FT was not part of the work. All authors checked and reviewed the manuscript.

Corresponding authors

Correspondence to Wangmeng Zhang, Xiaogang Cui, Jiao Feng or Yigang Tong.

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Edited by Andrew Millard.

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Li, F., Li, L., Zhang, Y. et al. Isolation and characterization of the novel bacteriophage vB_SmaS_BUCT626 against Stenotrophomonas maltophilia. Virus Genes 58, 458–466 (2022). https://doi.org/10.1007/s11262-022-01917-5

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  • DOI: https://doi.org/10.1007/s11262-022-01917-5

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