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Isolation and characterization of a novel temperate bacteriophage from gut-associated Escherichia within black soldier fly larvae (Hermetia illucens L. [Diptera: Stratiomyidae])

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Abstract

To gain insight into the presence and nature of prophages in the black soldier fly (BSF; Hermetia illucens L. [Diptera: Stratiomyidae]) gut, we isolated and characterized a novel, temperate Escherichia bacteriophage designated vB_EcoS_PHB10 (PHB10). Electron microscopy analysis revealed that phage PHB10 has a long, flexible, non-contractile tail and belongs to the family Siphoviridae. The phage was found to be stable over a wide range of temperatures (4–37 °C) and pH values (pH 5–9), and it lysed two out of 13 Escherichia strains tested. The genome of PHB10 contains genes encoding a putative transcriptional regulator and an integrase, and it shows a high degree of similarity to a region of the Enterobacter cloacae MBRL1077 genome. Induction experiments revealed that phage PHB10 could be induced by different gut substrates, suggesting that diet might be a potential regulator of lytic/lysogenic switches in commensal lysogens.

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References

  1. Meneguz M, Gasco L, Tomberlin JK (2018) Impact of pH and feeding system on black soldier fly (Hermetia illucens, L; Diptera: Stratiomyidae) larval development. PLoS One 13(8):e0202591

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Čičková H, Newton GL, Lacy RC, Kozánek M (2015) The use of fly larvae for organic waste treatment. Waste Manag 35:68–80

    Article  CAS  PubMed  Google Scholar 

  3. Nguyen TT, Tomberlin JK, Vanlaerhoven S (2015) Ability of black soldier fly (Diptera: Stratiomyidae) larvae to recycle food waste. Environ Entomol 44:406–410

    Article  CAS  PubMed  Google Scholar 

  4. Jeon H, Park S, Choi J, Jeong G, Lee SB, Choi Y, Lee SJ (2011) The intestinal bacterial community in the food waste-reducing larvae of Hermetia illucens. Curr Microbiol 62:1390–1399

    Article  CAS  PubMed  Google Scholar 

  5. Lalander C, Senecal J, Gros Calvo M, Ahrens L, Josefsson S, Wiberg K, Vinnerås B (2016) Fate of pharmaceuticals and pesticides in fly larvae composting. Sci Total Environ 15(565):279–286

    Article  CAS  Google Scholar 

  6. Wommack KE, Colwell RR (2000) Virioplankton: viruses in aquatic ecosystems. Microbiol Mol Biol Rev 64:69–114

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Brüssow H, Hendrix RW (2002) Phage genomics: small is beautiful. Cell 108:13–16

    Article  PubMed  Google Scholar 

  8. Comeau AM, Hatfull GF, Krisch HM, Lindell D, Mann NH, Prangishvili D (2008) Exploring the prokaryotic virosphere. Res Microbiol 159:306–313

    Article  CAS  PubMed  Google Scholar 

  9. Hatoum-Aslan A (2018) Phage genetic engineering using CRISPR-Cas systems. Viruses 10(6):E335

    Article  CAS  PubMed  Google Scholar 

  10. Tao P, Wu X, Rao V (2018) Unexpected evolutionary benefit to phages imparted by bacterial CRISPR-Cas9. Sci Adv 4:eaar4134

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Mirzaei MK, Maurice CF (2017) Ménage à trois in the human gut: interactions between host, bacteria and phages. Nat Rev Microbiol 15:397–408

    Article  CAS  PubMed  Google Scholar 

  12. Minot S, Sinha R, Chen J, Li H, Keilbaugh SA, Wu GD, Lewis JD, Bushman FD (2011) The human gut virome: inter-individual variation and dynamic response to diet. Genome Res 21:1616–1625

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Reyes A, Haynes M, Hanson N, Angly FE, Heath AC, Rohwer F, Gordon JI (2010) Viruses in the faecal microbiota of monozygotic twins and their mothers. Nature 466:334–338

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Spranghers T, Ottoboni M, Klootwijk C, Ovyn A, Deboosere S, De Meulenaer B, Michiels J, Eeckhout M, De Clercq P, De Smet S (2017) Nutritional composition of black soldier fly (Hermetia illucens) prepupae reared on different organic waste substrates. J Sci Food Agric 97:2594–2600

    Article  CAS  PubMed  Google Scholar 

  15. Zhou F, Tomberlin JK, Zheng L, Yu Z, Zhang J (2013) Developmental and waste reduction plasticity of three black soldier fly strains (Diptera: Stratiomyidae) raised on different livestock manures. J Med Entomol 50:1224–1230

    Article  PubMed  Google Scholar 

  16. Ma J, Lei Y, Rehman KU, Yu Z, Zhang J, Li W, Li Q, Tomberlin JK, Zheng L (2018) Dynamic effects of initial pH of substrate on biological growth and metamorphosis of black soldier fly (Diptera: Stratiomyidae). Environ Entomol 47:159–165

    Article  PubMed  Google Scholar 

  17. Adams MH (1959) Bacteriophages. Wiley, New York

    Google Scholar 

  18. Chen Y, Sun E, Song J, Tong Y, Wu B (2018) Three Salmonella enterica serovar Enteritidis bacteriophages from the Siphoviridae family are promising candidates for phage therapy. Can J Microbiol 64:865–875

    Article  CAS  PubMed  Google Scholar 

  19. Thomas JA, Hardies SC, Rolando M, Hayes SJ, Lieman K, Carroll CA, Weintraub ST, Serwer P (2007) Complete genomic sequence and mass spectrometric analysis of highly diverse, atypical Bacillus thuringiensis phage 0305phi8-36. Virology 368:405–421

    Article  CAS  PubMed  Google Scholar 

  20. Chen Y, Yang L, Sun E, Song J, Wu B (2018) Characterisation of a newly detected bacteriophage infecting Bordetella bronchiseptica in swine. Arch Virol 164:33–40

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Li S, Fan H, An X, Fan H, Jiang H, Chen Y, Tong Y (2014) Scrutinizing virus genome termini by high-through put sequencing. PLoS One 9:e85806

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Sullivan MJ, Petty NK, Beatson SA (2011) Easyfig: a genome comparison visualizer. Bioinformatics 27:1009–1010

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Li W, Li Q, Wang Y, Zheng L, Zhang Y, Yu Z, Chen H, Zhang J (2018) Efficient bioconversion of organic wastes to value-added chemicals by soaking, black soldier fly (Hermetia illucens L.) and anaerobic fermentation. J Environ Manag 227:267–276

    Article  CAS  Google Scholar 

  25. Erickson MC, Islam M, Sheppard C, Liao J, Doyle MP (2004) Reduction of Escherichia coli O157:H7 and Salmonella enterica serovar Enteritidis in chicken manure by larvae of the black soldier fly. J Food Prot 67:685–690

    Article  PubMed  Google Scholar 

  26. Liu Q, Tomberlin JK, Brady JA, Sanford MR, Yu Z (2008) Black soldier fly (Diptera: Stratiomyidae) larvae reduce Escherichia coli in dairy manure. Environ Entomol 37:1525–1530

    Article  PubMed  Google Scholar 

  27. Yoshida M, Yoshida-Takashima Y, Nunoura T, Takai K (2015) Genomic characterization of a temperate phage of the psychrotolerant deep-sea bacterium Aurantimonas sp. Extremophiles 19:49–58

    Article  CAS  PubMed  Google Scholar 

  28. Kropinski AM, Waddell T, Meng J, Franklin K, Ackermann HW, Ahmed R, Mazzocco A, Yates J 3rd, Lingohr EJ, Johnson RP (2013) The host-range, genomics and proteomics of Escherichia coli O157:H7 bacteriophage rV5. Virol J 10:76. https://doi.org/10.1186/1743-422X-10-76

    Article  PubMed  PubMed Central  Google Scholar 

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Authors and Affiliations

  1. State Key laboratory of Agricultural Microbiology, College of Veterinary Medicine, Huazhong Agricultural University, Wuhan, 430070, Hubei, China

    Yibao Chen, Xiangmin Li, Jiaoyang Song, Dan Yang, Wenqiang Liu, Huanchun Chen, Bin Wu & Ping Qian

  2. The Cooperative Innovation Center for Sustainable Pig Production, Huazhong Agricultural University, Wuhan, 430070, Hubei, China

    Yibao Chen, Xiangmin Li, Jiaoyang Song, Dan Yang, Wenqiang Liu, Huanchun Chen, Bin Wu & Ping Qian

Authors
  1. Yibao Chen
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  2. Xiangmin Li
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  3. Jiaoyang Song
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  4. Dan Yang
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  5. Wenqiang Liu
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  6. Huanchun Chen
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  7. Bin Wu
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  8. Ping Qian
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Contributions

Y. Chen drafted the manuscript. Y. Chen, X. Li and P. Qian performed the data analysis; Y. Chen, J. Song, D. Yang and W. Liu planned and performed experiments; P. Qian, B. Wu and H. Chen were responsible for experimental design. All authors reviewed and agreed the publication of this manuscript.

Corresponding author

Correspondence to Ping Qian.

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Funding

This work was supported by grants from the National Program on Key Research Project of China (no. 2018YFD0500204) and the Fundamental Research Funds for the Central Universities (2662016PY004).

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This article does not contain any studies with human participants or animals performed by any of the authors. I would like to declare on behalf of my co-authors that we have no conflict of interest.

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Chen, Y., Li, X., Song, J. et al. Isolation and characterization of a novel temperate bacteriophage from gut-associated Escherichia within black soldier fly larvae (Hermetia illucens L. [Diptera: Stratiomyidae]). Arch Virol 164, 2277–2284 (2019). https://doi.org/10.1007/s00705-019-04322-w

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  • DOI: https://doi.org/10.1007/s00705-019-04322-w

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