Bacteriophages for detection and control of foodborne bacterial pathogens—The case of Bacillus cereus and their phages
Haftom Baraki Abraha
Department of Food Science and Technology, Jeonbuk National University, Jeonju, Republic of Korea
Search for more papers by this authorKwang-Pyo Kim
Department of Food Science and Technology, Jeonbuk National University, Jeonju, Republic of Korea
Department of Agricultural Convergence Technology, Collage of Agriculture and Life Sciences, Jeonbuk National University, Jeonju, Republic of Korea
Search for more papers by this authorCorresponding Author
Desta Berhe Sbhatu
Department of Biological and Chemical Engineering, Mekelle Institute of Technology, Mekelle University, Mekelle, Ethiopia
Correspondence
Desta Berhe Sbhatu, Department of Biological and Chemical Engineering, Mekelle Institute of Technology, Mekelle University, PO Box 1632, Mekelle, Ethiopia.
Email: [email protected]
Search for more papers by this authorHaftom Baraki Abraha
Department of Food Science and Technology, Jeonbuk National University, Jeonju, Republic of Korea
Search for more papers by this authorKwang-Pyo Kim
Department of Food Science and Technology, Jeonbuk National University, Jeonju, Republic of Korea
Department of Agricultural Convergence Technology, Collage of Agriculture and Life Sciences, Jeonbuk National University, Jeonju, Republic of Korea
Search for more papers by this authorCorresponding Author
Desta Berhe Sbhatu
Department of Biological and Chemical Engineering, Mekelle Institute of Technology, Mekelle University, Mekelle, Ethiopia
Correspondence
Desta Berhe Sbhatu, Department of Biological and Chemical Engineering, Mekelle Institute of Technology, Mekelle University, PO Box 1632, Mekelle, Ethiopia.
Email: [email protected]
Search for more papers by this authorAbstract
Bacillus cereus is among the primary food-poisoning pathogenic bacterium that causes diarrhea and emetic types of diseases throughout the world. Recent advances show that bacteriophages become important tools in detection and control of foodborne bacterial pathogens in foods. They gain the interest of researchers for the food industries mainly because they are host-specific and harmless to humans. Studies showed that bacteriophages could be employed as natural or engineered, whole or part, and temperate or virulent type in designing a range of tools for the detection and control of foodborne bacterial pathogens. This article discusses the recent methods and advances in the utilization strategies of bacteriophages in detection and control of foodborne pathogens, with particular focus on B. cereus pathogen. Moreover, the article presents the latest and relevant information of B. cereus-infecting phages with respect to their potential applications in foods to address food safety issues. It also reflects future research directions by indicating gap of studies on the area.
CONFLICT OF INTEREST
The authors declare no conflict of interest.
Open Research
DATA AVAILABILITY STATEMENT
The data that support the findings of this study are available from the first author upon reasonable request.
REFERENCES
- Ackermann, H.-W. (1998). Tailed bacteriophages: The order Caudovirales. In Advances in Virus Research (Vol. 51, pp. 135–201). Canada: Elsevier.
- Arora, P., Sindhu, A., Dilbaghi, N., & Chaudhury, A. (2011). Biosensors as innovative tools for the detection of food borne pathogens. Biosensors and Bioelectronics, 28(1), 1–12. https://doi.org/10.1016/j.bios.2011.06.002
- Asare, P. T., Ryu, S., & Kim, K.-P. (2015). Complete genome sequence and phylogenetic position of the Bacillus cereus group phage JBP901. Archives of Virology, 160(9), 2381–2384. https://doi.org/10.1007/s00705-015-2485-0
- Bai, J., Kim, Y.-T., Ryu, S., & Lee, J.-H. (2016). Biocontrol and rapid detection of food-borne pathogens using bacteriophages and endolysins. Frontiers in Microbiology, 7, 474. https://doi.org/10.3389/fmicb.2016.00474
- Bandara, N., Jo, J., Ryu, S., & Kim, K.-P. (2012). Bacteriophages BCP1-1 and BCP8-2 require divalent cations for efficient control of Bacillus cereus in fermented foods. Food Microbiology, 31(1), 9–16. https://doi.org/10.1016/j.fm.2012.02.003
- Barylski, J., Enault, F., Dutilh, B. E., Schuller, M. B., Edwards, R. A., Gillis, A., & Kuhn, J. H. (2020). Analysis of spounaviruses as a case study for the overdue reclassification of tailed phages. Systematic Biology, 69(1), 110–123. https://doi.org/10.1093/sysbio/syz036
- Bennett, S. D., Walsh, K. A., & Gould, L. H. (2013). Foodborne disease outbreaks caused by Bacillus cereus, Clostridium perfringens, and Staphylococcus aureus—United States, 1998–2008. Clinical Infectious Diseases, 57(3), 425–433. https://doi.org/10.1093/cid/cit244
- Bhunia, A. K. (2014). One day to one hour: How quickly can foodborne pathogens be detected? Future Microbiology, 9(8), 935–946. https://doi.org/10.2217/FMB.14.61
- Bintsis, T. (2017). Foodborne pathogens. AIMS Microbiology, 3(3), 529. https://doi.org/10.3934/microbiol.2017.3.529
- Braun, P., Wolfschlager, I., Reetz, L., Bachstein, L., Jacinto, A. C., Tocantins, C., & Grass, G. (2020). Rapid microscopic detection of Bacillus anthracis by fluorescent receptor binding proteins of bacteriophages. Microorganisms, 8(6), 1–21. https://doi.org/10.3390/microorganisms8060934
- Brézillon, C., Haustant, M., Dupke, S., Corre, J.-P., Lander, A., Franz, T., & Leendertz, F. H. (2015). Capsules, toxins and AtxA as virulence factors of emerging Bacillus cereus biovar anthracis. PLoS Neglected Tropical Diseases, 9(4), e0003455. https://doi.org/10.1371/journal.pntd.0003455
- Brigati, J., Williams, D. D., Sorokulova, I. B., Nanduri, V., Hsuan Chen, I., Tumbough, C. L., & Petrenko, V. A. (2004). Dianostic probes for Bacillus anthracis spores selected from a landscape phage library. Clinical Chemistry, 50(10), 1899–1906. https://doi.org/10.1373/clinchem.2004.038018
- Browne, N., & Dowds, B. (2001). Heat and salt stress in the food pathogen Bacillus cereus. Journal of Applied Microbiology, 91(6), 1085–1094. https://doi.org/10.1046/j.1365-2672.2001.01478.x
- Chang, R. Y. K., Morales, S., Okamoto, Y., & Chan, H.-K. (2020). Topical application of bacteriophages for treatment of wound infections. Translational Research, 220, 153–166. https://doi.org/10.1016/j.trsl.2020.03.010
- Chang, Y. (2020). Bacteriophage-derived Endolysins applied as potent biocontrol agents to enhance food safety. Microorganisms, 8(5), 724. https://doi.org/10.3390/microorganisms8050724
- Choi, I. Y., Park, J. H., Gwak, K. M., Kim, K.-P., Oh, J.-H., & Park, M.-K. (2018). Studies on lytic, tailed Bacillus cereus-specific phage for use in a ferromagnetoelastic biosensor as a novel recognition element. Journal of Microbiology and Biotechnology, 28(1), 87–94. https://doi.org/10.4014/jmb.1710.10033
- Cooper, C. J., Koonjan, S., & Nilsson, A. S. (2018). Enhancing whole phage therapy and their derived antimicrobial enzymes through complex formulation. Pharmaceuticals, 11(2), 34. https://doi.org/10.3390/ph11020034
- de Jonge, P. A., Nobrega, F. L., Brouns, S. J., & Dutilh, B. E. (2019). Molecular and evolutionary determinants of bacteriophage host range. Trends in Microbiology, 27(1), 51–63. https://doi.org/10.1016/j.tim.2018.08.006
- de Sousa, J. M., Pfeifer, E., Touchon, M., & Rocha, E. P. (2020). Genome diversification via genetic exchanges between temperate and virulent bacteriophages. bioRxiv. doi: https://doi.org/10.1101/2020.04.14.041137.
10.1101/2020.04.14.041137 Google Scholar
- Dewey-Mattia, D., Manikonda, K., Hall, A. J., Wise, M. E., & Crowe, S. J. (2018). Surveillance for foodborne disease outbreaks—United States, 2009–2015. MMWR Surveillance Summaries, 67(10), 1. https://doi.org/10.15585/mmwr.ss6710a1
- Dunne, M., Hupfeld, M., Klumpp, J., & Loessner, M. J. (2018). Molecular basis of bacterial host interactions by Gram-positive targeting bacteriophages. Viruses, 10(8), 397. https://doi.org/10.3390/v10080397
- Ehling-Schulz, M., Frenzel, E., & Gohar, M. (2015). Food–bacteria interplay: Pathometabolism of emetic Bacillus cereus. Frontiers in Microbiology, 6, 704. https://doi.org/10.3389/fmicb.2015.00704
- Ehling-Schulz, M., Lereclus, D., & Koehler, T. M. (2019). The Bacillus cereus group: Bacillus species with pathogenic potential. Microbiology Spectrum, 6, 875–902. https://doi.org/10.1128/microbiolspec.GPP3-0032-2018
- El-Arabi, T. F., Griffiths, M. W., She, Y.-M., Villegas, A., Lingohr, E. J., & Kropinski, A. M. (2013). Genome sequence and analysis of a broad-host range lytic bacteriophage that infects the Bacillus cereus group. Virology Journal, 10(1), 1–11. https://doi.org/10.1186/1743-422X-10-48
- Etobayeva, I., Linden, S. B., Alem, F., Harb, L., Rizkalla, L., Mosier, P. D., & Nelson, D. C. (2018). Discovery and biochemical characterization of PlyP56, PlyN74, and PlyTB40—Bacillus specific endolysins. Viruses, 10(5), 276. https://doi.org/10.3390/v10050276
- Foddai, A. C. G., & Grant, I. R. (2020). Methods for detection of viable foodborne pathogens: Current state-of-art and future prospects. Applied Microbiology and Biotechnology, 104(10), 4281–4288. https://doi.org/10.1007/s00253-020-10542-x
- Fogele, B., Granta, R., Valciņa, O., & Bērziņš, A. (2018). Occurrence and diversity of Bacillus cereus and moulds in spices and herbs. Food Control, 83, 69–74. https://doi.org/10.1016/j.foodcont.2017.05.038
- Gálvez, A., Abriouel, H., López, R., & Omar, N. B. (2011). Biological control of pathogens and post-processing spoilage microorganisms in fresh and processed fruit and vegetables. In Protective cultures, antimicrobial metabolites and bacteriophages for food and beverage biopreservation (pp. 403–432). Spain: Elsevier.
10.1533/9780857090522.3.403 Google Scholar
- Garcia, P., Martinez, B., Obeso, J., & Rodriguez, A. (2008). Bacteriophages and their application in food safety. Letters in Applied Microbiology, 47(6), 479–485.
- Gdoura-Ben Amor, M., Siala, M., Zayani, M., Grosset, N., Smaoui, S., Messadi-Akrout, F., & Gdoura, R. (2018). Isolation, identification, prevalence, and genetic diversity of Bacillus cereus group bacteria from different foodstuffs in Tunisia. Frontiers in Microbiology, 9, 447. https://doi.org/10.3389/fmicb.2018.00447
- Geng, P., Tian, S., Yuan, Z., & Hu, X. (2017). Identification and genomic comparison of temperate bacteriophages derived from emetic Bacillus cereus. PLoS One, 12(9), e0184572. https://doi.org/10.1371/journal.pone.0184572
- Gill, J. J., & Hyman, P. (2010). Phage choice, isolation, and preparation for phage therapy. Current Pharmaceutical Biotechnology, 11(1), 2–14. https://doi.org/10.2174/138920110790725311
- Goodridge, L., & Griffiths, M. (2002). Reporter bacteriophage assays as a means to detect foodborne pathogenic bacteria. Food Research International, 35(9), 863–870. https://doi.org/10.1016/S0963-9969(02)00094-7
- Griffiths, M., & Schraft, H. (2017). Bacillus cereus food poisoning. In Foodborne diseases (pp. 395–405). Canada: Elsevier.
10.1016/B978-0-12-385007-2.00020-6 Google Scholar
- Gutiérrez, D., Rodríguez-Rubio, L., Martínez, B., Rodríguez, A., & García, P. (2016). Bacteriophages as weapons against bacterial biofilms in the food industry. Frontiers in Microbiology, 7, 825. https://doi.org/10.3389/fmicb.2016.00825
- Hagens, S., & Loessner, M. J. (2010). Bacteriophage for biocontrol of foodborne pathogens: Calculations and considerations. Current Pharmaceutical Biotechnology, 11(1), 58–68. https://doi.org/10.2174/138920110790725429
- Harada, L. K., Silva, E. C., Campos, W. F., Del Fiol, F. S., Vila, M., Dąbrowska, K., & Balcão, V. M. (2018). Biotechnological applications of bacteriophages: State of the art. Microbiological Research, 212, 38–58. https://doi.org/10.1016/j.micres.2018.04.007
- Hock, L., Gillis, A., & Mahillon, J. (2018). Complete genome sequence of bacteriophage deep-purple, a novel member of the family Siphoviridae infecting Bacillus cereus. Archives of Virology, 163(9), 2555–2559. https://doi.org/10.1007/s00705-018-3865-z
- Huss, P., & Raman, S. (2020). Engineered bacteriophages as programmable biocontrol agents. Current Opinion in Biotechnology, 61, 116–121. https://doi.org/10.1016/j.copbio.2019.11.013
- Jeßberger, N., Krey, V. M., Rademacher, C., Böhm, M.-E., Mohr, A.-K., Ehling-Schulz, M., & Märtlbauer, E. (2015). From genome to toxicity: A combinatory approach highlights the complexity of enterotoxin production in Bacillus cereus. Frontiers in Microbiology, 6, 560. https://doi.org/10.3389/fmicb.2015.00560
- Kim, J., Kim, G.-H., Lee, N.-G., Lee, J.-S., & Yoon, S.-S. (2018). Whole-genome sequencing and genomic analysis of a virulent bacteriophage infecting Bacillus cereus. Intervirology, 61(6), 272–280. https://doi.org/10.1159/000499068
- Kirk, M. D., Pires, S. M., Black, R. E., Caipo, M., Crump, J. A., Devleesschauwer, B., & Hald, T. (2015). World Health Organization estimates of the global and regional disease burden of 22 foodborne bacterial, protozoal, and viral diseases, 2010: A data synthesis. PLoS Medicine, 12(12), e1001921. https://doi.org/10.1371/journal.pmed.1001921
- Kong, M., Na, H., Ha, N.-C., & Ryu, S. (2019). LysPBC2, a novel endolysin harboring a Bacillus cereus spore binding domain. Applied and Environmental Microbiology, 85(5), 1–14. https://doi.org/10.1128/AEM.02462-18
- Kong, M., & Ryu, S. (2015). Bacteriophage PBC1 and its endolysin as an antimicrobial agent against Bacillus cereus. Applied and Environmental Microbiology, 81(7), 2274–2283. https://doi.org/10.1128/AEM.03485-14
- Kong, M., Shin, J. H., Heu, S., Park, J.-K., & Ryu, S. (2017). Lateral flow assay-based bacterial detection using engineered cell wall binding domains of a phage endolysin. Biosensors and Bioelectronics, 96, 173–177. https://doi.org/10.1016/j.bios.2017.05.010
- Kong, M., Sim, J., Kang, T., Nguyen, H. H., Park, H. K., Chung, B. H., & Ryu, S. (2015). A novel and highly specific phage endolysin cell wall binding domain for detection of Bacillus cereus. European Biophysics Journal, 44(6), 437–446. https://doi.org/10.1007/s00249-015-1044-7
- Kretzer, J. W., Lehmann, R., Schmelcher, M., Banz, M., Kim, K.-P., Korn, C., & Loessner, M. J. (2007). Use of high-affinity cell wall-binding domains of bacteriophage endolysins for immobilization and separation of bacterial cells. Applied and Environmental Microbiology, 73(6), 1992–2000. https://doi.org/10.1128/AEM.02402-06
- Kumari, S., & Sarkar, P. K. (2016). Bacillus cereus hazard and control in industrial dairy processing environment. Food Control, 69, 20–29. https://doi.org/10.1016/j.foodcont.2016.04.012
- Lee, J.-H., Shin, H., Son, B., & Ryu, S. (2012). Complete genome sequence of Bacillus cereus bacteriophage BCP78. Journal of Virology, 637–638. https://doi.org/10.1128/JVI.06520-11
- Lee, W. J., Billington, C., Hudson, J., & Heinemann, J. (2011). Isolation and characterization of phages infecting Bacillus cereus. Letters in Applied Microbiology, 52(5), 456–464. https://doi.org/10.1111/j.1472-765X.2011.03023.x
- Lee, Y.-D., & Park, J.-H. (2010). Genomic sequence of temperate phage 250 isolated from emetic B. cereus and cloning of putative endolysin. Food Science and Biotechnology, 19(6), 1643–1648. https://doi.org/10.1007/s10068-010-0232-6
- Liu, P., Han, L., Wang, F., Petrenko, V. A., & Liu, A. (2016). Gold nanoprobe functionalized with specific fusion protein selection from phage display and its application in rapid, selective and sensitive colorimetric biosensing of Staphylococcus aureus. Biosensors and Bioelectronics, 82, 195–203. https://doi.org/10.1016/j.bios.2016.03.075
- Loessner, M. J. (2005). Bacteriophage endolysins—Current state of research and applications. Current Opinion in Microbiology, 8(4), 480–487. https://doi.org/10.1016/j.mib.2005.06.002
- Loessner, M. J., Maier, S. K., Daubek-Puza, H., Wendlinger, G., & Scherer, S. (1997). Three Bacillus cereus bacteriophage endolysins are unrelated but reveal high homology to cell wall hydrolases from different bacilli. Journal of Bacteriology, 179(9), 2845–2851. https://doi.org/10.1128/jb.179.9.2845-2851.1997
- Loessner, M. J., Rudolf, M., & Scherer, S. (1997). Evaluation of luciferase reporter bacteriophage A511:: luxAB for detection of Listeria monocytogenes in contaminated foods. Applied and Environmental Microbiology, 63(8), 2961–2965. https://doi.org/10.1128/AEM.63.8.2961-2965.1997
- López-Cuevas, O., Medrano-Félix, J., Castro-Del Campo, N., & Chaidez, C. (2019). Bacteriophage applications for fresh produce food safety. International Journal of Environmental Health Research, 29, 1–16. https://doi.org/10.1080/09603123.2019.1680819
- Low, L. Y., Yang, C., Perego, M., Osterman, A., & Liddington, R. C. (2005). Structure and lytic activity of a Bacillus anthracis prophage endolysin. Journal of Biological Chemistry, 280(42), 35433–35439. https://doi.org/10.1074/jbc.M502723200
- Mahony, J., McAuliffe, O., Ross, R. P., & Van Sinderen, D. (2011). Bacteriophages as biocontrol agents of food pathogens. Current Opinion in Biotechnology, 22(2), 157–163. https://doi.org/10.1016/j.copbio.2010.10.008
- Martinović, T., Andjelković, U., Gajdošik, M. Š., Rešetar, D., & Josić, D. (2016). Foodborne pathogens and their toxins. Journal of Proteomics, 147, 226–235. https://doi.org/10.1016/j.jprot.2016.04.029
- Mehta, K. K., Paskaleva, E. E., Azizi-Ghannad, S., Ley, D. J., Page, M. A., Dordick, J. S., & Kane, R. S. (2013). Characterization of AmiBA2446, a novel bacteriolytic enzyme active against Bacillus species. Applied and Environmental Microbiology, 79(19), 5899–5906. https://doi.org/10.1128/AEM.02235-13
- Meile, S., Kilcher, S., Loessner, M. J., & Dunne, M. (2020). Reporter phage-based detection of bacterial pathogens: Design guidelines and recent developments. Viruses, 12(9), 944.
- Meile, S., Sarbach, A., Du, J., Schuppler, M., Saez, C., Loessner, M. J., & Kilcher, S. (2020). Engineered reporter phages for rapid bioluminescence-based detection and differentiation of viable Listeria cells. Applied and Environmental Microbiology, 86(11), 1–14. https://doi.org/10.1128/AEM.00442-20
- Moye, Z. D., Woolston, J., & Sulakvelidze, A. (2018). Bacteriophage applications for food production and processing. Viruses, 10(4), 205. https://doi.org/10.3390/v10040205
- Nakonieczna, A., Cooper, C. J., & Gryko, R. (2015). Bacteriophages and bacteriophage-derived endolysins as potential therapeutics to combat gram-positive spore forming bacteria. Journal of Applied Microbiology, 119(3), 620–631. https://doi.org/10.1111/jam.12881
- Nicastro, J., Wong, S., Khazaei, Z., Lam, P., Blay, J., & Slavcev, R. A. (2016). Bacteriophage applications-historical perspective and future potential. Switzerland: Springer.
10.1007/978-3-319-45791-8 Google Scholar
- Nobrega, F. L., Vlot, M., de Jonge, P. A., Dreesens, L. L., Beaumont, H. J., Lavigne, R., … Brouns, S. J. (2018). Targeting mechanisms of tailed bacteriophages. Nature Reviews Microbiology, 16(12), 760–773. https://doi.org/10.1038/s41579-018-0070-8
- O'Sullivan, L., Bolton, D., McAuliffe, O., & Coffey, A. (2019). The use of bacteriophages to control and detect pathogens in the dairy industry. International Journal of Dairy Technology, 73(1), 1–11. https://doi.org/10.1111/1471-0307.12641
- Oh, H., Seo, D. J., Jeon, S. B., Park, H., Jeong, S., Chun, H. S., & Choi, C. (2017). Isolation and characterization of Bacillus cereus bacteriophages from foods and soil. Food and Environmental Virology, 9(3), 260–269. https://doi.org/10.1007/s12560-017-9284-6
- Organji, S. R., Abulreesh, H. H., Elbanna, K., Osman, G. E. H., & Khider, M. (2015). Occurrence and characterization of toxigenic Bacillus cereus in food and infant feces. Asian Pacific Journal of Tropical Biomedicine, 5(7), 515–520. https://doi.org/10.1016/j.apjtb.2015.04.004
10.1016/j.apjtb.2015.04.004 Google Scholar
- Park, C., Kong, M., Lee, J.-H., Ryu, S., & Park, S. (2018). Detection of Bacillus cereus using bioluminescence assay with cell wall-binding domain conjugated magnetic nanoparticles. BioChip Journal, 12(4), 287–293. https://doi.org/10.1007/s13206-018-2408-8
- Park, J., Yun, J., Lim, J.-A., Kang, D.-H., & Ryu, S. (2012). Characterization of an endolysin, LysBPS13, from a Bacillus cereus bacteriophage. FEMS Microbiology Letters, 332(1), 76–83. https://doi.org/10.1111/j.1574-6968.2012.02578.x
- Park, K. M., Jeong, M., Park, K. J., & Koo, M. (2018). Prevalence, enterotoxin genes, and antibiotic resistance of Bacillus cereus isolated from raw vegetables in Korea. Journal of Food Protection, 81(10), 1590–1597. https://doi.org/10.4315/0362-028X.JFP-18-205
- Peng, Q., & Yuan, Y. (2018). Characterization of a novel phage infecting the pathogenic multidrug-resistant Bacillus cereus and functional analysis of its endolysin. Applied Microbiology and Biotechnology, 102, 7901–7912. https://doi.org/10.1007/s00253-018-9219-7
- Pires, D. P., Oliveira, H., Melo, L. D., Sillankorva, S., & Azeredo, J. (2016). Bacteriophage-encoded depolymerases: Their diversity and biotechnological applications. Applied Microbiology and Biotechnology, 100(5), 2141–2151. https://doi.org/10.1007/s00253-015-7247-0
- Ramarao, N., Tran, S. L., Marin, M., & Vidic, J. (2020). Advanced methods for detection of Bacillus cereus and its pathogenic factors. Sensors (Basel), 20(9), 1–23. https://doi.org/10.3390/s20092667
10.3390/s20092667 Google Scholar
- Rao, S. S., Mohan, K. V., & Atreya, C. D. (2013). A peptide derived from phage display library exhibits antibacterial activity against E. coli and Pseudomonas aeruginosa. PloS One, 8(2), e56081. https://doi.org/10.1371/journal.pone.0056081
- Rao, S. S., Mohan, K. V., Nguyen, N., Abraham, B., Abdouleva, G., Zhang, P., & Atreya, C. D. (2010). Peptides panned from a phage-displayed random peptide library are useful for the detection of Bacillus anthracis surrogates B. cereus 4342 and B. anthracis Sterne. Biochemical and Biophysical Research Communications, 395(1), 93–98. https://doi.org/10.1016/j.bbrc.2010.03.145
- 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. https://doi.org/10.1016/j.drudis.2017.11.007
- Roach, D. R., & Donovan, D. M. (2015). Antimicrobial bacteriophage-derived proteins and therapeutic applications. Bacteriophage, 5(3), e1062590. https://doi.org/10.1080/21597081.2015.1062590
- Rovik, A., & PRAMONO, H. (2020). Isolation and selection of Bacillus cereus specific phages from hospital wastewater. Biodiversitas, 21(7), 2871–2877. https://doi.org/10.13057/biodiv/d210701
10.13057/biodiv/d210701 Google Scholar
- Sainathrao, S., Mohan, K. V. K., & Atreya, C. (2009). Gamma-phage lysin PlyG sequence-based synthetic peptides coupled with Qdot-nanocrystals are useful for developing detection methods for Bacillus anthracis by using its surrogates, B. anthracis-Sterne and B. cereus-4342. BMC Biotechnology, 9(1), 67. https://doi.org/10.1186/1472-6750-9-67
- Sánchez-Chica, J., Correa, M. M., Aceves-Diez, A. E., & Castañeda-Sandoval, L. M. (2020). A novel method for direct detection of Bacillus cereus toxin genes in powdered dairy products. International Dairy Journal, 103(104625), 1–7. https://doi.org/10.1016/j.idairyj.2019.104625
- Schmelcher, M., Donovan, D. M., & Loessner, M. J. (2012). Bacteriophage endolysins as novel antimicrobials. Future Microbiology, 7(10), 1147–1171. https://doi.org/10.2217/fmb.12.97
- Schmelcher, M., & Loessner, M. J. (2014). Application of bacteriophages for detection of foodborne pathogens. Bacteriophage, 4(2), e28137. https://doi.org/10.4161/bact.28137
- Schmerer, M., Molineux, I. J., & Bull, J. J. (2014). Synergy as a rationale for phage therapy using phage cocktails. PeerJ, 2, e590. https://doi.org/10.7717/peerj.590
- Schofield, D., & Westwater, C. (2009). Phage-mediated bioluminescent detection of Bacillus anthracis. Journal of Applied Microbiology, 107(5), 1468–1478. https://doi.org/10.1111/j.1365-2672.2009.04332.x
- Schuch, R., Pelzek, A. J., Fazzini, M. M., Nelson, D. C., & Fischetti, V. A. (2014). Complete genome sequence of Bacillus cereus sensu lato bacteriophage Bcp1. Genome Announcements, 2(3), 1–2. https://doi.org/10.1128/genomeA.00334-14
10.1128/genomeA.00334-14 Google Scholar
- Schuch, R., Pelzek, A. J., Nelson, D. C., & Fischetti, V. A. (2019). The PlyB endolysin of bacteriophage vB_BanS_Bcp1 exhibits broad-spectrum bactericidal activity against Bacillus cereus sensu lato isolates. Applied and Environmental Microbiology, 85(9), 1–16. https://doi.org/10.1128/AEM.00003-19
- Sharma, S., Chatterjee, S., Datta, S., Prasad, R., Dubey, D., Prasad, R. K., & Vairale, M. G. (2017). Bacteriophages and its applications: An overview. Folia Microbiologia (Praha), 62(1), 17–55. https://doi.org/10.1007/s12223-016-0471-x
- Simoes, M., Simões, L. C., & Vieira, M. J. (2010). A review of current and emergent biofilm control strategies. LWT-Food Science and Technology, 43(4), 573–583. https://doi.org/10.1016/j.lwt.2009.12.008
- Šimoliūnienė, M., Tumėnas, D., Kvederavičiūtė, K., Meškys, R., Šulčius, S., & Šimoliūnas, E. (2020). Complete genome sequence of Bacillus cereus bacteriophage vB_BceS_KLEB30-3S. Microbiology Resource Announcements, 9(20), 1–3. https://doi.org/10.1128/MRA.00348-20
- Singh, A., Poshtiban, S., & Evoy, S. (2013). Recent advances in bacteriophage based biosensors for food-borne pathogen detection. Sensors, 13(2), 1763–1786. https://doi.org/10.3390/s130201763
- Smartt, A. E., Xu, T., Jegier, P., Carswell, J. J., Blount, S. A., Sayler, G. S., & Ripp, S. (2012). Pathogen detection using engineered bacteriophages. Analytical and Bioanalytical Chemistry, 402(10), 3127–3146. https://doi.org/10.1007/s00216-011-5555-5
- Son, B., Kong, M., Cha, Y., Bai, J., & Ryu, S. (2020). Simultaneous control of Staphylococcus aureus and Bacillus cereus using a hybrid Endolysin LysB4EAD-LysSA11. Antibiotics, 9(12), 906. https://doi.org/10.3390/antibiotics9120906
- Son, B., Yun, J., Lim, J.-A., Shin, H., Heu, S., & Ryu, S. (2012). Characterization of LysB4, an endolysin from the Bacillus cereus-infecting bacteriophage B4. BMC Microbiology, 12(1), 1–9. https://doi.org/10.1186/1471-2180-12-33
- Swift, S. M., Etobayeva, I. V., Reid, K. P., Waters, J. J., Oakley, B. B., Donovan, D. M., & Nelson, D. C. (2019). Characterization of LysBC17, a lytic endopeptidase from Bacillus cereus. Antibiotics, 8(3), 155. https://doi.org/10.3390/antibiotics8030155
- Tavares, P. (2018). The bacteriophage head-to-tail interface. In Virus protein and nucleoprotein complexes (pp. 305–328). Singapore: Springer.
10.1007/978-981-10-8456-0_14 Google Scholar
- Tewari, A., Singh, S., & Singh, R. (2015). Incidence and enterotoxigenic profile of Bacillus cereus in meat and meat products of Uttarakhand, India. Journal of Food Science and Technology, 52(3), 1796–1801. https://doi.org/10.1007/s13197-013-1162-0
- Thorsen, L., Azokpota, P., Hansen, B. M., Hounhouigan, D. J., & Jakobsen, M. (2010). Identification, genetic diversity and cereulide producing ability of Bacillus cereus group strains isolated from Beninese traditional fermented food condiments. International Journal of Food Microbiology, 142(1–2), 247–250. https://doi.org/10.1016/j.fm.2011.07.003
- Turnbough, C. L. (2003). Discovery of phage display peptide ligands for species-specific detection of Bacillus spores. Journal of Microbiological Methods, 53, 263–271.
- Vidic, J., Chaix, C., Manzano, M., & Heyndrickx, M. (2020). Food sensing: Detection of Bacillus cereus spores in dairy products. Biosensors, 10(3), 15. https://doi.org/10.3390/bios10030015
- Vikram, A., Woolston, J., & Sulakvelidze, A. (2020). Phage biocontrol applications in food production and processing. Current Issues in Molecular Biology, 40, 267–302. https://doi.org/10.21775/cimb.040.267
- Wan, J., Johnson, M. L., Guntupalli, R., Petrenko, V. A., & Chin, B. A. (2007). Detection of Bacillus anthracis spores in liquid using phage-based Magnetoelastic micro-resonators. Sensors & Actuators, B, 127(2), 559–566. https://doi.org/10.1016/j.snb.2007.05.017
- Wehrle, E., Moravek, M., Dietrich, R., Burk, C., Didier, A., & Martlbauer, E. (2009). Comparison of multiplex PCR, enzyme immunoassay and cell culture methods for the detection of enterotoxinogenic Bacillus cereus. Journal of Microbiological Methods, 78(3), 265–270. https://doi.org/10.1016/j.mimet.2009.06.013
- WHO. (2015). WHO estimates of the global burden of foodborne diseases: Foodborne disease burden epidemiology reference group 2007–2015. Switzerland: World Health Organization.
- Williams, D. D., Benedek, O., & Turnbough, C. L. (2003). Species-specific peptide ligands for the detection of Bacillus anthracis spores. Applied and Environmental Microbiology, 69, 6288–6293. https://doi.org/10.1128/AEM.69.10.6288-6293.2003
- Yemini, M., Levi, Y., Yagil, E., & Rishpon, J. (2007). Specific electrochemical phage sensing for Bacillus cereus and Mycobacterium smegmatis. Bioelectrochemistry, 70(1), 180–184. https://doi.org/10.1016/j.bioelechem.2006.03.014
- Yu, S., Yu, P., Wang, J., Li, C., Guo, H., Liu, C., & Lei, T. (2020). A study on prevalence and characterization of Bacillus cereus in ready-to-eat foods in China. Frontiers in Microbiology, 10, 3043. https://doi.org/10.3389/fmicb.2019.03043
- Yutin, N., Makarova, K. S., Gussow, A. B., Krupovic, M., Segall, A., Edwards, R. A., & Koonin, E. V. (2018). Discovery of an expansive bacteriophage family that includes the most abundant viruses from the human gut. Nature Microbiology, 3(1), 38–46. https://doi.org/10.1038/s41564-017-0053-y
- Zhai, Y., Zhao, C., Li, L., Xu, K., Wang, J., Song, X., & Li, H. (2020). Production of phage display-derived peptide and the application for detecting Vibrio parahaemolyticus by combined PCR technology. Food Analytical Methods, 13, 1906–1917. https://doi.org/10.1007/s12161-020-01800-9
- Zhang, Z., Feng, L., Xu, H., Liu, C., Shah, N. P., & Wei, H. (2016). Detection of viable enterotoxin-producing Bacillus cereus and analysis of toxigenicity from ready-to-eat foods and infant formula milk powder by multiplex PCR. Journal of Dairy Science, 99(2), 1047–1055. https://doi.org/10.3168/jds.2015-10147
- Zhang, Z., Wang, L., Xu, H., Aguilar, Z. P., Liu, C., Gan, B., & Wei, H. (2014). Detection of non-emetic and emetic Bacillus cereus by propidium monoazide multiplex PCR (PMA-mPCR) with internal amplification control. Food Control, 35(1), 401–406. https://doi.org/10.1016/j.foodcont.2013.07.035
- Zhao, X., Lin, C. W., Wang, J., & Oh, D. H. (2014). Advances in rapid detection methods for foodborne pathogens. Journal of Microbiology and Biotechnology, 24(3), 297–312. https://doi.org/10.4014/jmb.1310.10013
- Zuberovic, M., Aida, T., Granelli, R., & Hellenäs, K.-E. (2014). Quantitative analysis of cereulide toxin from Bacillus cereus in rice and pasta using synthetic cereulide standard and 13C6-cereulide standard—A short validation study. Toxins, 6(12), 3326–3335. https://doi.org/10.3390/toxins6123326