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AIMS Microbiology

2019, Volume 5, Issue 4: 324-346. doi: 10.3934/microbiol.2019.4.324
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Bacteriophages—a new hope or a huge problem in the food industry

  • Institute of Agricultural and Food Biotechnology, Department of Microbiology, 36 Rakowiecka, 02-532 Warsaw, Poland
  • Received: 31 July 2019 Accepted: 22 October 2019 Published: 24 October 2019

  • Bacteriophages are viruses that are ubiquitous in nature and infect only bacterial cells. These organisms are characterized by high specificity, an important feature that enables their use in the food industry. Phages are applied in three sectors in the food industry: primary production, biosanitization, and biopreservation. In biosanitization, phages or the enzymes that they produce are mainly used to prevent the formation of biofilms on the surface of equipment used in the production facilities. In the case of biopreservation, phages are used to extend the shelf life of products by combating pathogenic bacteria that spoil the food. Although phages are beneficial in controlling the food quality, they also have negative effects. For instance, the natural ability of phages that are specific to lactic acid bacteria to destroy the starter cultures in dairy production incurs huge financial losses to the dairy industry. In this paper, we discuss how bacteriophages can be either an effective weapon in the fight against bacteria or a bane negatively affecting the quality of food products depending on the type of industry they are used.

    Citation: Marzena Połaska, Barbara Sokołowska. Bacteriophages—a new hope or a huge problem in the food industry[J]. AIMS Microbiology, 2019, 5(4): 324-346. doi: 10.3934/microbiol.2019.4.324

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  • Bacteriophages are viruses that are ubiquitous in nature and infect only bacterial cells. These organisms are characterized by high specificity, an important feature that enables their use in the food industry. Phages are applied in three sectors in the food industry: primary production, biosanitization, and biopreservation. In biosanitization, phages or the enzymes that they produce are mainly used to prevent the formation of biofilms on the surface of equipment used in the production facilities. In the case of biopreservation, phages are used to extend the shelf life of products by combating pathogenic bacteria that spoil the food. Although phages are beneficial in controlling the food quality, they also have negative effects. For instance, the natural ability of phages that are specific to lactic acid bacteria to destroy the starter cultures in dairy production incurs huge financial losses to the dairy industry. In this paper, we discuss how bacteriophages can be either an effective weapon in the fight against bacteria or a bane negatively affecting the quality of food products depending on the type of industry they are used.


    加载中

    Abbreviation LAB: lactic acid bacteria; DP: depolymerase enzyme; MRSA: methicillin-resistant ; EFSA: European Food Safety Authority; WHO: World Health Organization; FDA: Food and Drug Administration; RTE: ready to eat; EPS: extracellular polymeric substances;
    Acknowledgments


    This work was financially supported by Institute of Agricultural and Food Biotechnology, 36 Rakowiecka, 02-532 Warsaw, Poland.

    Conflict of interest


    All authors declare no conflicts of interest in this paper.

    [1] Hendrix WR (2002) Bacteriophages: evolution of the majority. Theor Popul Biol 61: 471–480. doi: 10.1006/tpbi.2002.1590
    [2] Hietala V, Horsma-Heikkinen J, Carron A, et al. (2019) The removal of endo- and enterotoxins from bacteriophage preparations. Front Microbiol 10: 1–9. doi: 10.3389/fmicb.2019.00001
    [3] Sarhan WA, Azzazy HM (2015) Phage approved in food, why not as a therapeutic? Expert Rev Anti Infect Ther 13: 91–101. doi: 10.1586/14787210.2015.990383
    [4] Górski A, Międzybrodzki R, Borysowski J, et al. (2012) Phage as a modulator of immune responses: practical implications for phage therapy. Adv Virus Res 83: 41–71. doi: 10.1016/B978-0-12-394438-2.00002-5
    [5] Wittebole X, Roock De S, Opa M (2014) Historical overview of bacteriophage therapy as an alternative to antibiotics for the treatment of bacterial pathogens. Virulence 5: 226–235. doi: 10.4161/viru.25991
    [6] Kazi M, Annapure US (2016) Bacteriophage biocontrol of foodborne pathogens. J Food Sci Technol 53: 1355–1362. doi: 10.1007/s13197-015-1996-8
    [7] Gilmore BF (2012) Bacteriophages as anti-infective agents: recent developments and regulatory challenges. Expert Rev Anti Infe Ther 10: 533–535. doi: 10.1586/eri.12.30
    [8] Fernández L, Gutiérrez D, Rodríguez A, et al. (2018) Application of bacteriophages in the agro-food sector: a long way toward approval. Front Cell Infect Microbiol 8: 1–5. doi: 10.3389/fcimb.2018.00001
    [9] Balogh B, Jones JB, Iriarte FB (2010) Phage therapy for plant disease control. Curr Pharm Biotechno 11: 48–57. doi: 10.2174/138920110790725302
    [10] Civerolo EL, Kiel HL (1969) Inhibition of bacterial spot of peach foliage by Xanthomonas pruni bacteriophage. Phytopathology 59: 1966–1967.
    [11] Eman OH, El-Meneisy Afaf ZA (2014) Biocontrol of halo blight of bean caused by pseudomonas phaseolicola. Int J Virol 10: 235–242. doi: 10.3923/ijv.2014.235.242
    [12] Fujiwara A, Fujisawa M, Hamasaki R, et al. (2011) Biocontrol of ralstonia solanacearum by treatment with lytic bacteriophages. Appl Environ Microbiol 77: 4155–4162. doi: 10.1128/AEM.02847-10
    [13] Born Y, Bosshard L, Duffy B, et al. (2015) Protection of Erwinia amylovora bacteriophage Y2 from UV-induced damage by natural compounds. Bacteriophage 5: 1–5.
    [14] Zaccardelli M, Saccardi A, Gambin E (1992) Xanthomonas campestris pv. pruni bacteriophages on peach trees and their potential use for biological control. Plant Pathogenic Bacteria 8th International Conference 875–878.
    [15] Balogh B, Canteros BI, Stall RE (2008) Control of citrus canker and citrus bacterial spot with bacteriophages. Plant Dis 92: 1048–1052. doi: 10.1094/PDIS-92-7-1048
    [16] Balogh B, Jones JB, Iriarte FB (2010) Phage therapy for plant disease control. Curr Pharm Biotechno 11: 48–57. doi: 10.2174/138920110790725302
    [17] Leverentz B, Conway WS, Alavidze Z (2001) Examination of bacteriophage as a biocontrol method for Salmonella on fresh-cut fruit: a model study. J Food Protect 64: 1116–1121. doi: 10.4315/0362-028X-64.8.1116
    [18] Szczepankowska A (2012) Role of CRISPR/cas system in the development of bacteriophage resistance. Adv Virus Res 82: 289–338. doi: 10.1016/B978-0-12-394621-8.00011-X
    [19] Koskella B, Brockhurs MA (2014) Bacteria–phage coevolution as a driver of ecological and evolutionary processes in microbial communities. FEMS Microbiol Rev 38: 916–931. doi: 10.1111/1574-6976.12072
    [20] Carrillo LC, Atterbury JR, El-Shibiny A (2005) Bacteriophage therapy to reduce Campylobacter jejuni colonization of broiler chickens. Appl Environ Microb 71: 6554–6563. doi: 10.1128/AEM.71.11.6554-6563.2005
    [21] Wagenaar AJ, Van Bergen M, Mueller M (2005) Phage therapy reduces Campylobacter jejuni colonization in broilers. Vet Microbiol 109: 275–283. doi: 10.1016/j.vetmic.2005.06.002
    [22] Arthur MT, Kalchayanand N, Agga EG, et al. (2017) Evaluation of bacteriophage application to cattle in lairage at beef processing plants to reduce Escherichia coli O157:H7. Prevalence on hides and carcasses. Foodborne Pathog Dis 14: 17–22. doi: 10.1089/fpd.2016.2189
    [23] Wall KS, Zhang J, Rostagno HM (2010) Phage therapy to reduce preprocessing Salmonella infections in market-weight swine. Appl Environ Microb 76: 48–53. doi: 10.1128/AEM.00785-09
    [24] Bach JS, Johnson PR, Stanford K (2009) Bacteriophages reduce Escherichia coli O157:H7 levels in experimentally inoculated sheep. Can J Animal Sci 89: 285–293. doi: 10.4141/CJAS08083
    [25] Huanga K, Nitin N (2019) Edible bacteriophage based antimicrobial coating on fish feed for enhanced treatment of bacterial infections in aquaculture industry. Aquaculture 502: 18–25 doi: 10.1016/j.aquaculture.2018.12.026
    [26] Rivas L, Coffey B, McAuliffe O (2010) In vivo and ex vivo evaluations of bacteriophages e11/2 and e4/1c for use in the control of Escherichia coli O157:H7. App Environ Microb 76: 7210–7216. doi: 10.1128/AEM.01530-10
    [27] Hussain MA, Liu H, Wang Q (2017) Use of encapsulated bacteriophages to enhance farm to fork food safety. Crit Rev Food Sci 57: 2801–2810. doi: 10.1080/10408398.2015.1069729
    [28] Murthy K, Engelhardt R (2012) Encapsulated bacteriophage formulation. United States Patent 2012/0258175 A1. 2012-10-11.
    [29] Stanford K, Mcallister AT, Niu DY (2010) Oral delivery systems for encapsulated bacteriophages targeted at Escherichia coli O157:H7 in Feedlot Cattle. J Food Protect 73: 1304–1312. doi: 10.4315/0362-028X-73.7.1304
    [30] Saez AC, Zhang J, Rostagno MH, et al. (2011) Direct feeding of microencapsulated bacteriophages to reduce Salmonella colonization in pigs. Foodborne Pathog Dis 8: 1241–1248. doi: 10.1089/fpd.2011.0868
    [31] Ma Y, Pacan CJ, Wang Q (2008) Microencapsulation of bacteriophage felix O1 into chitosan- alginate microspheres for oral delivery. Appl Environ Microb 74: 4799–4805. doi: 10.1128/AEM.00246-08
    [32] EFSA (European Food Safety Authority), ECDC (European Centre for Disease Prevention and Control) (2017) The European Union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2016. EFSA J 15: 5077.
    [33] Word Health Organzation (2019) Food safety. Available from: https://www.who.int/news-room/fact-sheets/detail/food-safety.
    [34] Moye ZD, Woolstone J, Sulakvelidze A (2018) Bacteriophage Applications for Food Production and Processing. Viruses 10: 1–22.
    [35] Endersen L, O'Mahony J, Hill C, et al. (2014) Phage Therapy in the Food Industry. Annu. Rev Food Sci Technol 5: 327–349. doi: 10.1146/annurev-food-030713-092415
    [36] de Melo AG, Levesque S, Moineau S (2018) Phages as friends and enemies in food processing. Curr Opin Biotechnol 49: 185–190. doi: 10.1016/j.copbio.2017.09.004
    [37] Atterbury RJ, Connerton PL, Dodd CE, et al. (2003) Application of host-specific bacteriophages to the surface of chicken skin leads to a reduction in recovery of Campylobacter jejuni. Appl Environ Microb 69: 6302–6306. doi: 10.1128/AEM.69.10.6302-6306.2003
    [38] Goode D, Allen VM, Barrow PA (2003) Reduction of experimental Salmonella and Campylobacter contamination of chicken skin by application of lytic bacteriophages. Appl Environ Microb 69: 5032–5036. doi: 10.1128/AEM.69.8.5032-5036.2003
    [39] Bigwood T, Hudson JA, Billington C (2009) Influence of host and bacteriophage concentrations on the inactivation of food-borne pathogenic bacteria by two phages. FEMS Microbiol Lett 291: 59–64. doi: 10.1111/j.1574-6968.2008.01435.x
    [40] Orquera S, Golz G, Hertwig S, et al. (2012) Control of Campylobacter spp. and Yersinia enterocolitica by virulent bacteriophages. J Mol Genet Med 6: 273–278.
    [41] O'Flynn G, Ross RP, Fitzgerald GF, et al. (2004) Evaluation of a cocktail of three bacteriophages for biocontrol of Escherichia coli O157:H7. Appl Environ Microb 70: 3417–3424. doi: 10.1128/AEM.70.6.3417-3424.2004
    [42] Abuladze T, Li M, Menetrez MY, et al. (2008) Bacteriophages reduce experimental contamination of hard surfaces, tomato, spinach, broccoli, and ground beef by Escherichia coli O157:H7. Appl Environ Microb 74: 6230–6238. doi: 10.1128/AEM.01465-08
    [43] Sharma M, Patel JR, Conway WS, et al. (2009) Effectiveness of bacteriophages in reducing Escherichia coli O157:H7 on fresh-cut cantaloupe and lettuce. J Food Prot 72: 1481–1485. doi: 10.4315/0362-028X-72.7.1481
    [44] Carter CD, Parks A, Abuladze T, et al. (2012) Bacteriophage cocktail significantly reduced Escherichia coli O157H:7contamination of lettuce and beef, but does not protect against recontamination. Bacteriophage 2: 178–185. doi: 10.4161/bact.22825
    [45] Boyacioglu O, Sharma M, Sulakvelidze A, et al. (2013) Biocontrol of Escherichia coli O157: H7 on fresh-cut leafy greens. Bacteriophage 3: 1–6.
    [46] Viazis S, Akhtar M, Feirtag J, et al. (2011) Reduction of Escherichia coli O157:H7 viability on leafy green vegetables by treatment with a bacteriophage mixture and trans-cinnamaldehyde. Food Microbiol 28: 149–157.
    [47] Patel J, Sharma M, Millner P, et al. (2011) Inactivation of Escherichia coli O157:H7 attached to spinach harvester blade using bacteriophage. Foodborne Pathog Dis 8: 541–546. doi: 10.1089/fpd.2010.0734
    [48] Carlton RM, Noordman WH, Biswas B, et al. (2005) Bacteriophage P100 for control of Listeria monocytogenes in foods: genome sequence, bioinformatic analyses, oral toxicity study, and application. Regul Toxicol Pharm 43: 301–312. doi: 10.1016/j.yrtph.2005.08.005
    [49] Holck A, Berg J (2009) Inhibition of Listeria monocytogenes in cooked ham by virulent bacteriophages and protective cultures. Appl Environ Microbiol 75: 6944–6946 . doi: 10.1128/AEM.00926-09
    [50] Soni KA, Nannapaneni R., Hagens S (2010) Reduction of Listeria monocytogenes on the surface of fresh channel catfish fillets by bacteriophage listex p100. Foodborne Pathog Dis 7: 427–434 . doi: 10.1089/fpd.2009.0432
    [51] Soni KA, Desai M, Oladunjoye A, et al. (2012) Reduction of Listeria monocytogenes in queso fresco cheese by a combination of listericidal and listeriostatic GRAS antimicrobials. Int J Food Microbiol 155: 82–88. doi: 10.1016/j.ijfoodmicro.2012.01.010
    [52] Chibeu A, Agius L, Gao A, et al. (2013) Efficacy of bacteriophage LISTEXTM P100 combined with chemical antimicrobials in reducing Listeria monocytogenes in cooked turkey and roast beef. Int J Food Microbiol 167: 208–214. doi: 10.1016/j.ijfoodmicro.2013.08.018
    [53] Figueiredo ACL, Almeida RCC (2017) Antibacterial efficacy of nisin, bacteriophage P100 and sodium lactate against Listeria monocytogenes in ready-to-eat sliced pork ham. Braz J Microbiol 48: 724–729. doi: 10.1016/j.bjm.2017.02.010
    [54] Guenther S, Loessner MJ (2011) Bacteriophage biocontrol of Listeria monocytogenes on soft ripened white mold and red-smear cheeses. Bacteriophage 1: 94–100. doi: 10.4161/bact.1.2.15662
    [55] Bigot B, Lee WJ, McIntyre L, et al. (2011) Control of Listeria monocytogenes growth in a ready-to-eat poultry product using a bacteriophage. Food Microbiol 28: 1448–1452. doi: 10.1016/j.fm.2011.07.001
    [56] Modi R, Hirvi Y, Hill A, et al. (2001) Effect of phage on survival of Salmonella Enteritidis during manufacture and storage of cheddar cheese made from raw and pasteurized milk. J Food Protect 64: 927–933. doi: 10.4315/0362-028X-64.7.927
    [57] Leverentz B, Conway WS, Camp MJ, et al. (2003) Biocontrol of Listeria monocytogenes on fresh-cut produce by treatment with lytic bacteriophages and a bacteriocin. Appl Environ Microbiol 69: 4519–4526. doi: 10.1128/AEM.69.8.4519-4526.2003
    [58] Whichard JM, Sriranganathan N, Pierson FW, et al. (2003) Suppression of Salmonella growth by wild-type and large-plaque variants of bacteriophage Felix O1 in liquid culture and on chicken frankfurters. J Food Prot 66: 220–225. doi: 10.4315/0362-028X-66.2.220
    [59] Guenther S, Herzig O, Fieseler L, et al. (2012) Biocontrol of Salmonella Typhimurium in RTE foods with the virulent bacteriophage FO1-E2. Int J Food Microbiol 154: 66–72. doi: 10.1016/j.ijfoodmicro.2011.12.023
    [60] Spricigo DA, Bardina C, Cortés P, et al. (2013) Use of a bacteriophage cocktail to control Salmonella in food and the food industry. Int J Food Microbiol 165: 169–174. doi: 10.1016/j.ijfoodmicro.2013.05.009
    [61] Farber JM, Peterkin PI (1991) Listeria monocytogenes, a foodborne pathogen. Microbiol Rev 55: 476–511.
    [62] Leistner L, Gorris LGM (1995) Food preservation by hurdle technology. Trends Food Sci Technol 6: 41–46 . doi: 10.1016/S0924-2244(00)88941-4
    [63] Phages as probiotics. Available from: http://intralytix.com/index.php?page=pro.
    [64] Proteon Pharmaceuticals. Available from: https://www.proteonpharma.com.
    [65] Schmelcher M, Loessner JM (2016) Bacteriophage endolysins: applications for food safety. Curr Opin Biotechnol 37: 76–87. doi: 10.1016/j.copbio.2015.10.005
    [66] Gutiérrez D, Rodríguez-Rubio L, Martíne B, et al. (2016) Bacteriophages as weapons against bacterial biofilms in the food industry. Front Microbiol 7: 1–16.
    [67] Da Silva Felício MT, Hald T, Liebana E, et al. (2015) Risk ranking of pathogens in ready-to-eat unprocessed foods of non-animal origin (FoNAO) in the EU: initial evaluation using outbreak data (2007–2011). Int J Food Microbiol 16: 9–19.
    [68] Beuchat LR (2002) Ecological factors influencing survival and growth of human pathogens on raw fruits and vegetables. Microbes Infect 4: 413–423. doi: 10.1016/S1286-4579(02)01555-1
    [69] Siringan P, Connerton PL, Payne RJ (2011) Bacteriophage-mediated dispersal of Campylobacter jejuni biofilms. Appl Environ Microb 77: 3320–3326. doi: 10.1128/AEM.02704-10
    [70] Soni KA, Nannapaneni R, Hagens S (2010) Reduction of Listeria monocytogenes on the surface of fresh channel catfish fillets by bacteriophage listex p100. Foodborne Pathog Dis 7: 427–434. doi: 10.1089/fpd.2009.0432
    [71] Sutherland IW, Hughes KA, Skillman LC, et al. (2004) The interaction of phage and biofilms. FEMS Microbiol Lett 232: 1–6. doi: 10.1016/S0378-1097(04)00041-2
    [72] Maszewska A (2015) Phage associated polysaccharide depolymerases–characteristics and application. Postep Hig Med Dos 69: 690–702. doi: 10.5604/17322693.1157422
    [73] Drulis-Kawa Z, Majkowska-Skrobek G, Maciejewska B (2015) Bacteriophages and phage- derived proteins--application approaches. Curr Med Chem 22: 1757–1773. doi: 10.2174/0929867322666150209152851
    [74] Lehman SM (2007) Development of a bacteriophage-based biopesticide for fire blight. PhD Thesis. Department of Biological Sciences, Brock University, Canada.
    [75] Hughes KA, Sutherland IW, Jones MV (1998) Biofilm susceptibility to bacteriophage attack: the role of phage-borne polysaccharide depolymerase. Microbiology 144: 3039–3047. doi: 10.1099/00221287-144-11-3039
    [76] Chai Z, Wang J, Tao S, et al. (2014) Application of bacteriophage-borne enzyme combined with chlorine dioxide on controlling bacterial biofilm. LWT Food Sci Technol 59: 1159–1165. doi: 10.1016/j.lwt.2014.06.033
    [77] Love JM, Bhandari D, Dobson CR, et al. (2018) Potential for bacteriophage endolysins to supplement or replace antibiotics in food production and clinical care. Antibiotics 7: 1–25.
    [78] Gutierrez D, Ruas-Madiedo P, Martınez B (2014) Effective removal of Staphylococcal biofilms by the endolysin LysH5. PloS One 9: 1–8.
    [79] Oliveira H, Thiagarajan V, Walmagh M (2014) A thermostable Salmonella phage endolysin Lys68, with broad bactericidal properties against gram-negative pathogens in presence of weak acids. PloS One 9: 1–11.
    [80] Obeso MJ, Martínez B, Rodríguez A, et al. (2008) Lytic activity of the recombinant staphylococcal bacteriophage ΦH5 endolysin active against Staphylococcus aureus in milk. Int J Food Microbiol 128: 212–218. doi: 10.1016/j.ijfoodmicro.2008.08.010
    [81] Olsen NMC, Thiran E, Hasler T, et al. (2018) Synergistic removal of static and dynamic Staphylococcus aureus biofilms by combined treatment with a bacteriophage endolysin and a polysaccharide depolymerase. Viruses 10: 2–17.
    [82] Yoyeon Ch, Son B, Ryu S (2019) Effective removal of staphylococcal biofilms on various food contact surfaces by Staphylococcus aureus phage endolysin LysCSA13. Food Microbiol 84: 1–7.
    [83] Zhang H, Bao H, Billington C (2012) Isolation and lytic activity of the Listeria bacteriophage endolysin LysZ5 against Listeria monocytogenes in soya milk. Food Microbiol 31: 133–136. doi: 10.1016/j.fm.2012.01.005
    [84] Van Nassau TJ, Lenz CA, Scherzinger AS (2017) Combination of endolysins and high pressure to inactivate Listeria monocytogenes. Food Microbiol 68: 81–88. doi: 10.1016/j.fm.2017.06.005
    [85] Gaeng S, Scherer S, Neve H (2000) Gene cloning and expression and secretion of Listeria monocytogenes bacteriophage-lytic enzymes in Lactococcus lactis. Appl Environ Microb 66: 2951–2958. doi: 10.1128/AEM.66.7.2951-2958.2000
    [86] Garneau EJ, Moineau S (2001) Bacteriophages of lactic acid bacteria and their impact on milk fermentations. Microb Cell Fact 10: 1–10.
    [87] Atamer Z, Samtlebe M, Neve H, et al. (2013) Review: elimination of bacteriophages in whey and whey products. Front Microbiol 4: 1–9.
    [88] Mercanti D, Carminati D, Reinheimer JA, et al. (2011) Widely distributed lysogeny in probiotic lactobacilli represents a potentially high risk for the fermentative dairy industry. Int J Food Microbiol 144: 503–510. doi: 10.1016/j.ijfoodmicro.2010.11.009
    [89] Tahir A, Asif M, Abbas Z (2017) Three bacteriophages SA, SA2 and SNAF can control growth of milk isolated Staphylococcal species. Pak J Zool 49: 425–759. doi: 10.17582/journal.pjz/2017.49.2.425.434
    [90] Singh A, Poshtiban S, Evoy S (2013) Recent advances in bacteriophage based biosensors for food-borne pathogen detection. Sensors 13: 1763–1786. doi: 10.3390/s130201763
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