Review Special Issues

Bacteriophages—a new hope or a huge problem in the food industry

  • 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

    Related Papers:

    [1] Churni Gupta, Necibe Tuncer, Maia Martcheva . Immuno-epidemiological co-affection model of HIV infection and opioid addiction. Mathematical Biosciences and Engineering, 2022, 19(4): 3636-3672. doi: 10.3934/mbe.2022168
    [2] Churni Gupta, Necibe Tuncer, Maia Martcheva . A network immuno-epidemiological model of HIV and opioid epidemics. Mathematical Biosciences and Engineering, 2023, 20(2): 4040-4068. doi: 10.3934/mbe.2023189
    [3] Hui Jiang, Ling Chen, Fengying Wei, Quanxin Zhu . Survival analysis and probability density function of switching heroin model. Mathematical Biosciences and Engineering, 2023, 20(7): 13222-13249. doi: 10.3934/mbe.2023590
    [4] Gerardo Chowell, Zhilan Feng, Baojun Song . From the guest editors. Mathematical Biosciences and Engineering, 2013, 10(5&6): i-xxiv. doi: 10.3934/mbe.2013.10.5i
    [5] Xi-Chao Duan, Xue-Zhi Li, Maia Martcheva . Dynamics of an age-structured heroin transmission model with vaccination and treatment. Mathematical Biosciences and Engineering, 2019, 16(1): 397-420. doi: 10.3934/mbe.2019019
    [6] Christopher M. Kribs-Zaleta . Sociological phenomena as multiple nonlinearities: MTBI's new metaphor for complex human interactions. Mathematical Biosciences and Engineering, 2013, 10(5&6): 1587-1607. doi: 10.3934/mbe.2013.10.1587
    [7] Aditya S. Khanna, Dobromir T. Dimitrov, Steven M. Goodreau . What can mathematical models tell us about the relationship between circular migrations and HIV transmission dynamics?. Mathematical Biosciences and Engineering, 2014, 11(5): 1065-1090. doi: 10.3934/mbe.2014.11.1065
    [8] Cristian Tomasetti, Doron Levy . An elementary approach to modeling drug resistance in cancer. Mathematical Biosciences and Engineering, 2010, 7(4): 905-918. doi: 10.3934/mbe.2010.7.905
    [9] H. Thomas Banks, W. Clayton Thompson, Cristina Peligero, Sandra Giest, Jordi Argilaguet, Andreas Meyerhans . A division-dependent compartmental model for computing cell numbers in CFSE-based lymphocyte proliferation assays. Mathematical Biosciences and Engineering, 2012, 9(4): 699-736. doi: 10.3934/mbe.2012.9.699
    [10] Adam Peddle, William Lee, Tuoi Vo . Modelling chemistry and biology after implantation of a drug-eluting stent. Part Ⅱ: Cell proliferation. Mathematical Biosciences and Engineering, 2018, 15(5): 1117-1135. doi: 10.3934/mbe.2018050
  • 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.


    1. Introduction

    Oil exploration and exploitation activities in addition to refining and distribution often lead to spillages that pollute the aquatic and terrestrial environment. The ecological impact of petroleum pollutants have been well documented [1,2,3,4]. Decontamination of oil-polluted environment involves mechanical, chemical and biological measures. Apart from cost, mechanical and chemical methods of treatment can lead to incomplete removal of the hydrocarbons [5] and the chemical dispersants and surfactants often used, may be toxic to the environment [6]. Microbiological techniques involve bioremediation which is a less expensive and ecologically friendly alternative for restoring the integrity of contaminated soils. It is a natural process that relies on the metabolic activities of microorganisms to degrade pollutants. A variety of microorganisms are known to be capable of degrading hydrocarbons [7], but the extent depends on the availability of nutrients such as nitrogen and phosphorus[8]. Studies have shown that addition of nitrogen and phosphorus in form of fertilizers enhances biodegradation of hydrocarbons [9]. Animal wastes (poultry droppings, cow and pig dung) as less costly source of nutrients [6] have also been used because they contain nitrogen, phosphorus and trace elements needed for microbial metabolism [10,11,12]. The animal wastes also contain a variety of microorganisms that may combine with the resident microflora of oil-polluted environment to degrade hydrocarbons.

    However, researchers often ignore the possibility that the microflora of the animal may degrade hydrocarbon as much as the resident microflora of oil-polluted environments. This study was therefore designed to test two bacterial isolates from animal wastes (poultry and pig droppings) for crude oil degradation potential; and compare their crude oil degradation capability with that of the same bacterial species isolated from soil with history of petroleum contamination in the presence and absence of the animal wastes.


    2. Materials and Methods


    2.1. Isolation of hydrocarbon-utilizing bacteria

    Soil samples were obtained from the oil-producing Niger Delta soil in an area with a history of petroleum spillage based on personal knowledge. The soil samples were collected with polythene bags that were previously sterilized by immersion in 3.5% (w/v) sodium hypochlorite solution for 12 hours. The soil was collected at depths of 5, 10 and 15 cm and bulked together for homogeneity. Thereafter, 1 mL aliquot of the serially diluted soil was used to streak mineral salts agar incorporated with crude oil (crude oil, 10 mL; KH2PO4, 1.0 g; K2HPO4, 1.0 g; NH4NO3, 0.2 g; MgSO4·7H2O, 0.2 g; FeCl2, 0.05 g; CaCl2·2H2O, 0.02 g; distilled water, 1000 mL, pH 7.0). The crude oil (Escravos light) used was obtained from Warri Refining and Petrochemical Company, Delta State, Nigeria. After 72 h incubation at room temperature (30 ± 2 ℃) emerging colonies were transferred to Nutrient Agar plates and further sub-cultured for purification. The same procedure was used to isolate hydrocarbon-utilizing bacteria from poultry and pig wastes collected from Mannes Farms, New-layout, Ekpan, Delta State, Nigeria.


    2.2. Selection of isolates with the best hydrocarbon-utilizing capacity

    The 2, 6-dichlorophenol indophenol method[13] was used to screen the crude oil degradation ability of the isolates. A loopful of each isolate was introduced into 7.5 mL of mineral salts medium containing 50 μL of crude oil before 40 μL of 2, 6-dichlorophenol indophenol (DCPIP) was added and incubated at room temperature (30 ± 2 ℃) for five days. The isolates, (two from each animal wastes and two from oil-polluted soil) that discoloured the medium in the shortest time were selected. The selection was confirmed by spectrophotometric analyses at 600 nm where the isolates that caused the lowest absorbance were matched with those selected by the visual method. The organisms were subsequently identified by cultural, microscopic and biochemical tests based on Bergeys Manual of Determinative Bacteriology [14]. For the purpose of the comparative experiment on biodegradation of crude oil in soil, two identical bacterial species from each of the animal wastes and oil-polluted soil were chosen. This brought the number of bacterial strains used for the experiment to six.


    2.3. Determination of some physical and chemical characteristics of test soil and animal wastes

    The pH of the garden soil and animal wastes used for the experiments was determined in distilled water using a digital pH meter. It was standardized with buffer solutions of pH 4, 7 and 9. Moisture content was determined by gravimetry based on oven dry weight. Total organic carbon, total nitrogen and phosphorus were analyzed by potassium dichromate, Kjeldhal and hypochlorate, methods, respectively [15].


    2.4. Biodegradation of crude oil in soil with and without amendment with animal wastes

    Garden soil samples weighing 500 g were placed in flasks and sterilized by autoclaving at 121 ℃ for 30 mins. Upon cooling, the soil in six replicate flasks was mixed with filter-sterilized crude oil at 50 mL/flask. Thereafter, the flasks were inoculated with 10 mL normal saline suspension of 106 test bacterial isolate. This inoculum size was determined by plate count on Nutrient Agar plates. The set-up was repeated for each of the six test bacterial strains and set aside on the laboratory bench at room temperature for six weeks. The flasks were manually turned over for aeration and moistened with 10 mL sterile tap water at weekly intervals. The control flasks were not inoculated. After incubation for six weeks, the flask contents were extracted with hexane and subsequently analysed for TPH by gas chromatography. The concentrations were recorded in ppm. The reduction of TPH was calculated by subtracting the concentration (ppm) in test flasks from that of control and expressing it as % loss. The n-alkanes were quantified with a range of C8-C36 and the reduction of each chain was similarly expressed as % loss. The above experiment was repeated with soils mixed separately with 50 g poultry or pig wastes. The animal wastes were also sterilized by autoclave at 121 ℃ for 30 mins. The control flasks were not inoculated with the test bacterial strains. The differences in TPH concentrations in all inoculated flasks and un-inoculated control flask were analyzed by one-way Analysis of Variance (ANOVA) and Tukey post hoc multiple comparison tests using SPSS version 22.


    2.5. Growth of selected bacterial isolates in sterilized garden soil amended with animal wastes

    Freshly obtained poultry and pig wastes samples were separately mixed with garden soil at a ratio of 1:1 and dispensed into 50 mL flasks in 10 g quantities before sterilisation by autoclave at 121 ℃ for 30 mins. The control flask contained garden soil only. Each of the six bacterial strains from the three sources was used to inoculate three separate flasks as illustrated in Table 1. This brought the total number of flasks inoculated to 18. A 1 mL normal saline suspension of 106bacterial strains served as inoculum. The flasks were manually shaken to ensure even mixture. The overall set up was in three replicates. The flasks were incubated at room temperature for 14 days and moistened with 1 mL sterile tap water on the 7th day. At intervals of two days, 1 g samples were aseptically withdrawn and analysed for bacterial population by plate counts on Nutrient Agar after appropriate serial dilutions.

    Table 1. Inoculation arrangement for determining the growth of test bacteria in soil amended with animal wastes
    Bacteria Source of bacteria Medium
    Soil + poultry waste Soil + pig waste Soil only (control)
    P. vulgaris
    B. subtilis
    Petroleum-contaminated soil Poultry waste
    Pig waste
    Petroleum-contaminated soil
    Poultry waste
    Pig waste
    +
    +
    +
    +
    +
    +
    +
    +
    +
    +
    +
    +
    +
    +
    +
    +
    +
    +
    +, present
     | Show Table
    DownLoad: CSV

    3. Results and discussion

    Over 35 bacterial isolates were screened for crude oil degradation ability and 12 were selected based on their high identical crude oil degradation ability. The identity of the 12 strains is presented in Table 2. However, Proteus vulgaris and Bacillus subtilis were the only strains selected for subsequent experiments because they were the only identical isolates encountered in both petroleum-polluted soil and animal wastes (Table 2). It was considered more reliable to use identical strains for the purpose of comparing the influence of their sources (animal waste, petroleum-contaminated soil) on their crude oil biodegradation potential.

    Table 2. Bacterial isolates with substantial crude oil degradation potential
    Source of bacteria Bacteria
    Oil-polluted soil Bacillus subtilis
    Proteus vulgaris
    Poultry waste
    Pig waste
    Acinetobacter sp.
    Arthrobacter sp.
    Bacillus cereus
    Klebsiella sp.
    Proteus vulgaris
    Bacillus subtilis
    Enterobacter aerogenes
    Bacillus subtilis
    Proteus vulgaris
    Enterococcus faecalis
     | Show Table
    DownLoad: CSV

    The degradation of crude oil by the three strains of Proteus vulgaris was significant when compared to control. However, there was no significant difference in the degradation caused by the three strains (poultry waste, pig waste, petroleum-polluted soil) in normal soil (Table 3). Over 75.5% of the total petroleum hydrocarbon (TPH) in both normal and amended soil was degraded by the bacterial strains. However, degradation of TPH in soil amended with animal wastes was significantly greater than in normal soil. This was not unexpected, because previous reports show that biodegradation of petroleum hydrocarbon is enhanced in soil treated with animal wastes [11,12,16,17]. The results in Table 3 further show that degradation of crude oil by animal waste strains of P. vulgaris was significantly enhanced in soil amended with animal wastes when compared to degradation by the strain from oil-polluted soil. Degradation of crude oil in poultry waste-amended soil by the poultry waste strain of P. vulgaris was significantly more enhanced than degradation by the pig waste strain. However, such significant difference did not occur in soil amended with pig waste. The above trend was similarly encountered in the degradation of crude oil by the three strains of Bacillus subtilis as shown in Table 4.

    Table 3. Biodegradation of crude oil in normal and animal waste-amended soil by Proteus vulgaris isolated from three sources
    Crude oil medium Source of P. v ulgaris Mean TPH (ppm ± SD) after 6 weeks Reduction of TPH (%)
    Normal soil Petroleum-contaminated soil
    Poultry waste
    ab20.5 ± 0.1
    ab19.2 ± 0.1
    75.5
    78.1
    Poultry
    waste-amended
    soil
    Pig
    waste-amended
    soil
    Pig waste
    Control
    Petroleum-contaminated soil
    Poultry waste
    Pig waste
    Control
    Petroleum-contaminated soil
    Poultry waste
    Pig waste
    Control
    ab19.0 ± 0.1
    104.5 ± 3.8
    ac11.7 ± 0.02
    ac2.8 ± 0.01
    ac4.8 ± 0.01
    102.5 ± 4.0
    ac10.4 ± 0.05
    abc4.5 ± 0.02
    abc4.2 ± 0.03
    a103.4 ± 3.6
    8.8
    0.0
    88.6
    97.3
    95.3
    0.0
    89.9
    95.6
    95.9
    0.0
    Control = Not inoculated with P vulgaris (See Materials and Methods). Significant difference: from control, aP < 0.0001; between sources of P. vulgaris, bP > 0.05, cP < 0.001.
     | Show Table
    DownLoad: CSV

    The observation that degradation of crude oil by the animal waste isolates was enhanced in the presence of animal wastes when compared to strains from petroleum-polluted soil suggests the influence of ecological niche adaptation. Going by this concept, highly enhanced biodegradation ability was expected from the petroleum-polluted soil strains given their frequent exposure to petroleum contaminants. But it was not the case. The plausible explanation lies in the adaptation ability of the bacterial isolates to exact nutrients from the animal wastes as biostimulants. The attendant population growth would therefore, result in greater attack on the petroleum hydrocarbon. The animal waste strains can therefore, be seen as better placed to exact the nutrients. The observation that degradation of crude oil by animal waste strains was enhanced in soil amended with the wastes lends credence to this inference. This deduction is supported by the results presented in Figure 1, which showed that the growth of the animal waste bacterial strains was markedly greater than that of petroleum-polluted soil strains in soil mixed with animal wastes. The influence of the nutrients in animal wastes and the greater degradation ability of the bacterial strains from animal wastes were further demonstrated by the results of biodegradation of n-alkane chains (Figures 2). All the bacterial strains expectedly preferentially degraded the shorter chains (C8-C23) in normal and animal waste-amended soil as shown in Figure 2. The pattern of degradation of the alkane chains in normal soil by all the bacterial strains were not markedly different. However, there was marked increase in the degradation of the longer chains in soils amended with animal wastes when compared to biodegradation in normal soil. Compared to other strains, degradation of longer chains of n-alkane (C24-C36) by poultry waste strains in soil amended with poultry waste markedly increased. Degradation of longer chains by pig waste strains followed a similar pattern (Figures 2).

    Figure 1. Growth of P. vulgaris and B. subtilis in soil and soil amended with animal wastes. *Source of strains of P. vulgaris and B. subtilis.
    Figure 2. Loss of n-alkane after degradation of crude oil for 6 weeks by Proteus vulgaris and B. subtilis in soil and soil amended with animal wastes. *Source of strains of P. vulgaris and B. subtilis.
    Table 4. Biodegradation of crude oil in normal and animal waste-amended soil by Bacillus subtilis isolated from three sources
    Crude oil medium Source of B. subtilis Mean TPH (ppm ± SD) after 6 weeks Reduction of TPH (%)
    Normal soil Petroleum-contaminated soil
    Poultry waste
    ab18.7 ± 0.4
    ab17.9 ± 0.3
    72.1
    72.8
    Poultry waste-amended soil
    Pig
    waste-amended
    soil
    Pig waste
    Control
    Petroleum-contaminated soil
    Poultry waste
    Pig waste
    Control
    Petroleum-contaminated soil
    Poultry waste
    Pig waste
    Control
    ab18.0 ± 0.3
    104.5 ± 3.8
    ac13.4 ± 0.1
    ac3.4 ± 0.01
    ac6.5 ± 0.01
    102.5 ± 4.0
    ac12.0 ± 0.1
    ac4.3 ± 0.02
    ac7.0 ± 0.03
    103.4 ± 3.6
    74.7
    0.0
    89.1
    96.6
    93.6
    0.0
    88.3
    95.8
    93.2
    0.0
    Control = Not inoculated with B. subtilis (See Materials and Methods). Significant difference from control: aP < 0.0001; between sources of B. subtilis, bP > 0.05, cP < 0.001.
     | Show Table
    DownLoad: CSV

    While it is acknowledged that preferential degradation of hydrocarbons by microorganisms depends on their metabolic machinery, inadequate or absence of vital nutrients (nitrogen and phosphorus) would generally impede their metabolism [18] irrespective of their hydrocarbon specificity. It is known that alkanes of C10-C24 length are more easily degraded [19] hence microorganisms tend to begin degradation with these intermediate chain lengths before the longer chains. Depending on the environment, the vital nutrients may become exhausted before the attack on the longer chain hydrocarbons begins. Thus the ability of the organism to exact nutrients from available sources such as animal wastes is likely to promote attack on longer chains as indicated by the results of this study. Some reports [10,11,12] have shown that animal wastes contain nitrogen, phosphorus and minerals that can act as biostimulants. The results of the analyses of some of the physical and chemical characteristics of the test garden soil and the animal wastes showed that concentrations of nitrogen and phosphorus were markedly higher in the animal wastes than in test soil (Table 5). Indeed phosphorus was not detected in the test soil. The alkaline pH of the animal wastes would be favorable to the strains than the acidic pH of the test soil, because bacteria tend to thrive better in neutral to alkaline environment.

    Table 5. Some physical and chemical properties of the soil and animal wastes used for hydrocarbon biodegradation tests
    Physico-chemical parameters Soil Source of animal waste
    Poultry Pig
    pH
    Moisture content (%)
    6.3 ± 0.11
    3.1 ± 0.14
    8.7 ± 0.57
    20.9 ± 0.71
    8.3 ± 0.13
    23.7 ± 0.16
    Total organic carbon (%)
    Total Nitrogen (%)
    27.1 ± 0.01
    0.05 ± 0.00
    44.5 ± 0.01
    0.12 ± 0.01
    44.6 ± 0.00
    0.09 ± 0.01
    Phosphorus (%) 0.00 ± 0.00 0.01 ± 0.00 0.01 ± 0.00
    Values in the table represent Mean ± SD
     | Show Table
    DownLoad: CSV

    The results indicated that the animal waste strains may have become adapted to the physical and chemical characteristics of the wastes (Table 5) hence they thrived better than the strains from soil polluted by petroleum hydrocarbon in the presence of the animal wastes. After all, the animal waste nutrients were also available to the petroleum-polluted soil strains. The specificity of adaptation was further indicated by the observation that each of the animal waste strains tended to degrade n-alkane better in the presence of the waste from which they originated. Adaptation is a natural phenomenon that ensures the survival and perpetuation of organisms in their habitats where they face physical and chemical challenges. Survival therefore depends on the ability of the organisms to develop appropriate metabolic mechanisms that will enable them overcome the physical and chemical hurdles in their environment [20].


    4. Conclusion

    The results of the investigation indicate that the microflora of animal wastes are prominent in biodegradation of hydrocarbon in polluted soils where animal wastes have been applied for biostimulation. The greater growth of the animal waste strains in animal waste-amended soil when compared to petroleum-polluted soil strains increased the attack on the crude oil. Thus bioaugmentation and biostimulation may be achieved in bioremediation of petroleum-polluted sites if it includes the use of animal wastes such as poultry droppings and pig dung.


    Conflict of interest

    The research was self-funded. The authors declare that there is no conflict of interest.



    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
  • Reader Comments
  • © 2019 the Author(s), licensee AIMS Press. This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0)
通讯作者: 陈斌, bchen63@163.com
  • 1. 

    沈阳化工大学材料科学与工程学院 沈阳 110142

  1. 本站搜索
  2. 百度学术搜索
  3. 万方数据库搜索
  4. CNKI搜索

Metrics

Article views(11622) PDF downloads(1506) Cited by(120)

Article outline

Figures and Tables

Tables(2)

Other Articles By Authors

/

DownLoad:  Full-Size Img  PowerPoint
Return
Return

Catalog