Physical Methods Used to Inactivate Bacteriophages: History
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Subjects: Biochemistry & Molecular Biology
Contributor:
Monika Karczewska
,
Patryk Strzelecki
,
Agnieszka Szalewska-Pałasz
,
Dariusz Nowicki

Bacteriophage-based applications have a renaissance today, increasingly marking their use in industry, medicine, food processing, biotechnology, and more. However, phages are considered resistant to various harsh environmental conditions; besides, they are characterized by high intra-group variability. Phage-related contaminations may therefore pose new challenges in the future due to the wider use of phages in industry and health care. The risk of bacteriophage infection can be reduced by several techniques, including sterilization by physical agents.

  • bacteriophages
  • contamination
  • eradication
  • phage decontamination

1. Thermal Disinfection

Temperature regulation is a well-known method that has been used for decades or even centuries as the main method of environmental microorganism inactivation; also, it is widely used in the food industry [1]. Most bacteriophage inactivation research is focused on the application of thermal disinfection [2][3][4][5][6][7][8][9][10][11][12][13][14][15][16][17][18][19]. Additionally, when using microwave radiation, it is the thermal effect that is associated with the inactivation of bacteriophages, compared to the application of radiation under non-thermal conditions [20]. Such conclusions were reached by Bryant et al. in an attempt to explain the mechanism of inactivation by microwave radiation of bacteriophage T4 that occurs within 20 s when compared to control samples treated on ice [20]. The mechanism of inactivation is most likely related to damage of the capsid, but before reaching the melting point, DNA is released [14][15]. The most studied application of this disinfection method is the control of bacteriophages infecting lactic acid bacteria (LAB) [21]. Among these bacteriophages, there are some that can survive pasteurization due to their high heat resistance, e.g., P680, P1532, and P008 [6][8][22]. Another interesting finding from these studies is the importance of the culture medium and its composition for bacteriophage inactivation efficiency. In the presence of fat, phage survival increases which is related to its protective effect by keeping the particles moist [2][3][4]. Such conclusions were reached, among others, by Muller-Merbach et al., who inactivated the model phage P008 in selective M17 broth and milk. In the case of M17 broth, the higher the temperature used, the faster the inactivation progressed. Exposure to 55 °C led to a 1-log reduction within 3 h. Under short-term pasteurization conditions (i.e., 30 s at 75 °C), about 1 log of the phage population was inactivated, with a 7-log decrease after 6 min at this temperature. In comparison, inactivation in milk proceeded more slowly. At 55 °C, the phage titer hardly dropped even after 24 h, and short pasteurization conditions reduced the P008 titer by less than 1 log [2][3][4].

2. UV Radiation

UV radiation has been a validated technology for disinfecting surfaces as well as in air and water. It can eradicate a wide range of microorganisms. UV radiation is becoming an increasingly affordable method that yields reproducible significant reductions of infection [23][24]. Factors that may be involved in phage susceptibility to UV wavelengths are the type of nucleic acids (DNA or RNA), genome structure (single- or double-stranded), guanine and cytosine content, lipid envelope, the size of the viral particle, as well as other features of molecular structure. Therefore, in general, bacteriophages containing single-stranded RNA or DNA are more sensitive to UV radiation than phages containing double-stranded RNA or DNA. Tseng et al. determined in their study that the UV dose causing 99% inactivation was twice as high for phages containing ssRNA/DNA (MS2 and ΦX-174, respectively) than for dsRNA/DNA (Φ6 and T7, respectively) [25]. For all four virus types, the survival fraction decreased exponentially with increasing dose, by either increasing the UV intensity or exposure time. Toxic UV photoproducts are usually thymine dimers, so RNA viruses are more resistant to UV damage than DNA viruses [26], with the UV dose causing 99.9% (4 log) reduction in bacteriophages for MS2 (RNA) versus PRD1 (DNA) was 65.2 and 31.6 mW/cm2, respectively. Similar results were observed [26][27][28][29][30][31] when MS2 or Qβ phage (RNA) was compared with ΦX-174 (DNA), obtaining results with higher UV sensitivity for DNA bacteriophage. Therefore, each bacteriophage may have different susceptibility to UV dose, and this affects the effectiveness of the UV disinfection [32][33][34]. Ultraviolet waves spectra are not exclusive for inactivation of bacteriophages. Several reports demonstrating phage sensitivity to visible light (VL) at 405 and 455 nm have been published [35][36][37]. Inactivation of microorganisms under visible light can be associated with photodynamic inactivation (PDI) where a photosensitizer is excited by specific wavelengths of visible light in the presence of oxygen that leads to the production of reactive oxygen species (ROS), ultimately resulting in structural damage. Tomb and colleagues studied the effect of violet-blue light on the reduction of phage ΦC31 (genetic material on form of dsDNA) [36]. For the 103 PFU/mL, they achieved a 2.7 log reduction after exposure to 0.3 kJ/cm2, while ΦC31 titer of 105 and 107 PFU/mL were successfully decreased by ~5- and 7 log after exposure to doses of 0.5 and 1.4 kJ/cm2, respectively, by 405 nm light. It should be noted here that the inactivation was effective if the phage was suspended in liquids or substrates containing appropriate light-sensitive components (photosensitive porphyrin molecules), while no reduction in phage titer was observed when suspended in PBS. However, the study by Vatter et al. demonstrated inactivation of the enveloped virus Φ6 at 7.2 kJ/cm2 [35]. The phage titer was reduced by more than three folds within 40 h without the addition of photosensitizers [35]. However, Φ6 phage differs in genetic material structure (dsRNA) and the presence of an envelope, which is in line with previous reports that the structure of a bacteriophage affects the conditions of the observed inactivation efficiency.
Phage-inactivating agents can also be used in combination with other technologies to increase disinfection efficiency, so the use of UV or visible light with ultrasound (US) shows synergistic effects. This has been proven by the study in which the simultaneous application of US and VL was more effective than US alone for MS2 inactivation [38]. Moreover, along with UV light, synergy has been shown in combination with US (bacteriophage from Klip river) [39], ozone (MS2 bacteriophage) [40], or silver ions (MS2 bacteriophage) [41].

3. Pressure and Humidity

The effect of pressure on bacteriophages appears to be effective at values greater than 300 MPa [42][43]; this has been particularly studied for lactic acid bacterial phages, which were resistant to pressure ≤100 MPa [44][45][46][47]. Electron microscope images showed shrunken phage heads containing or lacking DNA after applying pressure on T4 phage [48].
The least effective appears to be the impact of humidity, since many additional factors affect its efficiency, such as the structure of the bacteriophage. The survival rate of the non-sheath phage MS2 turns out to be better than that of the enveloped phage Φ6 [49]. The pH, presence of proteins and environmental factors also have an impact of phage sensitivity. Bacteriophages survive in the range of low and high values of relative humidity, which in addition is often correlated with temperature, and only the intermediate value of humidity is effective in virus eradication, which is also dependent on the phage type. While salt, pH and surfactant reduced survival under wide range of humidity conditions, proteins provided some protection against phage particles degradation [49][50][51][52][53][54][55][56]. Thus, the effect of chemical composition has a significant impact on relative humidity effectiveness, highlighting the importance of simultaneous investigation of different factors in bacteriophage survival.

4. Filtration

Filtration technology is not a new invention; however, due to a rapid development through modifications of membrane elements, it has been continuously improved in terms of performance over past 50 years. New materials with improved chemical and thermo-mechanical properties and better permeability and selectivity are increasingly applied. The development of membranes significantly increases the range of applications of filtration, hence in the literature one can find many studies on the use of the technique in industry, which includes purification of water and dairy products as well as wastewater and air. It is also being used in the production processes, the environment, and public health applications [57][58]. The rapid development of nanotechnology has sparked great interest in nanomaterials, which are excellent adsorbents, catalysts and sensors due to their large specific surface area and high reactivity. Several natural nanomaterials have been shown to have strong antimicrobial properties. These include, for example, carbon nanotubes (CNTs), which can enhance membrane filtration [59][60]. CNTs are graphene sheets, either single-walled (SWNT—single tube) or multi-walled (MWNT—several packed tubes) [61]. Research by Brady-Estevez et al. has shown that bacteriophages are removed by the CNT filter matrix through a deep filtration mechanism, that is, captured by bundles of nanotubes inside the SWNT layer [62]. The filter was developed using a microporous poly(vinylidene fluoride) (PVDF)-based membrane coated with a thin layer of SWNTs. A model virus particle, bacteriophage MS2, with a diameter of 27 nm, was employed and the results indicated complete removal of bacteriophage particles. This thickness of the SWNT layer removes 107 virus particles per mL (5–7 log) [62]. However, the removal of MS2 bacteriophages by the MWNT filter was 1.5 to 3 log higher than that observed in SWNTs [63]. Brady-Estevez et al. also determined the efficiency of the SWNT-MWNT hybrid layer on different bacteriophages, i.e., MS2, PRD1 and T4, which have different structures, ribonucleic acids, diameters, and isoelectric points [64]. The hybrid filter was expected to be more similar to the performance of the MWNT filter, since the nanotubes were made of 83% MWNT and only 17% SWNT, and SWNT alone had a much lower efficiency. However, the SWNT–MWNT dual filter performed better than the 100% MWNT filter, and is effective against a wide range of bacteriophages [64]. Nevertheless, the complex chemical compositions of solutions and the presence of impurities can affect filter performance. Phage removal increased at higher ionic strengths (NaCl) due to suppression of repulsive electrostatic interactions between viruses and nanotubes. The addition of divalent salts, on the other hand, had opposite effects. While CaCl2 increased the removal, probably due to the complexation of calcium ions with the phage surface, the addition of MgCl2 decreased the phage eradication [65]. This effect was also observed in other cases, and it was determined that SJC3 phage filtration was strongly dependent on the concentration and valence of the dominant cation in the pore fluid. While using a filtration system consisting of quartz sand-filled columns, column retention increased from 0% to 99.99% when the electrolyte composition was changed from NaCl to CaCl2 [66].

5. Femtosecond Laser

Another modern technique is femtosecond laser irradiation. These are ultra-short laser pulses that show great potential for disinfection. Work by Tsen et al. has shown that femtosecond infrared and visible lasers can inactivate phages, and they attribute this to a mechanism called pulsed stimulated Raman scattering (ISRS) [67][68][69][70][71][72][73][74]. It appears that during ISRS, vibrational excitation of the capsid and disruption of the protein coat occur. The sample’s exposure time to laser radiation in the study by Tsen et al. was about 1 h or longer and resulted in a 5-log reduction of M13 phage titer [70]. Gel electrophoresis results indicated that laser irradiation does not change the structure of single-stranded DNA but leads to the breaking of hydrogen/hydrophobic bonds or the separation of weak protein linkages in the envelope [70][73]. More recently, Berchtikou et al. used millijoule laser pulses (40 fs) with different exposure times (1–15 min) and different wavelengths (800, 400 nm separately of combined), pulse energy ~20 mJ, and repetition rate of 10 Hz [71]. According to data presented, the 4-log reduction of phage titer took 31 min with 800 nm wavelength of laser used. Further evaluation showed that longer exposure times and shorter excitation wavelengths result in greater reduction of viral counts. The maximum observed inactivation about 6 log was obtained using a femtosecond laser with a wavelength of 400 nm, energy of 20 mJ, and pulse width of 40 fs, after 15 min of exposure. The authors deduced that virus inactivation increases with increasing irradiation energy density and shortening wavelength [75].

6. Non-Thermal Plasma

A promising approach to sterilization and disinfection is the use of atmospheric pressure non-thermal plasma (APNTP). APNTP has potential advantages over standard chemical disinfectants and sanitizers. First of all, it uses non-toxic gases and is known for the absence of toxic products during its process. The effectiveness of disinfection is related to the generation of a large number of different active agents, including chemically reactive forms (oxygen and nitrogen), UV or electromagnetic fields [76]. There are several reports on the effectiveness of APNTPs in inactivating bacteriophages. Venezia et al. obtained a reduction in the PFU/mL of λ C-17 and lytic bacteriophage (Rambo; Microphage) by at least 4–6 logs after 10 min of exposure [77]. On the other hand, Yasuda et al. observed inactivation of λ phage by 6 logs after 20 s using stable plasma generated by dielectric barrier discharge (DBD) [78]. Both of these studies detected nucleic acid damage, as well as changes in coat proteins. During the investigation what factors could improve the efficiency of inactivation by plasma, it was found that the percentage concentration of oxygen in the carrier gas was positively correlated with the rate of phage inactivation (MS2). Namely, oxygen concentration (0.75%) and 3 min of exposure to a plasma source operating in a helium/oxygen gas mixture (99.25%:0.75%) resulted in 99.9% reduction of MS2, additionally, increasing the time to 9 min resulted in >7 log inactivation. Moreover, interesting results of pre-activation of water with plasma were also presented. Water was pre-treated with plasma (for 120 s for T4 or 80 s for Φ174 and MS2) and then mixed with suspensions of tested bacteriophages. After incubation for 4 and 8 h with such prepared water, the titer of bacteriophage T4 was reduced by about 7.2 and 8.8 orders of magnitude, respectively, indicating that the process was time-dependent. The titers of active bacteriophages Φ174 and MS2 decreased close to the detection limit. Moreover, the action of plasma alone for 100 s completely abolished the infectivity of bacteriophage T4 suspension, and a similar effect for the other two phages was obtained after 60 s [79] （Table 1）.
Table 1. The physical methods to eradicate bacteriophages.
Factor Phage Conditions Remarks/Mechanism References
Temperature P008, pll98, MS2, P680, P1532, PRD1, ΦX174, somatic coliphages, Bacteroides fragilis phage, Lactobacillus helveticus, Lactococcus lactis bacteriophages, OMKO1, HK97, λ, PP7, thermophilic Bacillus phages Medium temperature range from 55 °C to 100 °C Structural damage, protein denaturation
The medium plays an important role in terms of the thermal resistance of phages
P680 requires a higher temperature (from 100 °C for 20 min to 140 °C for 2 s)		 [2][3][4][5][6][7][8][9][10][11][12][13][14][15][16][17][18][19]
E. coli phage Inactivation in the wet and dry state In the dried state, rate of inactivation varies exponentially [80]
MS2 Low temperature 4–15 °C Reduction 15 °C after 30 days
Virus inactivation of 2 log at 15 °C after 30 days and reduction of 3.5 log at 25 °C after 28 days		 [81][82]
Pressure 832-B1, QP4, QF12, 13.2, B1, MLC-A, MLC-A8, ΦiLp84, ΦiLp1308 <100 MPa High pressure resistance [44][45]
P001, P008 0.1–600 MPa
25–80 °C		 Structural damage caused by pressure and heat combination. However, over a specific range of pressure and heat, they act antagonistically [46][47]
ΦX174, λ,T4, MS2 >300 MPa Structural damage caused by pressure: (1) phage with shrunken envelopes and DNA-containing heads; (2) phage with shrunken envelopes and heads lacking DNA. The ratio of the two types is strongly dependent on temperature used [42][43][48][83]
Irradiation MS2, S-13, C-36 and Staph-K, ΦX-174, B40-8 y-rays, X-rays and a-rays Dose effect dependent on exposure time [84][85][86]
Φ6 IR
0.5 m for 3 h at different humidity levels		 Over 90% inactivation at humidity levels above 50% [87]
Microwaves T4, T7, λ, MS2, E. coli bacteriophage isolated from sewage Different times from 10 s to 2 min Thermal inactivation [20][88][89][90]
Filtration MS2 Modified Al2O3 granular ceramic filter materials Al2O3 or Cu/Ag Highly porous granular structures play a key role in the removal [91][92]
SJC3 Columns of quartz sand Filtration strongly dependent on the concentration and valence of the dominant cation in the pore fluid (CaCl2 increased virus removal) [66]
MS2, PRD1,T4 Carbon nanotubes (CNT) Both filtration and inactivation of viral aerosols, CaCl2 increased virus removal, likely due to complexation of calcium ions to viral surface [62][63][64][93]
λ, T4, MS2 Iodinated resin filters Structural damage to the capsid protein through filter enrichment with iodine [94][95][96]
f2, MS2, T4, T7 Filtration and UV   [97][98][99][100]
UV λ, MS2, PRD1, R17, PP7, fd, M13, T4, T7, SP8, ΦX174, B40-8, GA, Qβ, Staphylococcus-phage A994, Φ6, P680, P008, T1, P22, T2, R17 From 9 mJ/cm2 to 50 mJ/cm2 depending on the phage Time- and phage-dependent dose. MS2 phage had the greatest resistance [28][29][30][31][32][85][101][102][103][104][105][106][107][108][109][110][111][112][113][114][115][116][117][118]
MS2, different coliphages from the treated municipal wastewater 0.05–0.25 mg/L Cl and 14–22 mWs/cm2 UV More effective than chlorine alone [119][120][121]
Ozone MS2 0.03 mg min/L and a small O3-Ct value ROS-mediated oxidative damage. The synergistic effect after the sequential ozone-UV and UV-ozone exposures [40][122][123]
Electric field M13, M18, λ Pulsed electric field (PEF), 5 or 7 kV Survival ratios after 12 min PEF treatment were 10−4–10−5
inactivation regardless of the form of the phage particle		 [124]
Ultrasound (US) Phage of the Bacillus megaterium, bacteriophages in Klip River water, ΦX174, MS2 29.10, 582, 862, 1142 kHz The synergistic effect US and UV [38][39][125][126]
Plasma ΦX174 One atmosphere uniform glow discharge plasma (OAUGDP) Titer reduction >106 after 15 min [127][128]
ΦX174, MS2, λ Non-thermal atmospheric pressure plasma Membrane destruction, inactivation of proteins, and DNA damage [77][78][129][130][131][132][133]
MS2 Nonthermal plasma jet operated at varying helium/oxygen Inactivation is a function of oxygen concentration in the carrier gas mixture [76][131]
ΦX174, MS2, T4 Surface plasma in argon mixed with 1% air and plasma-activated water ROS-mediated oxidative damage [79]
Energetic femtosecond lasers MS2, M13 400–800 nm lasers Coats’ proteins disruption through laser-induced excitation of large-amplitude acoustic vibrations [67][68][69][70][71][72][73][74][75][134][135]
Visible Light ΦC31, Φ6 405, 455 nm ROS-mediated oxidative damage [35][36][37]
Humidity MS2, Φ6, T3 Range from low to high RH Structure damage [49][50][51][53][54][55][56]

This entry is adapted from the peer-reviewed paper 10.3390/ijms24054447

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