Article pubs.acs.org/est
Inactivation of Bacteriophage MS2 with Potassium Ferrate(VI) Lanhua Hu,† Martin A. Page,‡ Therese Sigstam,§ Tamar Kohn,§ Benito J. Mariñas,† and Timothy J. Strathmann*,† †
Department of Civil and Environmental Engineering and Center of Advanced Materials for the Purification of Water with Systems, University of Illinois at Urbana−Champaign, Urbana, Illinois 61801, United States ‡ USACE Engineer Research and Development Center, Construction Engineering Research Laboratory, Champaign, Illinois 61822, United States § Laboratory of Environmental Chemistry, School of Architecture, Civil and Environmental Engineering (ENAC), École Polytechnique Fédérale de Lausanne (EPFL), 1015 Lausanne, Switzerland S Supporting Information *
ABSTRACT: Ferrate [Fe(VI); FeO42−] is an emerging oxidizing agent capable of controlling chemical and microbial water contaminants. Here, inactivation of MS2 coliphage by Fe(VI) was examined. The inactivation kinetics observed in individual batch experiments was well described by a Chick−Watson model with first-order dependences on disinfectant and infective phage concentrations. The inactivation rate constant ki at a Fe(VI) dose of 1.23 mgFe/L (pH 7.0, 25 °C) was 2.27(±0.05) L/(mgFe × min), corresponding to 99.99% inactivation at a Ct of ∼4 (mgFe × min)/L. Measured ki values were found to increase with increasing applied Fe(VI) dose (0.56−2.24 mgFe/L), increasing temperature (5−30 °C), and decreasing pH conditions (pH 6−11). The Fe(VI) dose effect suggested that an unidentified Fe byproduct also contributed to inactivation. Temperature dependence was characterized by an activation energy of 39(±6) kJ mol−1, and ki increased >50-fold when pH decreased from 11 to 6. The pH effect was quantitatively described by parallel reactions with HFeO4− and FeO42−. Mass spectrometry and qRT-PCR analyses demonstrated that both capsid protein and genome damage increased with the extent of inactivation, suggesting that both may contribute to phage inactivation. Capsid protein damage, localized in the two regions containing oxidant-sensitive cysteine residues, and protein cleavage in one of the two regions may facilitate genome damage by increasing Fe(VI) access to the interior of the virion.
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Ferrate [Fe(VI); FeO42−] has attracted growing attention in recent years as an alternative oxidant and disinfectant for water and wastewater treatment applications.12−19 Fe(VI) is a promising disinfectant for many reasons: (i) Fe(VI) is a strong oxidant reported to react readily with amino acids and other biomolecules;20,21 (ii) Fe(VI) is a selective oxidant that is more stable than free chlorine and ozone in waters rich in ammonium or natural organic matter (e.g., wastewater);13 (iii) past work has shown that Fe(VI) inactivates bacteria and viruses, including E. coli and the coliphages f2 and Qβ;14,15,17,22,23 (iv) Fe(VI) oxidation of organic molecules is not expected to produce halogenated DBPs; (v) in vitro assays indicate no mutagenic or carcinogenic byproducts formed in Fe(VI)treated water;24−26 (vi) unlike ozone, Fe(VI) does not oxidize bromide to bromate;20 and (vii) insoluble Fe(III) oxyhydroxide byproducts of Fe(VI) reactions and autodecomposition can
INTRODUCTION
For over a century, free chlorine has been applied extensively as a disinfectant to control bacteria, viruses, and other pathogens in drinking water.1 However, recent regulations mandating more stringent control of Cryptosporidium parvum oocysts and disinfection byproducts (DBPs)2,3 has prompted many utilities to replace free chlorine with alternative processes. Although chlorination remains the dominant disinfection process, UV disinfection and/or treatment with combined chlorine are increasingly being applied as alternatives to control C. parvum and regulated DBPs, respectively. This industry trend has increased concerns about viral pathogens,4,5 especially enteric viruses, because of their greater resistance to UV light and combined chlorine than to free chlorine.1,6 Furthermore, recent reports indicate that combined chlorine disinfection processes promote increased formation of unregulated, but potentially more toxic, DBPs (e.g., N-nitrosamines).7−9 As a result, there remains strong interest in the development of alternative disinfection processes that are both effective at inactivating viral pathogens and producing fewer and less toxic DBPs than free chlorine.10,11 © 2012 American Chemical Society
Received: Revised: Accepted: Published: 12079
August 6, 2012 September 26, 2012 October 2, 2012 October 2, 2012 dx.doi.org/10.1021/es3031962 | Environ. Sci. Technol. 2012, 46, 12079−12087
Environmental Science & Technology
Article
Table 1. Batch Reaction Conditions and Measured Kinetic Parameters for MS2 Phage Inactivation and Fe(VI) Decomposition exp ID
pH
T (°C)
buffera
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22
7.0 7.0 7.0 7.0 7.0 7.0 7.0 7.0 7.0 7.0 7.0 7.0 7.0 6.0 6.5 7.5 8.0 8.5 9.0 9.5 10.0 11.0
25 25 25 25 25 25 25 25 5 10 15 20 30 25 25 25 25 25 25 25 25 25
10 mM PBS 10 mM PBS 10 mM PBS 10 mM PBS 10 mM PBS 10 mM PBS 10 mM PBS 10 mM PBS 10 mM PBS 10 mM PBS 10 mM PBS 10 mM PBS 10 mM PBS 10 mM PBS 10 mM PBS 10 mM PBS 10 mM PBS 10 mM PBS 10 mM PBS + 2 mM BBS 10 mM PBS + 2 mM BBS 10 mM PBS + 2 mM BBS 10 mM PBS + 2 mM BBS
measured N0 of MS2 (pfu/mL)
measured [Fe(VI)]0b (mgFe/L)
× × × × × × × × × × × × × × × × × × × × × ×
1.23 1.35 1.23 1.36 1.37 0.57e 1.43f 1.42f 1.46 1.22 1.26 0.95 1.44 1.14 1.24 1.52 1.63 1.54 1.56 1.33 1.36 1.24
4.3 1.3 6.6 2.1 4.0 7.3 7.3 1.1 4.4 1.3 1.6 3.2 1.7 8.8 2.6 1.1 7.4 1.7 1.7 5.9 7.3 2.7
105 107 105 106 106 106 106 107 104 105 105 105 105 105 105 106 105 106 106 106 106 106
kic (L/(mgFe × min)) 2.27(±0.05) 2.3 (±0.2) 2.37(±0.05) 2.9(±0.4) 2.2(±0.1) 1.44(±0.03) 4.7(±0.5) 4.5(±0.2) 7.7(±0.2) × 9.9(±0.3) × 9.2(±0.3) × 1.49(±0.04) 3.0(±0.2) 2.44(±0.04) 2.42(±0.09) 1.66(±0.04) 1.14(±0.04) 2.8(±0.1) × 1.8(±0.1) × 1.2(±0.1) × 8.4(±0.1) × 4.3(±0.1) ×
10−1 10−1 10−1
10−1 10−1 10−1 10−2 10−2
kdd (L/(mgFe × min)) 1.02(±0.04) × 10−1 9.3(±0.7) × 10−2 1.09(±0.08) × 10−1 9.3(±0.1) × 10−2 9.6(±0.9) × 10−2 1.03(±0.03) × 10−1 3(±1) × 10−2 3.7(±0.3) × 10−2 5.8(±0.4) × 10−2 7.3(±0.2) × 10−2 8.1(±0.1) × 10−2 8.3(±0.2) × 10−2 9.9(±0.9) × 10−2 2.3(±0.1) × 10−1 1.5(±0.1) × 10−1 8.5(±0.9) × 10−3
