Association with Natural Organic Matter Enhances the Sunlight-Mediated Inactivation of MS2 Coliphage by Singlet Oxygen

Abstract

MS2 coliphage, a surrogate for human enteric viruses, is inactivated by singlet oxygen (1O2) produced via sunlight-mediated excitation of natural organic matter (NOM) in surface waters. The 1O2 concentration within a NOM macromolecule or supramolecular assembly ([1O2]internal) is orders of magnitude higher than in the bulk solution ([1O2]bulk). In close proximity of NOM, MS2 is thus exposed to an elevated 1O2 concentration ([1O2]NOM), and inactivation is likely to be enhanced as compared to the bulk solution. In experiments using a solar simulator, we determined [1O2]bulk, [1O2]internal, as well as the association of MS2 with four NOMs (Fluka humic acid, FHA; Suwannee river humic acid, SRHA; Aldrich humic acid, AHA; Pony lake fulvic acid, PLFA), and studied their effect on the MS2 inactivation rate constant, k(obs), over a range of 1-25 mg NOM/L. The k(obs) values were modeled as the sum of the inactivation rate constants in close proximity to the NOM and in the bulk solution, assuming Langmuir-type adsorption of NOM onto MS2. FHA and SRHA exhibited 13-22 fold greater adsorption equilibrium constants than AHA and PLFA. Inactivation in the bulk solution contributed between 2% (20 mg/L FHA) and 39% (5 mg/L AHA) toward the overall k(obs). Thus, even for the less adsorbing NOM, inactivation was dominated by [1O2]NOM rather than [1O2]bulk. Changes in solution chemistry to promote closer interactions between MS2 and NOM also enhanced k(obs). Addition of Mg2+ to neutralize the negative surface charge of MS2 and NOM increased k(obs) up to 4.1-fold. Similarly, lowering the solution pH closer to the isoelectric point of MS2 (pl = 3.9) enhanced k(ob), 51-fold in 5 mg/L AHA.

Sunlight-mediated inactivation of health-relevant microorganisms in water: a review of mechanisms and modeling approaches

“…5, which shows that the probability of an encounter with photochemically produced 1 O 2 decreases by 50% if the sensitizer is separated by a distance of 75 nm from the virus, compared to if the sensitizer is sorbed to the virus, due to quenching of 1 O 2 as it diffuses away from the sensitizer. 61 Higher rates of inactivation due to sorbed organic matter have been demonstrated for some viruses 62,63 and Ent. faecalis.…”

“…For laboratory experiments with collimated light sources, it is common to View Article Online estimate sunlight attenuation due to absorption using Beer's Law, assuming that reection at the surface and scattering by particles suspended in the water are negligible. 117 For natural water bodies exposed to sunlight, the diffuse downwelling attenuation coefficient is used (eqn (1)), which can either be measured directly or modeled using fundamental optical measurements (e.g. Kirk 2011, 10 or using an optical model like Hydrolight 8 ).…”

“…69 Compared to free molecules, it has proven difficult to experimentally demonstrate enhanced photoreactions for organic matter-bound microorganisms. Nevertheless, it is clear that viruses and bacteria will associate with organic matter-rich (micro)phases 62,70 and the likelihood of enhanced exogenous photoinactivation in such cases deserves further study.…”

The role of Fe(III) on phosphate released during the photo-decomposition of organic phosphorus in deionized and natural waters

“…Humic acids are important natural photosensitizer because they contain many active functional groups, such as carboxyl groups, phenolic hydroxyl, and carbonyl-type chromophores. These active functional groups could absorb solar radiation between 300 and 500 nm to reach an excited state and generate free radicals (e.g., hydroxyl radicals, peroxyl radicals and singlet oxygen), which result in the photooxidation degradation of organic contaminants (Kohn et al, 2007;Thirumavalavan et al, 2012). Iron ions have has an important function in this photochemical process because HA is strong affinity with iron ions (Christoforidis et al, 2015;Martínez-Zapata et al, 2013).…”

Mechanisms of Human Adenovirus Inactivation by Sunlight and UVC Light as Examined by Quantitative PCR and Quantitative Proteomics

“…Indirect solar disinfection relies on the production of oxidants upon irradiation of chromophores in solution (exogenous) or within the organism (endogenous) and subsequent energy or electron transfer to dissolved oxygen or other solution constituents. These oxidants, e.g., 1 O 2 (18), then react with the virus constituents and cause inactivation. An enhanced efficiency of solar disinfection compared to monochromatic UVC light may be found if, in addition to causing genome damage, solar disinfection damages vitally important proteins.…”