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Communication

Actinic Radiation, Viruses, Bacteria, the Open Air Factor (OAF) and Indoor Sterilization with UV-C Radiation

by
Adrian F. Tuck
†
Retired Scientist, Boulder, CO 80303, USA
†
Formerly at Physical Chemistry Department, Cambridge University, 1965–1968; Chemistry Department, University of California at San Diego, 1969–1971; Physics Department, University College London, 1971–1972; UK Meteorological Office, 1972–1986; NOAA Aeronomy Laboratory, 1986–2007; Visiting Professor, Physics Department, Imperial College London, 2007–2021; Professeur Invité, École Nationale des Ponts—Paris Tech, 2010–2011.
Processes 2023, 11(10), 2882; https://doi.org/10.3390/pr11102882
Submission received: 25 August 2023 / Revised: 15 September 2023 / Accepted: 27 September 2023 / Published: 30 September 2023
(This article belongs to the Special Issue Formation Mechanisms and Process Analysis of Air Pollutants)
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Abstract

:
Two issues embedded in air pollution research are considered to be the long-observed effect of outdoor exposure to sunlight having a germicidal effect—the Open Air Factor (OAF)—and the wavelength dependence and implications of the use of UV-C light indoors to achieve germicidal action. Suggestions are made about the mechanism of the OAF and about the possible emergence of resistant strains indoors.

1. Introduction

Reference [1] reconsidered work from the 1960s, which showed that there was a germicidal effect of open air upon airborne microbes and viruses, attributed to photochemical effects driven by solar radiation. The photochemical agents are now not thought to be in direct reaction with OH and HO2, the primary tropospheric oxidisers, nor the formation of Criegee intermediates from the addition of ozone to the double bonds in biopolymers. The airborne transmission of SARS-CoV-2 was demonstrated recently [2].
Suggestions are made here about the possible role of translationally hot ground state oxygen atoms (O3P) resulting from tropospheric photodissociation of ozone at wavelengths >290 nm in connection with the intermittency of temperature [3]. While that process was considered earlier in the context of the much lower fluxes of O(1D) producing OH via reaction with water vapour and considered insufficient [4], despite the orders of magnitude greater fluxes, the effects of translationally hot (O3P) upon organic molecules and aerosols in air has not been considered hitherto. We note that the side chains of proteins forming the capsid of viruses frequently contain double bonds, as do proteins embedded in the membranes of single-celled bacteria. Hot (O3P) reacting with or penetrating such capsids and membranes appears to be possible at double bonds, whether in olefins or 5- and 6-membered rings in biopolymers.
Regarding the effects of indoor sterilization using the more energetic wavelengths below those found in the troposphere, the α-hydroxy lactic acid has been investigated [5], employing a Hg-Xe lamp at wavelengths >215 nm. Given that the peptide bond in proteins photodissociates in both aromatic and nonaromatic peptides in the vacuum ultraviolet [6], the germicidal mechanism could be directly photolytic. That is also true of sulphur–sulphur bonds in some proteins [7]. Few coronaviruses and nucleic acids (both DNA and RNA) are also unaffected by UV-C radiation [8]. Nevertheless, the emergence of a resistant strain cannot be discounted with certainty.

2. Naturally Selective Possibilities

Microorganisms have been found to remain viable after desiccation and exposure to UV-A and UV-B in desert conditions [9]. Some have been found to be resistant to UV-C when possessing a sufficient Mn/Fe ratio [10]. Viruses could encounter desiccation in low-humidity indoor circumstances before or after exposure to germicidal radiation, the single-celled bacteria could encounter it at low relative humidities at jet stream and upper troposphere/lower stratosphere altitudes [11,12]. At those altitudes, half the periodic table can be detected in aerosols [13], including Fe, Mn and many other row four elements, from meteorites as well as the planetary surface. Such transition metals are also well known as catalysts. Merging with such naturally occurring aerosols is not beyond the bounds of possibility for microbes, especially when the aerosols have an organic, surfactant coating [14,15].
Primitive microbes, such as cyanobacteria, first used photosynthesis as an energy source 2400 million years ago, transferring and delocalizing the high energy-photons by fluorescence, converting them to an electron or rapid transfer by protein or chlorophyll complexes. Mergers with existing aerosols or microbes could initiate evolution by natural selection to form at least possibly resistant strains.
From an indoor point of view, the use of 222 nm and 254 nm radiation will not only be a potential hazard to people via the direct effect of the radiation, but also by their photochemical effects [5] on indoor airborne compounds. While there are papers saying that 222 nm radiation is safe in regard to eye and skin damage [16,17,18], there is also work showing DNA damage in cells [19]. The 222 nm wavelength just overlaps the Schumann–Runge absorption system of O2, which initiates the production of odd oxygen, while the 254 nm wavelength is centred in the oxygen atom and excited oxygen molecule producing Hartley band of the ozone, the mechanism for producing oxygen atoms and ozone naturally in the stratosphere and the polluted troposphere. In addition to the major products carbon dioxide (CO2) and carbon monoxide (CO), some of the decomposition products of lactic acid, for example [5], lesser products such as acetaldehyde (CH3CHO), acetic acid (CH3COOH), formic acid (HCOOH), methane (CH4) and ethane (C2H6), are also formed. Many of these are either toxic or unbreathable, e.g., acetaldehyde photodissociates at wavelengths between 290 and 330 nm, via 4 channels, to CH3 + HCO, CH4 + CO, H + CH3CO and H2 + CH2CO. None of these products will improve air quality, particularly the free radicals. Ozone, of course, is notoriously unhealthy indoors, as well as outdoors, where its concentration in the troposphere has increased substantially during the 20th Century [20]. Reviews exist for both open air and indoor air [21,22]. Among the general classes found, indoors are alkanes, aromatics, terpenoids, alcohols, aldehydes, ketones, esters and halogenated compounds. Many of these are photochemically active, and several will photodissociate under 222 nm radiation in particular and UV-C in general. Lactic acid, acetone and isoprene are emitted by humans. Indoor air can become very polluted, both from the presence of people and from a variety of sources within domestic and commercial premises [22]. Many references in [5] examine some indoor effects of UV-C., for example [23,24]. It is necessary to use sensitive techniques in examining indoor airborne microbes. Averaging what occurs in impactor techniques makes them insufficient, and single-particle analysis instruments are required [2].

3. Mechanisms and Tests

Indoor air is even more chemically complicated than open air, with concentrations generally higher; in some instances, HOx mixing ratios can approach peak outdoor values. Indoor disinfection is usually carried out in the absence of people, although there are proposals to use UV-C in occupied spaces accompanied by optical shields and flow management baffles. Whether or not a space is occupied under irradiation, the emergence of resistant strains of airborne microbes remains a possibility. There are two aspects of the problem: direct photodissociation and chemical reaction with photofragments, especially ground-state oxygen atoms, O(3P). Bear in mind that putting a UV-C source in the ceiling of a room is akin to putting a miniature stratosphere in place. Ozone photodissociation also produces O2(a1Δg), a molecule which is biologically active. Indeed, cell chemistry produces it. They are less common now, but past forms of fluorescent lighting emitted 184.9 nm of radiation, which is in the long wavelength edge of a water vapour absorption band.
Viruses consist of an RNA or sometimes DNA moiety of genetic material encased in a protein coat, the capsid. They are frequently equilibrium systems incapable of autonomous reproduction. Airborne bacteria are alive and far from chemical equilibrium and capable of autonomous reproduction. In each case, their viability involves cooperation between proteins and nucleic acids. They may have sheaths of water molecules, depending on the relative humidity, which can also affect their internal water content if the capsid or the bilipid membrane allows transit of the H2O molecules. The hydrogen bonding important in the folding of proteins and nucleic acids is intimately linked to the water content.
The photodissociation of gas-phase protonated peptides has been examined recently, with an emphasis on the effects of 226 nm and 193 nm radiation. The aim was to understand the photodynamics of the amide bond in proteins [25]. In simple peptides, the amide bond is flat, but in much larger, more complicated proteins, some of the bonds are strained, which can lead to absorptions which are forbidden by symmetry selection rules in the undistorted form.
Techniques have also been developed to examine the products of the reaction in the gas phase of O(3P) atoms with purines and pyrimidines, the constituent bases of nucleic acids [26]. A rich chemistry was observed when gas-phase ground-state O atoms reacted with the deprotonated bases.
Testing these ideas indoors seems to be possible. A first step would be to investigate whether the temperature showed intermittency as it does outdoors in the lower stratosphere [3]. Measurement of the concentrations of O(3P) and O2(a1Δg) when germicidal UV-C radiation is present is an essential step.
The possible interactions between airborne viruses and bacteria with aerosols in the ambient open air seem to be an unexplored possibility, both indoors and outdoors. The theoretical and experimental examination of chemistry in and on microdroplets (the size of single-cell bacteria and atmospheric aerosols) is, in principle, possible but also demanding [27].

3.1. Photodissociation of Nucleic Acids and Proteins

The information-carrying bases, the purines adenine and guanine, and the pyrimidines cytosine, thymine and uracil, are folded inside the relatively inert sugar-phosphate backbone which is helical in DNA. These bases further have very short-lived excited states under UV-C irradiation [28], of order picoseconds (10−12 s). Extremely rapid internal conversion delocalizes the photon energy and prevents much direct photolysis. It is, however, possible to enable thymine–thymine dimer formation between neighbouring bases, a mechanism also possible between neighbouring pyrimidine bases [29]. Photochemistry has recently been adopted as a method for modifying nucleotides [30], but much remains to be understood about the detailed molecular mechanisms, the photofragments produced and their further decays and reactions.
The photochemistry of proteins is dominated by the chromophore properties of the peptide bond [6,25], with some absorption of UV radiation by the phenolic moieties in the side chains of certain proteins, occurring at about 214 nm. The absorption spectrum is typically broad, extending between 190 and 230 nm. Strong absorption at the lower wavelengths is attributed to π–π* transitions, which are allowed by symmetry selection rules. There is also weaker but significant absorption around 226 nm, attributable to the nominally forbidden n–π* transition which occurs when the flat amide bond is distorted by the local molecular environment. The distortions appear to be an effect arising from internal hydrogen bonding involved in the formation of protein folds. This role of hydrogen bonding implies there will be effects of the internal and external water content of airborne microbes and the local humidity.
The concept of photostability [31] will be important in the effects of UV-C radiation on the proteins and nucleic acids that constitute airborne viruses and single-cell bacteria. It has a role to play in their evolution by natural selection.

3.2. Reactions of O(3P) and O2(a1Δg) with Nucleic Acids and Proteins

The production of odd oxygen by UV-C radiation in indoor air will primarily produce O(3P) and O2(a1Δg). Both photofragments are biologically active [26,32]. They may attack olefinic double bonds and so be an alternative to the formation of Criegee intermediates by the parent ozone.
The interaction of ground state O atoms with the purine and pyrimidine nucleotides that constitute RNA and DNA produces a rich and varied chemistry [26]. That chemistry will be open to acceleration in the interiors of bacteria and viruses [27]; there will be Gibbs free energy available from the translationally hot O atoms and a-state singlet O2 in addition to that inherent at the microbe surfaces. The products of O atom reactions with adenine, guanine, cytosine, thymine and uracil result from the replacement of an H atom on an unsaturated ring carbon at, respectively, the 2,8,6,6,5 carbon atoms. The reaction of the deprotonated nucleotide bases X− with O produces the cyanate anion OCN−. The adducts from the O atom reaction, with a deprotonated nucleotide, have high degrees of excitation that can enable complex fragmentation products [26]. Adenine is a pentamer of HCN, and there is evidence that the HCN monomers can be lost sequentially. Other neutral products include HCHO, HNCO and CO.
The O2(a1Δg) photofragment can, by reaction with amino acid residues in proteins, play a significant role in cell biology, including apoptosis (cell death). The effect has been systematically investigated for five different proteins, each containing a single tryptophan amino acid [26]. The rate of reaction depended on the local molecular position and geometry, an echo of the effect observed in peptide photodissociation in [6] and [25]. Could the Open Air Factor be driven by the production of hot O(3P) and O2(a1Δg)? Figure 1 shows the primary candidate source, the Huggins bands. The O2 (a1Δg) state lies 94 kJ mol−1 above the 3Σg− ground state. The a1Δg state is metastable, and the radiative transition to the 3Σg− ground state is forbidden by symmetry selection rules for the isolated O2(1Δg) molecule. The radiative lifetime is about 60 min. It is also relatively stable against collisional deactivation to the ground state, so it is persistent in the air.
The threshold wavelengths, products and energies are as follows:
O3 + hυ → O(3P) + O2(X3Σg−)101 kJ mol−11180 nm
→ O(3P) + O2(1Δg)195 kJ mol−1612 nm
→ O(3P) + O2(b1Σg+)258 kJ mol−1463 nm
→ O(1D) + O2(X3Σg−)291 kJ mol−1411 nm
→ O(1D) + O2(1Δg)386 kJ mol−1310 nm
→ O(1D) + O2(b1Σg+)448 kJ mol−1267 nm
→ 3O(3P)595 kJ mol−1201 nm
→ O(1S) + O2(1Δg)610 kJ mol−1196 nm

3.3. Aerosols, Airborne Microbes

Many atmospheric aerosols have organic surfactant exteriors [14,15,27], and over the whole sampled population of millions between 5 and 19 km altitude have contained half the elements in the periodic table [13]. That raises questions about what can happen when an airborne virus or bacterium collisionally encounters a background aerosol particle, indoors as well as in open air. Engulfment is possible, as is an extensive range of ensuing chemical reactions, many unexplored. Both continental and marine aerosols have been shown to have surfactant coatings, mainly carboxylic acids [34,35]. Marine aerosols predominantly had palmitic acid on their surface, while continental aerosols had a range of carboxylic acids up to the C32 molecule. If the naked viruses and bacteria are released into the air, several possibilities exist. Their water content can change as humidity fluctuates, or they can collide with pre-existing aerosols, or more rarely with each other, inside or outside any engulfing aerosols. The acidity is also a variable and important factor [24]; pH needs to be measured.
In addition to the surface-orientated effects, the effects of both photons and ozone photofragments internally should be considered, as discussed in [27]. Both the increased photon pathlengths and the molecular crowding will, operating through the Gibbs free energy, tend to both facilitate and accelerate reactions that may not be allowed in the bulk fluid.
A possible trade-off between health benefits and damages arising from air pollution and germicidal radiation has been discussed [36].

3.4. Experimental Tests

The mechanisms suggested here are open to experimental tests in the laboratory, indoors, outdoors and possibly by molecular dynamics calculation.

3.4.1. Laboratory Experiments

Laboratory experiments, as exemplified by [5,6,7,8] could be pursued to investigate the effects of hot O(3P) and O2(a1Δg) on airborne viruses, bacteria and their protein and nucleic acid constituents. It is possible to envisage both the fragmentation and expansion of the microbes. There is also scope for the further investigation of the direct effects of irradiation across the visible and the entire ultraviolet spectrum, for both single wavelengths such as 184.9, 193, 222, 226 and 254 nm and solar simulation Xenon arcs from 200 to 800 nm. Systematic investigations of the effects of fluctuations in relative humidity upon the exterior and interior water content of airborne microbes are indicated, given the results in [37]. Suggestions for experimental examination of micron-sized droplets, including single-celled bacteria, are made in [27]. Given the complexity of processes on, in and inside cell surfaces [38,39], there is room for advanced experimental and theoretical research in this area. Molecular dynamics calculations have a role to play [27].
The laboratory would seem to be the place to investigate the results of collisional encounters between aerosols and airborne microbes. The latest techniques would need to be employed, including single-particle chemical analysis and optical and mass spectrometric monitoring of the ‘reactants’ and the resulting products. Detection of the emergence of resistant strains might be particularly demanding.

3.4.2. Indoor Tests

Indoor tests should aim at the detection of ozone and its photofragments with the proposed UV-C germicidal radiation in use and turned off as a control [17,18]. High-resolution observations of temperature and air movement would test for intermittency and applicability of statistical multifractal techniques [3]. People must be absent, but lactic acid, acetone and isoprene could be injected to simulate their gaseous emissions, and any airborne microbes under investigation added as required. The effects on surfaces probably offer further complexity to be studied as the situation indicates. Indoor air has a variety of molecular species, and the measurements needed will call for comprehensive instrumentation.

3.4.3. Open AirTests

Investigation of the Open Air Factor is possible with the basic platform of the NOAA SABRE payload [40], with the addition of instruments to detect the O(3P) and O2(a1Δg) photofragments from ozone photodissociation. They are the proposed active reactants in place of OH, HO2 and O3 itself [1,3].

4. Discussion

Viruses and bacteria have enormous abundances, enormous variety and in particular circumstances, impressive durability. Their ability to evolve rapidly is evident inside and outside plants and animals and often leads to resistant strains in human environments. Airborne microbes are a more immediate danger than the long-observed build-up of gases, both indoors and outdoors. Altering the microbial and viral populations by using UV-C radiation as an indoor germicide risks the evolution of resistant strains. It is difficult to see how increasing odd oxygen in an enclosed space will improve the air for breathing. The roles of ozone photofragments from the Chappuis and Huggins bands, O(3P) and O2(a1Δg) need to be explored. Once produced, airborne microbes and viruses can ride meteorological winds, such as jet streams, to travel between continents in days, with a possible ability to evade the Open Air Factor via desiccation at the low humidities on either side of the tropopause. The interaction of airborne viruses and bacteria with aerosols seems to be largely unexplored.

5. Conclusions

Experimental investigations to examine the behaviour of airborne viruses and bacteria indoors and in ambient open air within an air pollution context are recommended. The tests should focus on the effects of photodissociation products on the cellular molecular constituents such as DNA and proteins that are susceptible to absorbing the radiations proposed as germicidal, both indoors and outdoors. Hot O(3P) and O2(1Δg) from ozone photodissociation deserve particular attention. The study should aim to go beyond the simple issues of eye and skin safety.

Funding

This research received no external funding.

Data Availability Statement

Widely avaolable, see Reference [3].

Acknowledgments

This work resulted from discussions of Reference [5] with Veronica Vaida, who provided Figure 1b. James Burkholder provided Figure 1a.

Conflicts of Interest

The author declares no conflict of interest.

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Figure 1. (a) The Chappuis absorption band of ozone. The products are translationally hot O(3P) and ground state triplet molecular oxygen O2(X3Σg−), which may be rovibrationally excited. In both cases, the products are available in the troposphere. Diagram provided by J. B. Burkholder. (b) The Huggins band of ozone. Wavelengths <385 nm with the Chappuis band to the longer wavelengths. The Huggins band produces hot O(3P) plus O2 (a1Δg) and is their primary source in the troposphere. After Axson et al. [33].
Figure 1. (a) The Chappuis absorption band of ozone. The products are translationally hot O(3P) and ground state triplet molecular oxygen O2(X3Σg−), which may be rovibrationally excited. In both cases, the products are available in the troposphere. Diagram provided by J. B. Burkholder. (b) The Huggins band of ozone. Wavelengths <385 nm with the Chappuis band to the longer wavelengths. The Huggins band produces hot O(3P) plus O2 (a1Δg) and is their primary source in the troposphere. After Axson et al. [33].
Processes 11 02882 g001aProcesses 11 02882 g001b
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Tuck, A.F. Actinic Radiation, Viruses, Bacteria, the Open Air Factor (OAF) and Indoor Sterilization with UV-C Radiation. Processes 2023, 11, 2882. https://doi.org/10.3390/pr11102882

AMA Style

Tuck AF. Actinic Radiation, Viruses, Bacteria, the Open Air Factor (OAF) and Indoor Sterilization with UV-C Radiation. Processes. 2023; 11(10):2882. https://doi.org/10.3390/pr11102882

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Tuck, Adrian F. 2023. "Actinic Radiation, Viruses, Bacteria, the Open Air Factor (OAF) and Indoor Sterilization with UV-C Radiation" Processes 11, no. 10: 2882. https://doi.org/10.3390/pr11102882

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