Airborne bacteria in the atmosphere: Presence, purpose, and potential

Atmospheric Environment 139 (2016) 214e221

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Atmospheric Environment journal homepage: www.elsevier.com/locate/atmosenv

Review article

Airborne bacteria in the atmosphere: Presence, purpose, and potential Wenke Smets a, 1, Serena Moretti a, 1, Siegfried Denys b, Sarah Lebeer a, * a b

University of Antwerp, Dept. Bioscience Engineering, Environmental Ecology and Applied Microbiology, Antwerp, Belgium University of Antwerp, Dept. Bioscience Engineering, Sustainable Energy, Air and Water Technology, Antwerp, Belgium

h i g h l i g h t s  Understanding the presence of airborne bacteria in the atmosphere.  Unravelling the roles airborne bacteria have on atmospheric processes and health.  Exploring the underlying potential of airborne bacteria for various applications.

a r t i c l e i n f o

a b s t r a c t

Article history: Received 2 February 2016 Received in revised form 27 April 2016 Accepted 21 May 2016 Available online 24 May 2016

Numerous recent studies have highlighted that the types of bacteria present in the atmosphere often show predictable patterns across space and time. These patterns can be driven by differences in bacterial sources of the atmosphere and a wide range of environmental factors, including UV intensity, precipitation events, and humidity. The abundance of certain bacterial taxa is of interest, not only for their ability to mediate a range of chemical and physical processes in the atmosphere, such as cloud formation and ice nucleation, but also for their implications -both beneficial and detrimental-for human health. Consequently, the widespread importance of airborne bacteria has stimulated the search for their applicability. Improving air quality, modelling the dispersal of airborne bacteria (e.g. pathogens) and biotechnological purposes are already being explored. Nevertheless, many technological challenges still need to be overcome to fully understand the roles of airborne bacteria in our health and global ecosystems. © 2016 Elsevier Ltd. All rights reserved.

Keywords: Airborne bacteria Endotoxin Respiratory health Air quality Atmospheric modelling

1. Introduction When a beam of light is shone in a darkened room, it illuminates the particles in its path, reminding us that air consists of more than just gases. Beyond the visible particles, lies an airborne ecosystem teeming with microorganisms. From 1860, when airborne microbes were first systemically studied by Louis Pasteur (Pasteur, 1861), they have intrigued scientists not only with their presence, but also with their purpose. The advent of DNA-based molecular tools served to push the field forward, by no longer being limited to the very small fraction of culturable microbes (Gandolfi et al., 2013). Intriguingly, using DNA-based methods, bacterial communities in the outdoor atmosphere appear to show a diversity approximating soil and aquatic environments (Brodie et al., 2007; Katra et al.,

2014; Maron et al., 2005). Over the last decade, the number of studies in this field are steadily increasing. These studies have revealed the unique and prominent roles airborne bacteria may have on atmospheric processes (Delort et al., 2010; Morris et al., 2011) and human health (Degobbi et al., 2011; Liebers et al., 2008). However, what is less explored is the underlying potential of airborne bacteria for various applications. This review will address the aspects that govern outdoor airborne bacteria (such as their sources, dispersal, survival, and factors influencing their metabolism), their impacts on human health, and their role in regional and global climate feedback mechanisms. These aspects illustrate the versatile importance of the bacteria in the atmosphere and allow insight in possible applications of these organisms. 2. Airborne bacteria in the atmosphere

* Corresponding author. University of Antwerp, Dep. Bioscience Engineering, Groenenborgerlaan 171, B-2020, Belgium. E-mail address: [email protected] (S. Lebeer). 1 Equal contribution. http://dx.doi.org/10.1016/j.atmosenv.2016.05.038 1352-2310/© 2016 Elsevier Ltd. All rights reserved.

2.1. Sources Bacteria enter the near-surface atmosphere by aerosolization

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from various surfaces exposed to air currents. Jones and Harrison (2004) state that bacteria from soil and plant surfaces are released into the atmosphere based on the theory of particle resuspension processes. Their theory is supported by several observations. Firstly, several studies show a correlation between land cover and near-surface atmospheric concentrations of bacteria including those by Bertolini et al. (2013), Shaffer and Lighthart (1997), and Tong and Lighthart (2000). Secondly, so-called ‘source-tracking studies’ allow an estimation of the relative contribution of the sources of airborne bacteria at a particular location. The taxonomic identifications of airborne organisms are used to determine contribution of the putative source environments, in which these taxonomic units are typically found (Bowers et al., 2011a, 2011b; Cao et al., 2014). Thirdly, upward bacterial fluxes from soil and vegetation can be measured (as reviewed by Burrows et al. (2009b)). For instance, Lighthart and Shaffer (1994) measured a maximum flux of 17,000 colony forming units m 2 h 1 above a desert-like scrubland. Moreover, they showed that the upward bacterial flux is correlated with the intensity of sensible heat, which can be explained by its role in upward convective air movements. Besides soil and vegetation, oceans and seas are also known to contribute to the bacterial content of the atmosphere by ejection of aerosol droplets into the air (Aller et al., 2005). Other potential sources of airborne bacteria have been identified, as illustrated in Fig. 1. The relative contribution of these sources varies greatly and dominant sources tend to change with time and space. 2.2. Dispersal Bacteria can persist in the atmosphere as individual cells or can be associated with other particles, such as soil dust, leaf fragments, spores or other microorganisms (Lighthart, 1997; Maki et al., 2008; Maron et al., 2005; Tong and Lighthart, 2000). Once aerosolized, bacteria can be transported upwards by convective air movements and, due to their small size, they can remain in the atmosphere for a

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significant period of time. In fact, intercontinental transport has been observed, including transport of bacteria associated with dust plumes originating from deserts and drought stricken areas
n et al., 2014; Hara and Zhang, 2012; Kellogg and Griffin, (Barbera 2006; Lim et al., 2011; Polymenakou et al., 2008). These dust events are known to cause great changes in the downwind atmospheric bacterial community (Maki et al., 2013). For instance, the bacteria associated with the desert dust were shown to easily outnumber the local atmospheric bacteria 10 to 1 at a downwind location over 1000 km from the source (Jeon et al., 2011). Travelling dust plumes may also accumulate other bacteria on their way, for example, marine bacteria when travelling over oceans or seas. (Kellogg and Griffin, 2006; Maki et al., 2013). In addition to dust plumes, tropical storms or transportation higher into the troposphere may assist in long range transport of airborne bacteria (Burrows et al., 2009a; DeLeon-Rodriguez et al., 2013; Stres et al., 2013). An increasing number of studies on airborne microbes are supported with backward trajectory modelling that allows a better insight as to where the airborne microbes originated, such as those by Bottos et al. (2014), Fahlgren et al. (2010), Lee et al. (2007), and Murata and Zhang (2014). These studies also show that longdistance transport by normal wind patterns can contribute greatly to the bacterial composition of a local atmosphere. 2.3. Deposition Bacteria are eventually removed from the atmosphere by either “dry” deposition or “wet” deposition (Jones et al., 2008). Dry deposition is explained by adherence to buildings, plants, water surfaces, the ground and other surfaces in contact with the air (Jones and Harrison, 2004; Jones et al., 2008). The wet deposition of bacteria is caused by the precipitation of rain, snow or hail that has collected atmospheric particles (Christner et al., 2008a; Jones et al., 2008; Monteil et al., 2014; Peter et al., 2014). In some cases, wet deposition can be actively induced by the bacteria themselves,

Fig. 1. Scheme of typical processes that determine the composition of local airborne bacterial communities. Abundant sources of aerosolized bacteria are marked with an upward arrow. Soil and leaf surfaces are often considered the main contributors of airborne bacteria (Bowers et al., 2011b). Other sources of airborne bacteria include water bodies (Blanchard, 1989; de Leeuw et al., 2011), humans and animals (Fujimura et al., 2010; Pan et al., 2003; Sciple et al., 1967; Zhao et al., 2014), faecal material (Bowers et al., 2011b), wastewater treatment (Han et al., 2012), and composting facilities (Albrecht et al., 2007). In case airborne bacteria are transported upwards, indicated as upward flux, they can be transported over medium or long distances and may occur in cloud droplets. Mechanisms leading to deposition are indicated with a downward arrow.

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which is further explained in section 2.6. 2.4. Factors influencing the composition of airborne bacterial communities Despite spatiotemporal variability and lack of standardization in air collection and sample-processing methods e which complicates comparisons across studies e a general trend can be observed in different studies correlating the composition of the bacterial communities and the environmental factors. Of these factors, seasonality, meteorological conditions, anthropogenic influences, and variability in bacterial sources play an influential role in shaping the abundance and composition of airborne bacterial communities across time and space (Table 1). How and to what extent these factors affect the bacterial communities is, however, very context dependent. In Milan (Italy), summer communities differed less from each other than the communities sampled during the other seasons, possibly owing to the stability of the air and particulate matter levels in summer (Bertolini et al., 2013). It may be possible that, in addition, the stressors in summer, such as ozone, drought and solar radiation all together induce a constant selective pressure, which leads consistently to the survival of adapted species. In relation to this, there are two general speculations for the correlation of meteorological factors with community composition: the shifts in atmospheric stressors select for different adaptations of bacteria (e.g. spore formation, pigmentation), or the wind, temperature, precipitation and season affect the contribution of different source environments for the airborne bacteria at a set location (e.g. more leaf-associated bacteria in summer) (Bowers et al., 2013; Huffman et al., 2013; Jones and Harrison, 2004). In the case of the latter, source contribution is playing the leading role in the abundance of the different bacteria in the atmosphere. This implies that airborne bacteria are no more than a collection of organisms dispersed from different sources, and therefore less likely to be part of an atmospheric ecosystem. However, airborne bacterial communities are distinctly different from their source environments, possibly because many of the bacteria do not survive in the atmospheric environment (Bowers et al., 2011a). The specific selection pressure in the atmosphere may, additionally, be caused by other ecological factors, such as availability of certain substrate. This ecological point of view rather fits into the “atmosphere biome” hypothesis of

Morris et al. (2011), whereby the airborne microbes actively interact with each other and with the environment. This hypothesis is supported by the studies on adaptations and metabolic activity of airborne bacteria (discussed in section 2.6). It is likely these two explanations co-exist, as also stated by Womack et al. (2010). This means that only a certain fraction of bacteria in the atmosphere would be metabolically active.

2.5. Survival of airborne bacteria Despite the recurrent mention of the atmosphere being a stressful environment for bacteria to live in, diverse bacterial communities have been found in other extreme environments, such as the deep sea, hot springs and deserts (An et al., 2013; Puspitasari et al., 2015; Rothschild and Mancinelli, 2001; Womack et al., 2010). Life in the atmosphere is characterized by scarcity of nutrients and substrate, UV radiation, desiccation, temperature and pH shifts, and the presence of reactive oxygen species. The survival of airborne microbes likely emanates from, among others, DNArepair mechanisms, pigmentation, mechanisms promoting aggregation, and metabolic adaptations to nutrient shortages such as biosynthesis of cytochrome bd in order to survive iron deprivation (Tringe et al., 2008; Womack et al., 2010). For instance, Bowers et al. (2013) found more diversity on coarser particles compared to finer particles and suggested that bacterial cells attached to substrates can survive more easily. Additionally, Stres et al. (2013) found a strong relationship between dust particle abundance and cell count. Also in the cloud simulation chamber of Amato et al. (2015), aggregation seemed to favour cell survival. It is likely that the aggregates of bacteria and substrate allow the activity and interactions that are typical of an atmosphere biome. Another protection mechanism of bacteria is to enter a nondividing state (dormancy), where they morphologically transform to spores or undergo other cell wall modifications and slow down or stop their metabolic activity (B€ ar et al., 2002; Delort et al., 2010). These transformations can improve the resistance to physical stresses, such as UV radiation (Kobayashi et al., 2015), which increases chances of survival in the atmosphere. For instance, during Asian dust events, the viable fraction of airborne bacteria often seems to consist mainly of spore-forming Bacillus spp. (Maki et al., 2013; Yamaguchi et al., 2014).

Table 1 Factors that have been found affecting the community structure of airborne bacteria. Factor Weather Precipitation Temperature Air humidity UV index Wind speed and direction Weather of the recent past Location Geographic location Point sources nearby Land use Traffic Climate Altitude Time Time of the day Season Atmospheric composition PM and its size distribution CO2 pH in water droplets

Examples in literature Santos-Burgoa et al. (1994) Di Giorgio et al. (1996) Shaffer and Lighthart (1997) Shaffer and Lighthart (1997) Jeon et al. (2011); Maki et al. (2014) Ravva et al. (2012) Bowers et al. (2011b) Bowers et al. (2011b); Han et al. (2012) Bowers et al. (2011a) Fang et al. (2007) Polymenakou (2012) Griffin et al. (2011); Li et al. (2010); Munday et al. (2013); Maki et al. (2015) Shaffer and Lighthart (1997) Bowers et al. (2012); Franzetti et al. (2011) Bertolini et al. (2012); Brodie et al. (2007) Klironomos et al. (1997) Amato et al. (2005)

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2.6. Atmospheric interactions The inevitable question therefore arises, whether the viable airborne bacteria are merely trying to survive the harsh atmospheric environment by ceasing all activity or if they play an active role in modifying environmental conditions within the atmosphere. This is currently one of the main questions concerning microbial life in the atmosphere (Delort et al., 2010; Morris et al., 2014; Womack et al., 2010). The first indication that airborne bacteria affect their environment was the discovery of their potential to act as ice nuclei and cloud condensation nuclei (Bauer et al., 2003; Vali et al., 1976). This can co-induce cloud formation and precipitation (Bigg et al., 2015; Hill et al., 2014; Joly et al., 2013; €hler et al., 2007; Morris et al., Lohmann and Feichter, 2005; Mo 2014). Some airborne bacteria are capable of expressing ice nucleating or ice-binding proteins which regulate ice nucleation or bind and inhibit the growth of ice crystals, respectively (Christner, 2010). As precipitation causes deposition of airborne bacteria back to the surface, it has been proposed that alteration of the nucleation activity of some species may be a mechanism to postpone or stimulate their own deposition (Lindow, 1982; Morris et al., 2014). Interestingly, many of these ice nucleating proteins occur in plant pathogens such as Pseudomonas syringae, which cause significant freezing injuries in plants and crops (Hill et al., 2014; Lindow et al., 1982). Although clouds are very complex systems to simulate in the lab and in situ evidence of microbial metabolic activity in the atmosphere is limited, several approaches have been undertaken to assess the possibility of metabolically active airborne bacteria. Initially, Dimmick et al. (1979) observed that bacteria aerosolized into rotating-drum aerosol chambers at 30  C with saturated humidity were dividing within 1e2 h. However, this experimental setup did not mimic the natural cloud conditions, thus only indicating that aerosolization is not a barrier for cell division. More recently, Sattler et al. (2001) showed that bacteria collected at high altitudes were capable of growing and reproducing in cloud water when incubated at 0  C. Similarly, Amato et al. (2007) found that bacteria sampled from clouds were capable of growing at temperatures typically encountered in troposphere clouds. However, conditions in clouds differ markedly from the rest of the atmosphere and research conclusions of either environment should not be used interchangeably, without a valid argument. As for the cloudborne microbes, they have been found capable of influencing atmospheric chemistry, as described by Delort et al. (2010). For instance, biodegradation of organic compounds, such as formic acid, seems to significantly influence carbon chemistry in clouds (DeLeon-Rodriguez et al., 2013; Vaïtilingom et al., 2010). Moreover, microbial degradation of airborne organic compounds may also occur outside the cloud environment. Ariya et al. (2002) observed airborne microbes capable of degrading dicarboxylic acids, which are abundant organic aerosols in the atmosphere. They proposed that not only fog and clouds, but also organic aerosols of the ambient air present a suitable medium for growth of microorganisms. Therefore, it can be hypothesised that aggregates of microbes and particulate matter not only facilitate contact between bacteria and substrate, occurring in relatively low concentrations in the air, but also allow the fraction of active microorganisms to form interacting communities. Many studies assessing airborne bacteria by using a wide variety of approaches, indicate at least some bacterial activity in the atmosphere. However, real proof of interacting bacterial communities in the outdoor air seems challenging to produce. To tackle this problem, there is a need for in situ detection of bacterialactivity-indicators, such as, substrate degradation, cell division, crosstalk molecules or a high ATP to cell ratio. Although, when in

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situ detection is not feasible, a closed atmospheric chamber such as that used by Amato et al. (2015) may be employed. Other approaches include high throughput whole-genome metagenomics, transcriptomics and proteomics to explore metabolic capacity (at DNA level) and activity (at mRNA and protein level). Behzad et al. (2015) and Yooseph et al. (2013) argue that whole-genome metagenomic sequencing could determine what specific metabolic activity is taking place in the atmosphere. However, metagenomics cannot distinguish between the metabolic capacities necessary for an airborne state, and those of passive (and often dead or dormant) airborne bacteria. Therefore, metagenomics will have to be combined with other techniques before new atmospheric functions of airborne bacteria can be established. 3. Human health The air is often considered an important carrier medium for bacterial pathogens, such as Streptococcus pneumoniae, Streptococcus pyogenes, Mycoplasma pneumoniae, Haemophilus influenzae, Klebsiella pneumoniae, Pseudomonas aeruginosa and Mycobacterium tuberculosis. In order to manage outdoor pathogens, it is important to understand and identify their source, survival, dispersal and relation to the environment. For more information on the detection, monitoring, and transportation of bacterial pathogens in the atmosphere, we refer to other reviews such as of Lai et al. (2009) and Kuske (2006), who more extensively cover this topic. As previously discussed, dust events play an important role in the aerosolization and transport of bacteria, which may also have important consequences for the spread of disease (Griffin, 2007). A wellknown case is the meningococcal meningitis outbreaks throughout sub-Saharan Africa, strongly corresponding to the dry seasons frequented with dust storms, and ceasing with the onset of the wet season (Molesworth et al., 2002). The dust particles, in a setting of low absolute humidity, are also believed to facilitate infection by causing abrasions of the nasopharyngeal mucosa, thus allowing the entry of Neisseria meningitidis. Apart from pathogens, airborne microbes and their components (e.g. endotoxins, mycotoxins, glucans) may also strongly influence our health in specific settings. Airborne biological agents have become prominent safety and health issues in agriculture, biotechnology, and industrial settings (Eduard et al., 2012; Martinez et al., 2004). Much of the concern has focused on the capacity of these agents to elicit allergic or inflammatory responses. Of the bacterial fraction of these agents, lipopolysaccharides (LPS) also known as endotoxins are most commonly studied in the air. They are found in the outer membrane of Gram-negative bacteria, and can produce a strong immune response, independent on the viability of the bacteria. Furthermore, endotoxins are particularly durable, and together with their ubiquitous presence, they are a frequent visitor to our respiratory tracts. Although it is clear that high endotoxin concentrations can cause acute and chronic health effects (Rylander, 2006), the current lack of an occupational exposure limit is mainly due to inter-laboratory variability and the absence of a standard, international protocol for sampling and analyzing airborne endotoxins. Factors influencing the type and height of our immune response towards endotoxins are, however, complex and may result in either a beneficial or detrimental outcome. These factors include the individual’s immune susceptibility (previous exposures and genetic predisposition), time and dose exposure, and synergistic contaminants (Liu, 2002). For the latter for instance, endotoxins form an important component of airborne particulate matter and are believed to amplify the immune response of PM co-pollutants such as transition metals (Degobbi et al., 2011). These synergistic effects have been mainly demonstrated in cell models (den Hartigh et al.,

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2010; Imrich et al., 1999; Long et al., 2001) but have also been shown in the Cincinnati Childhood Allergy and Air Pollution highrisk birth cohort study, where exposure to traffic-related particles and endotoxin during infancy is associated with wheezing at age 3 years (Ryan et al., 2009). As yet briefly indicated above, the role of airborne endotoxins is not always a detrimental one. The most widely studied beneficial role of endotoxin involves immune stimulation and maturation. Some studies suggest that exposure in early childhood to microbes and their components (e.g. endotoxins) is fundamental for developing the immune system and preventing the onset of allergies and atopic asthma (Liebers et al., 2008; Mutius, 2000; Schuijs et al., 2015). This is in concordance with epidemiological data showing that children raised in rural areas of developing countries and in farming communities have a lower prevalence of allergy and €nder asthma when compared with urban populations (Braun-Fahrla et al., 1999; Ernst and Cormier, 2000). However, further research is needed to highlight exposure conditions and synergistic effects of endotoxin with other environmental factors, together with the potential for early immune modulatory approaches for asthma therapy and prevention. 4. Potential applications With technological advances and our increasing knowledge of the role of airborne bacteria, a variety of practical applications can be foreseen. 4.1. Improving air quality The detection of pathogenic bacteria dispersed in outdoor air is an important concern for public health, agriculture and biothreat surveillance. Promising real-time techniques include single particle laser desorption/ionisation time-of-flight mass spectrometry, which could for example specifically detect M. tuberculosis at relevant airborne concentrations (Tobias et al., 2005). Despite the current methods used, the atmosphere provides a complex and diverse background for the accurate detection of bacterial pathogens, which remains an inevitable obstacle (Kuske et al., 2006). Another application pertains to better air quality management, by understanding how bacterial exposures affect our health. For example, source tracking allowed Bowers et al. (2011b) to discover that dog faeces was likely the dominant source of bacteria in outdoor air during winter periods in Cleveland and Detroit. Incidences such as this could result in new measures and policies to protect or improve air quality. Our lungs are the largest interface between the human host and the external environment, being exposed to more than 8000 L of inhaled air each day. Subsequently, understanding how the diversity, composition and components of airborne bacteria affect our immune systems is crucial, since the impact of airborne bacteria to human health is not only detrimental, but can also be beneficial. Finally, airborne bacteria may be applied for their use in bioremediation. Currently, bioremediation is more commonly applied in polluted soils, for which it is gaining increasing interest for its low costs and environmental impacts (Kurisu and Yagi, 2010). At present, bioremediation of air is mainly limited to biofilters for odour treatment and low-concentration-VOC (volatile organic compounds) degradation. Nevertheless, for these purposes, it is the most cost-efficient and durable method available (Estrada et al., 2012; European Commission, 2003). Additionally, the degradation of organic compounds by atmospherically-isolated microbes is an encouraging indication for their bioremedial potential, even in nutrient-poor circumstances.

4.2. Predicting the dispersion of airborne pathogens The knowledge on the transportation of bacteria by air currents can aid in the prevention of airborne spread of pathogens or source identification. Nguyen et al. (2006) used disease incidence and the atmospheric modelling tool, ADMS (McHugh et al., 1997), to determine the dispersion of a Legionella pneumophila outbreak. They managed to identify the source of the pathogen and the most important risk factors for people living nearby. This case study proves that models of airborne pathogen dispersal can be useful for timely intervention at the source of an airborne pathogen with additional measures to decrease the risk of people getting infected. Besides ADMS, computational fluid dynamics (CFD) has also been used to predict the dispersion of airborne microorganisms (Hathway et al., 2011). These two different modelling approaches have not been extensively studied for their performance with airborne bacteria, but seem to result in similar trends when applied to airborne dust dispersal (Rinaldi and Mukhriza, 2011). Furthermore, pathogens of fauna and flora are also transported through the atmosphere, often associated with dust plumes (Gonzalez-Martin et al., 2014; Kellogg and Griffin, 2006). Therefore, improving these modelling methods is not only advantageous for the abatement of human disease incidence, but also for gaining insight in the spread of plant or animal pathogens of economic and ecologic importance. 4.3. Reducing climate change Although challenging, weather models and future climate predictions can also become more accurate by integrating airborne bacteria and their effects. Radiative forcing, temperature and humidity can be indirectly altered by airborne bacteria, because these microorganisms can affect the amount of precipitation and cloud cover (section 2.6). These meteorological factors, in turn, will affect terrestrial and aquatic ecosystems and cause feedback to conditions for aerosolization and microbial life in the atmosphere (Christner et al., 2008b; Jaenicke, 2005). Related to this, Morris et al. (2014) re-evaluated the hypothesis of the bioprecipitation cycle, a feedback cycle whereby potential ice nucleating microorganisms are aerosolized from plants and subsequently initiate precipitation to sustain plant growth and associated microorganisms, originally proposed by Sands et al. (1982). These are invaluable insights when estimating the impact of tree planting and deforestation. Future research might reveal that the introduction of certain nucleating bacteria in an environment or the introduction of certain plant taxa that sustain them, would help in attaining desirable weather patterns. 4.4. Predictions on a global scale To model the global effects of airborne bacteria on human health, atmospheric chemistry and climate, we first need a reliable model of global bacterial transport and concentrations. Burrows et al. (2009a) have attempted to model airborne bacterial concentrations by using an atmospheric general circulation model. Despite the agreement with existing experimental data, their model still has many limitations as knowledge of emissions, dispersal, deposition, cell survival, metabolism and cell division is still developing. To increase input data for these kind of models, methods that allow real-time monitoring of airborne bacteria are important. Real-time detection of bacteria in a complex mixture of aerosols has proven challenging, however, single-particle induced fluorescence seems to be a promising technique. The applicability of laserinduced-fluorescence is still being explored, but bacteria in different aerosols (>3 mm) can be detected due to the fluorescence

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of polycyclic aromatic hydrocarbon compounds in the bacteria (Pan et al., 2007). UV-induced fluorescence can also be used to detect particles associated with bacteria (Gabey et al., 2013; Miyakawa et al., 2015). However, bacteria may occur in complex mixtures and more research is needed to quantify airborne bacteria in situ, using these real-time fluorescence techniques. To further improve the modelling of the effects of airborne bacteria on human health and atmospheric chemistry, approaches focusing more on bacterial function may be applied for the assessment of community structure and the potential functions of the community members. Recent metagenomic approaches such as by Yooseph et al. (2013) and Cao et al. (2014) allow a more thorough assessment of the full extent of the impact of airborne microbes in atmospheric chemistry and their allergenic and pathogenic potentials. For instance, the work of Cao et al. (2014) showed that the majority of the inhalable microorganisms were soil-associated and non-pathogenic to humans. 4.5. Biotechnology Airborne bacteria can also be considered as a useful source for novel enzymes. It can be expected that they possess valuable characteristics applicable in biotechnological industries, because the atmospheric bacterial communities are highly diverse and exposed to a unique environment. For example, bacterial growth at low temperatures indicates potential applications in lowtemperature and freezing processes (Christner, 2010; Huston, 2008). In addition, secondary metabolites of airborne bacteria can be useful, such as pigments, which are used for the development of sunscreen (Geng et al., 2008) and medicines (Vaishnav and Demain, 2011). 5. Conclusions Airborne bacteria affect both physical processes in the atmosphere, such as cloud formation and precipitation, and atmospheric chemistry via cloudborne bacteria. However, the hypothesis that a fraction of the atmospheric bacteria are forming actual microbial communities remains to be definitively proven. Nevertheless, many indicative studies have been published and it is likely that future metagenomics and related research will improve our understanding of bacterial activity in the atmosphere. Further research of the presence and purpose of airborne microbes will open up opportunities for new applications concerning human health, air quality and weather patterns. Additionally, airborne bacteria are useful for biotechnological applications, because of their unique metabolic enzymes and metabolites, and their stress resistance capacities to typical airborne conditions such as drought, UV irradiation, specific pollutants and low temperatures. The potential applicability and impact of airborne bacteria will undoubtedly encourage more extensive microbiological research of the atmosphere. Conflict of interest The authors declare no conflict of interest. Acknowledgments The authors are very grateful to Prof. Noah Fierer for his insightful comments and to Sven Cloostermans for the artwork of Fig. 1. The authors also thank Dr Ingmar Claes for revising the text. This research was financially supported by the University of Antwerp (project ID 28645), EUROSA (29560), the Fund for Scientific Research Flanders (FWO-Vlaanderen) (1120116N and 1507114N) and the ProCure IWT SBO (150052).

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