Atmospheric Environment 139 (2016) 214e221

Contents lists available at ScienceDirect

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
University of Antwerp, Dept. Bioscience Engineering, Environmental Ecology and Applied Microbiology, Antwerp, Belgium
b
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: Numerous recent studies have highlighted that the types of bacteria present in the atmosphere often
Received 2 February 2016 show predictable patterns across space and time. These patterns can be driven by differences in bacterial
Received in revised form sources of the atmosphere and a wide range of environmental factors, including UV intensity, precipi-
27 April 2016
tation events, and humidity. The abundance of certain bacterial taxa is of interest, not only for their
Accepted 21 May 2016
Available online 24 May 2016
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
Keywords:
Airborne bacteria
applicability. Improving air quality, modelling the dispersal of airborne bacteria (e.g. pathogens) and
Endotoxin biotechnological purposes are already being explored. Nevertheless, many technological challenges still
Respiratory health need to be overcome to fully understand the roles of airborne bacteria in our health and global
Air quality ecosystems.
Atmospheric modelling © 2016 Elsevier Ltd. All rights reserved.

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.
2.1. Sources
E-mail address: sarah.lebeer@uantwerpen.be (S. Lebeer).
1
Equal contribution. Bacteria enter the near-surface atmosphere by aerosolization

http://dx.doi.org/10.1016/j.atmosenv.2016.05.038
1352-2310/© 2016 Elsevier Ltd. All rights reserved.
 W. Smets et al. / Atmospheric Environment 139 (2016) 214e221 215

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 ob-
servations. 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 environ-
ments, 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
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
(Barbera
n et al., 2014; Hara and Zhang, 2012; Kellogg and Griffin,
2006; Lim et al., 2011; Polymenakou et al., 2008). These dust
events are known to cause great changes in the downwind atmo-
spheric 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 tropo-
sphere 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 long-
distance 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.
216 W. Smets et al. / Atmospheric Environment 139 (2016) 214e221
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, sea-
sonality, 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 atmo-
spheric 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
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
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, DNA-
repair mechanisms, pigmentation, mechanisms promoting aggre-
gation, 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 ag-
gregates of bacteria and substrate allow the activity and in-
teractions that are typical of an atmosphere biome.
Another protection mechanism of bacteria is to enter a non-
dividing 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 in-
creases 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).
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)
 W. Smets et al. / Atmospheric Environment 139 (2016) 214e221
2.6. Atmospheric interactions
The inevitable question therefore arises, whether the viable
airborne bacteria are merely trying to survive the harsh atmo-
spheric environment by ceasing all activity or if they play an active
role in modifying environmental conditions within the atmo-
sphere. 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 bac-
teria 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;
Lohmann and Feichter, 2005; Mo €hler et al., 2007; Morris et al.,
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 atmo-
sphere 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 hu-
midity were dividing within 1e2 h. However, this experimental
setup did not mimic the natural cloud conditions, thus only indi-
cating 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 temper-
atures typically encountered in troposphere clouds. However,
conditions in clouds differ markedly from the rest of the atmo-
sphere 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 microor-
ganisms. Therefore, it can be hypothesised that aggregates of mi-
crobes 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 at-
mosphere. However, real proof of interacting bacterial commu-
nities in the outdoor air seems challenging to produce. To tackle
this problem, there is a need for in situ detection of bacterial-
activity-indicators, such as, substrate degradation, cell division,
crosstalk molecules or a high ATP to cell ratio. Although, when in
217
situ detection is not feasible, a closed atmospheric chamber such as
that used by Amato et al. (2015) may be employed. Other ap-
proaches 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 meta-
genomic sequencing could determine what specific metabolic ac-
tivity 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 com-
bined 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, Strepto-
coccus 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 detec-
tion, 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 pre-
viously discussed, dust events play an important role in the aero-
solization and transport of bacteria, which may also have important
consequences for the spread of disease (Griffin, 2007). A well-
known 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 expo-
sure 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 in-
dividual’s immune susceptibility (previous exposures and genetic
predisposition), time and dose exposure, and synergistic contami-
nants (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.,
218 W. Smets et al. / Atmospheric Environment 139 (2016) 214e221
2010; Imrich et al., 1999; Long et al., 2001) but have also been
shown in the Cincinnati Childhood Allergy and Air Pollution high-
risk 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 devel-
oping 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
asthma when compared with urban populations (Braun-Fahrla €nder
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 patho-
gens, 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 out-
door 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 bac-
teria 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 biore-
mediation. 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 pre-
sent, bioremediation of air is mainly limited to biofilters for odour
treatment and low-concentration-VOC (volatile organic com-
pounds) 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). Further-
more, 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 abate-
ment 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 pre-
dictions can also become more accurate by integrating airborne
bacteria and their effects. Radiative forcing, temperature and hu-
midity 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 feed-
back 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 concen-
trations 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, depo-
sition, 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 laser-
induced-fluorescence is still being explored, but bacteria in
different aerosols (>3 mm) can be detected due to the fluorescence
 W. Smets et al. / Atmospheric Environment 139 (2016) 214e221
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 po-
tentials. 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 low-
temperature 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 atmo-
sphere, 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 understand-
ing of bacterial activity in the atmosphere. Further research of the
presence and purpose of airborne microbes will open up oppor-
tunities 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 Ant-
werp (project ID 28645), EUROSA (29560), the Fund for Scientific
Research Flanders (FWO-Vlaanderen) (1120116N and 1507114N)
and the ProCure IWT SBO (150052).
219
References
Albrecht, A., Witzenberger, R., Bernzen, U., Jackel, U., 2007. Detection of airborne
microbes in a composting facility by cultivation based and cultivation-
independent methods. Ann. Agric. Environ. Med. 14 (1), 81e85.
Aller, J.Y., Kuznetsova, M.R., Jahns, C.J., Kemp, P.F., 2005. The sea surface microlayer
as a source of viral and bacterial enrichment in marine aerosols. J. Aerosol. Sci.
36 (5), 801e812.
Amato, P., Joly, M., Schaupp, C., Attard, E., Mo € hler, O., Morris, C., Brunet, Y.,
Delort, A.-M., 2015. Survival and ice nucleation activity of bacteria as aerosols in
a cloud simulation chamber. Atmos. Chem. Phys. Discuss. 15 (3), 4055e4082.
Amato, P., Me
nager, M., Sancelme, M., Laj, P., Mailhot, G., Delort, A.-M., 2005. Mi-
crobial population in cloud water at the Puy de Do ^ me: implications for the
chemistry of clouds. Atmos. Environ. 39 (22), 4143e4153.
Amato, P., Parazols, M., Sancelme, M., Laj, P., Mailhot, G., Delort, A.M., 2007. Mi-
croorganisms isolated from the water phase of tropospheric clouds at the Puy
^me: major groups and growth abilities at low temperatures. FEMS
de Do
Microbiol. Ecol. 59 (2), 242e254.
An, S., Couteau, C., Luo, F., Neveu, J., DuBow, M.S., 2013. Bacterial diversity of surface
sand samples from the Gobi and Taklamaken deserts. Micro. Ecol. 66 (4),
850e860.
Ariya, P.A., Nepotchatykh, O., Ignatova, O., Amyot, M., 2002. Microbiological
degradation of atmospheric organic compounds. Geophys. Res. Lett. 29 (22),
2077.
€r, M., Hardenberg, J., Meron, E., Provenzale, A., 2002. Modelling the survival of
Ba
bacteria in drylands: the advantage of being dormant. Proc. R. Soc. Lond. B. Biol.
Sci. 269 (1494), 937e942.
Barber
an, A., Henley, J., Fierer, N., Casamayor, E.O., 2014. Structure, inter-annual
recurrence, and global-scale connectivity of airborne microbial communities.
Sci. Total Environ. 487, 187e195.
Bauer, H., Giebl, H., Hitzenberger, R., Kasper-Giebl, A., Reischl, G., Zibuschka, F.,
Puxbaum, H., 2003. Airborne bacteria as cloud condensation nuclei. J. Geophys.
Res. Atmos. 108 (D21), 1984e2012.
Behzad, H., Gojobori, T., Mineta, K., 2015. Challenges and opportunities of airborne
metagenomics. Genome Biol. Evol. 7 (5), 1216e1226.
Bertolini, V., Gandolfi, I., Ambrosini, R., Bestetti, G., Innocente, E., Rampazzo, G.,
Franzetti, A., 2012. Temporal variability and effect of environmental variables on
airborne bacterial communities in an urban area of Northern Italy. Appl.
Microbiol. Biotechnol. 1e10.
Bertolini, V., Gandolfi, I., Ambrosini, R., Bestetti, G., Innocente, E., Rampazzo, G.,
Franzetti, A., 2013. Temporal variability and effect of environmental variables on
airborne bacterial communities in an urban area of Northern Italy. Appl.
Microbiol. Biotechnol. 97 (14), 6561e6570.
Bigg, E., Soubeyrand, S., Morris, C., 2015. Persistent after-effects of heavy rain on
concentrations of ice nuclei and rainfall suggest a biological cause. Atmos.
Chem. Phys. 15 (5), 2313e2326.
Blanchard, D.C., 1989. The ejection of drops from the sea and their enrichment with
bacteria and other materials: a review. Estuaries 12 (3), 127e137.
Bottos, E.M., Woo, A.C., Zawar-Reza, P., Pointing, S.B., Cary, S.C., 2014. Airborne
bacterial populations above desert soils of the McMurdo Dry Valleys, Antarctica.
Micro. Ecol. 67 (1), 120e128.
Bowers, R.M., Clements, N., Emerson, J.B., Wiedinmyer, C., Hannigan, M.P., Fierer, N.,
2013. Seasonal variability in bacterial and fungal diversity of the near-surface
atmosphere. Environ. Sci. Technol. 47 (21), 12097e12106.
Bowers, R.M., McCubbin, I.B., Hallar, A.G., Fierer, N., 2012. Seasonal variability in
airborne bacterial communities at a high-elevation site. Atmos. Environ. 50,
41e49.
Bowers, R.M., McLetchie, S., Knight, R., Fierer, N., 2011a. Spatial variability in
airborne bacterial communities across land-use types and their relationship to
the bacterial communities of potential source environments. ISME J. 5 (4),
601e612.
Bowers, R.M., Sullivan, A.P., Costello, E.K., Collett, J.L., Knight, R., Fierer, N., 2011b.
Sources of bacteria in outdoor air across cities in the midwestern United States.
Appl. Environ. Microbiol. 77 (18), 6350e6356.
Braun-Fahrla €nder, C., Gassner, M., Grize, L., Neu, U., Sennhauser, F., Varonier, H.,
Vuille, J., Wüthrich, B., 1999. Prevalence of hay fever and allergic sensitization in
farmer’s children and their peers living in the same rural community. Clin. Exp.
Allergy 29 (1), 28e34.
Brodie, E.L., DeSantis, T.Z., Parker, J.P.M., Zubietta, I.X., Piceno, Y.M., Andersen, G.L.,
2007. Urban aerosols harbor diverse and dynamic bacterial populations. Proc.
Natl. Acad. Sci. U. S. A. 104 (1), 299e304.
Burrows, S., Butler, T., Jo € ckel, P., Tost, H., Kerkweg, A., Po € schl, U., Lawrence, M.,
2009a. Bacteria in the global atmosphereePart 2: modeling of emissions and
transport between different ecosystems. Atmos. Chem. Phys. 9 (23), 9281e9297.
Burrows, S., Elbert, W., Lawrence, M., Po €schl, U., 2009b. Bacteria in the global
atmosphereePart 1: review and synthesis of literature data for different eco-
systems. Atmos. Chem. Phys. 9 (23), 9263e9280.
Cao, C., Jiang, W., Wang, B., Fang, J., Lang, J., Tian, G., Jiang, J., Zhu, T.F., 2014. Inhalable
microorganisms in Beijing’s PM2. 5 and PM10 pollutants during a severe smog
event. Environ. Sci. Technol. 48 (3), 1499e1507.
Christner, B.C., 2010. Bioprospecting for microbial products that affect ice crystal
formation and growth. Appl. Microbiol. Biotechnol. 85 (3), 481e489.
Christner, B.C., Cai, R., Morris, C.E., McCarter, K.S., Foreman, C.M., Skidmore, M.L.,
Montross, S.N., Sands, D.C., 2008a. Geographic, seasonal, and precipitation
220 W. Smets et al. / Atmospheric Environment 139 (2016) 214e221
chemistry influence on the abundance and activity of biological ice nucleators
in rain and snow. Proc. Natl. Acad. Sci. U. S. A. 105 (48), 18854e18859.
Christner, B.C., Morris, C.E., Foreman, C.M., Cai, R., Sands, D.C., 2008b. Ubiquity of
biological ice nucleators in snowfall. Science 319 (5867), 1214e1214.
de Leeuw, G., Andreas, E.L., Anguelova, M.D., Fairall, C., Lewis, E.R., O’Dowd, C.,
Schulz, M., Schwartz, S.E., 2011. Production flux of sea spray aerosol. Rev.
Geophys 49 (2), RG2001.
Degobbi, C., Saldiva, P.H.N., Rogers, C., 2011. Endotoxin as modifier of particulate
matter toxicity: a review of the literature. Aerobiologia 27 (2), 97e105.
DeLeon-Rodriguez, N., Lathem, T.L., Rodriguez-R, L.M., Barazesh, J.M., Anderson, B.E.,
Beyersdorf, A.J., Ziemba, L.D., Bergin, M., Nenes, A., Konstantinidis, K.T., 2013.
Microbiome of the upper troposphere: species composition and prevalence,
effects of tropical storms, and atmospheric implications. Proc. Natl. Acad. Sci. U.
S. A. 110 (7), 2575e2580.
Delort, A.-M., Vaïtilingom, M., Amato, P., Sancelme, M., Parazols, M., Mailhot, G.,
Laj, P., Deguillaume, L., 2010. A short overview of the microbial population in
clouds: potential roles in atmospheric chemistry and nucleation processes.
Atmos. Res. 98 (2), 249e260.
den Hartigh, L., Lame
, M., Ham, W., Kleeman, M., Tablin, F., Wilson, D., 2010.
Endotoxin and polycyclic aromatic hydrocarbons in ambient fine particulate
matter from Fresno, California initiate human monocyte inflammatory re-
sponses mediated by reactive oxygen species. Toxicol. in Vitro 24 (7),
1993e2002.
Di Giorgio, C., Krempff, A., Guiraud, H., Binder, P., Tiret, C., Dumenil, G., 1996. At-
mospheric pollution by airborne microorganisms in the city of Marseilles.
Atmos. Environ. 30 (1), 155e160.
Dimmick, R.L., Wolochow, H., Chatigny, M.A., 1979. Evidence that bacteria can form
new cells in airborne particles. Appl. Environ. Microbiol. 37 (5), 924e927.
Eduard, W., Heederik, D., Duchaine, C., Green, B.J., 2012. Bioaerosol exposure
assessment in the workplace: the past, present and recent advances. J. Environ.
Monit. 14 (2), 334e339.
Ernst, P., Cormier, Y., 2000. Relative scarcity of asthma and atopy among rural ad-
olescents raised on a farm. Am. J. Respir. Crit. Care Med. 161 (5), 1563e1566.
Estrada, J.M., Kraakman, N.B., Lebrero, R., Mun ~ oz, R., 2012. A sensitivity analysis of
process design parameters, commodity prices and robustness on the economics
of odour abatement technologies. Biotechnol. Adv. 30 (6), 1354e1363.
European Commission (2003). IPPC reference document on the best available
techniques in common waste water and waste gas teatment/management
systems in the chemical sector. Sevilla.
Fahlgren, C., Hagstro €m Å., Nilsson D., Zweifel, U.L., 2010. Annual variations in the
diversity, viability, and origin of airborne bacteria. Appl. Environ. Microbiol. 76
(9), 3015e3025.
Fang, Z., Ouyang, Z., Zheng, H., Wang, X., Hu, L., 2007. Culturable airborne bacteria in
outdoor environments in Beijing, China. Micro. Ecol. 54 (3), 487e496.
Franzetti, A., Gandolfi, I., Gaspari, E., Ambrosini, R., Bestetti, G., 2011. Seasonal
variability of bacteria in fine and coarse urban air particulate matter. Appl.
Microbiol. Biotechnol. 90 (2), 745e753.
Fujimura, K.E., Johnson, C.C., Ownby, D.R., Cox, M.J., Brodie, E.L., Havstad, S.L.,
Zoratti, E.M., Woodcroft, K.J., Bobbitt, K.R., Wegienka, G., 2010. Man’s best
friend? The effect of pet ownership on house dust microbial communities.
J. Allergy Clin. Immunol. Pract. 126 (2), 410e412.
Gabey, A., Vaitilingom, M., Freney, E., Boulon, J., Sellegri, K., Gallagher, M.,
Crawford, I., Robinson, N., Stanley, W., Kaye, P.H., 2013. Observations of fluo-
rescent and biological aerosol at a high-altitude site in central France. Atmos.
Chem. Phys. 13 (15), 7415e7428.
Gandolfi, I., Bertolini, V., Ambrosini, R., Bestetti, G., Franzetti, A., 2013. Unravelling
the bacterial diversity in the atmosphere. Appl. Microbiol. Biotechnol. 97 (11),
4727e4736.
Geng, J., Tang, W., Wan, X., Zhou, Q., Wang, X.J., Shen, P., Lei, T.C., Chen, X.D., 2008.
Photoprotection of bacterial-derived melanin against ultraviolet Aeinduced cell
death and its potential application as an active sunscreen. J. Eur. Acad. Der-
matol. Venereol. 22 (7), 852e858.
Gonzalez-Martin, C., Teigell-Perez, N., Valladares, B., Griffin, D.W., 2014. The global
dispersion of pathogenic microorganisms by dust storms and its relevance to
agriculture. In: Sparks, D.L. (Ed.), Advances in Agronomy. Elsevier, pp. 1e41.
Griffin, D.W., 2007. Atmospheric movement of microorganisms in clouds of desert
dust and implications for human health. Clin. Microbiol. Rev. 20 (3), 459e477.
Griffin, D.W., Gonzalez, C., Teigell, N., Petrosky, T., Northup, D.E., Lyles, M., 2011.
Observations on the use of membrane filtration and liquid impingement to
collect airborne microorganisms in various atmospheric environments. Aero-
biologia 27 (1), 25e35.
Han, Y., Li, L., Liu, J., Zhang, M., 2012. Microbial structure and chemical components
of aerosols caused by rotating brushes in a wastewater treatment plant. Envi-
ron. Sci. Pollut. Res. 19 (9), 4097e4108.
Hara, K., Zhang, D., 2012. Bacterial abundance and viability in long-range trans-
ported dust. Atmos. Environ. 47, 20e25.
Hathway, E., Noakes, C., Sleigh, P., Fletcher, L., 2011. CFD simulation of airborne
pathogen transport due to human activities. Build. Environ. 46 (12), 2500e2511.
Hill, T.C., Moffett, B.F., DeMott, P.J., Georgakopoulos, D.G., Stump, W.L., Franc, G.D.,
2014. Measurement of ice nucleation-active bacteria on plants and in precipi-
tation by quantitative PCR. Appl. Environ. Microbiol. 80 (4), 1256e1267.
Huffman, J.A., Po €hlker, C., Prenni, A., DeMott, P., Mason, R., Robinson, N., Fro €hlich-
Nowoisky, J., Tobo, Y., Despre
s, V., Garcia, E., 2013. High concentrations of bio-
logical aerosol particles and ice nuclei during and after rain. Atmos. Chem. Phys.
Discuss. 13 (1), 1767e1793.
Huston, A.L., 2008. Biotechnological Aspects of Cold-adapted Enzymes, Psychro-
philes: from Biodiversity to Biotechnology. Springer, pp. 347e363.
Imrich, A., Ning, Y.Y., Koziel, H., Coull, B., Kobzik, L., 1999. Lipopolysaccharide
priming amplifies lung macrophage tumor necrosis factor production in
response to air particles. Toxicol. Appl. Pharmacol. 159 (2), 117e124.
Jaenicke, R., 2005. Abundance of cellular material and proteins in the atmosphere.
Science 308 (5718), 73e73.
Jeon, E.M., Kim, H.J., Jung, K., Kim, J.H., Kim, M.Y., Kim, Y.P., Ka, J.-O., 2011. Impact of
Asian dust events on airborne bacterial community assessed by molecular an-
alyses. Atmos. Environ. 45 (25), 4313e4321.
Joly, M., Attard, E., Sancelme, M., Deguillaume, L., Guilbaud, C., Morris, C.E.,
Amato, P., Delort, A.-M., 2013. Ice nucleation activity of bacteria isolated from
cloud water. Atmos. Environ. 70, 392e400.
Jones, A.M., Harrison, R.M., 2004. The effects of meteorological factors on atmo-
spheric bioaerosol concentrationsda review. Sci. Total Environ. 326 (1),
151e180.
Jones, S.E., Newton, R.J., McMahon, K.D., 2008. Potential for atmospheric deposition
of bacteria to influence bacterioplankton communities. FEMS Microbiol. Ecol.
64 (3), 388e394.
Katra, I., Arotsker, L., Krasnov, H., Zaritsky, A., Kushmaro, A., Ben-Dov, E., 2014.
Richness and diversity in dust stormborne biomes at the Southeast Mediter-
ranean. Sci. Rep. 4.
Kellogg, C.A., Griffin, D.W., 2006. Aerobiology and the global transport of desert
dust. Trends Ecol. Evol. 21 (11), 638e644.
Klironomos, J.N., Rillig, M.C., Allen, M.F., Zak, D.R., Pregitzer, K.S., Kubiske, M.E., 1997.
Increased levels of airborne fungal spores in response to Populus tremuloides
grown under elevated atmospheric CO2. Can. J. Bot. 75 (10), 1670e1673.
Kobayashi, F., Maki, T., Kakikawa, M., Yamada, M., Puspitasari, F., Iwasaka, Y., 2015.
Bioprocess of Kosa bioaerosols: effect of ultraviolet radiation on airborne bac-
teria within Kosa (Asian dust). J. Biosci. Bioeng. 119 (5), 570e579.
Kurisu, F., Yagi, O., 2010. Bioremediation of Soil and Groundwater Contaminated by
Volatile Organic Compounds, Sustainability in Food and Water. Springer,
Netherlands, pp. 411e416.
Kuske, C.R., 2006. Current and emerging technologies for the study of bacteria in
the outdoor air. Curr. Opin. Biotechnol. 17 (3), 291e296.
Kuske, C.R., Barns, S.M., Grow, C.C., Merrill, L., Dunbar, J., 2006. Environmental
survey for four pathogenic bacteria and closely related species using phyloge-
netic and functional genes. J. Forensic. Sci. 51 (3), 548e558.
Lai, K., Emberlin, J., Colbeck, I., 2009. Outdoor environments and human pathogens
in air. Environ. Health 8 (Suppl. 1), S15.
Lee, A.K., Lau, A.P., Cheng, J.Y., Fang, M., Chan, C.K., 2007. Source identification
analysis for the airborne bacteria and fungi using a biomarker approach. Atmos.
Environ. 41 (13), 2831e2843.
Li, K., Dong, S., Wu, Y., Yao, M., 2010. Comparison of the biological content of air
samples collected at ground level and at higher elevation. Aerobiologia 26 (3),
233e244.
Liebers, V., Raulf-Heimsoth, M., Brüning, T., 2008. Health effects due to endotoxin
inhalation (review). Arch. Toxicol. 82 (4), 203e210.
Lighthart, B., 1997. The ecology of bacteria in the alfresco atmosphere. FEMS
Microbiol. Ecol. 23 (4), 263e274.
Lighthart, B., Shaffer, B., 1994. Bacterial flux from chaparral into the atmosphere in
mid-summer at a high desert location. Atmos. Environ. 28 (7), 1267e1274.
Lim, N., Munday, C.I., Allison, G.E., O’Loingsigh, T., De Deckker, P., Tapper, N.J., 2011.
Microbiological and meteorological analysis of two Australian dust storms in
April 2009. Sci. Total Environ. 412, 223e231.
Lindow, S., 1982. Phytopathogenic Prokaryotes. In: Epiphytic Ice Nucleation-active
Bacteria, vol. 1, pp. 335e362.
Lindow, S.E., Arny, D.C., Upper, C.D., 1982. Bacterial ice nucleation: a factor in frost
injury to plants. Plant. Physiol. 70 (4), 1084e1089.
Liu, A.H., 2002. Endotoxin exposure in allergy and asthma: reconciling a paradox.
J. Allergy Clin. Immunol. Pract. 109 (3), 379e392.
Lohmann, U., Feichter, J., 2005. Global indirect aerosol effects: a review. Atmos.
Chem. Phys. 5 (3), 715e737.
Long, C.M., Suh, H.H., Kobzik, L., Catalano, P.J., Ning, Y.Y., Koutrakis, P., 2001. A pilot
investigation of the relative toxicity of indoor and outdoor fine particles:
in vitro effects of endotoxin and other particulate properties. Environ. Health
Perspect. 109 (10), 1019e1026.
Maki, T., Hara, K., Kobayashi, F., Kurosaki, Y., Kakikawa, M., Matsuki, A., Chen, B.,
Shi, G., Hasegawa, H., Iwasaka, Y., 2015. Vertical distribution of airborne bac-
terial communities in an Asian-dust downwind area, Noto Peninsula. Atmos.
Environ. 119, 282e293.
Maki, T., Kakikawa, M., Kobayashi, F., Yamada, M., Matsuki, A., Hasegawa, H.,
Iwasaka, Y., 2013. Assessment of composition and origin of airborne bacteria in
the free troposphere over Japan. Atmos. Environ. 74, 73e82.
Maki, T., Puspitasari, F., Hara, K., Yamada, M., Kobayashi, F., Hasegawa, H.,
Iwasaka, Y., 2014. Variations in the structure of airborne bacterial communities
in a downwind area during an Asian dust (Kosa) event. Sci. Total Environ. 488,
75e84.
Maki, T., Susuki, S., Kobayashi, F., Kakikawa, M., Yamada, M., Higashi, T., Chen, B.,
Shi, G., Hong, C., Tobo, Y., 2008. Phylogenetic diversity and vertical distribution
of a halobacterial community in the atmosphere of an Asian dust (KOSA) source
region, Dunhuang City. Air Qual. Atmos. Health 1 (2), 81e89.
Maron, P.-A., Lejon, D.P., Carvalho, E., Bizet, K., Lemanceau, P., Ranjard, L., Mougel, C.,
2005. Assessing genetic structure and diversity of airborne bacterial commu-
nities by DNA fingerprinting and 16S rDNA clone library. Atmos. Environ. 39
 W. Smets et al. / Atmospheric Environment 139 (2016) 214e221
(20), 3687e3695.
Martinez, K., Rao, C., Burton, N., 2004. Exposure assessment and analysis for bio-
logical agents. Grana 43 (4), 193e208.
McHugh, C., Carruthers, D., Edmunds, H., 1997. ADMS and ADMSeurban. Int. J.
Environ. Pollut. 8 (3e6), 438e440.
Miyakawa, T., Kanaya, Y., Taketani, F., Tabaru, M., Sugimoto, N., Ozawa, Y.,
Takegawa, N., 2015. Ground-based measurement of fluorescent aerosol parti-
cles in Tokyo in the spring of 2013: potential impacts of nonbiological materials
on autofluorescence measurements of airborne particles. J. Geophys. Res.
Atmos. 120 (3), 1171e1185.
Mo€hler, O., DeMott, P., Vali, G., Levin, Z., 2007. Microbiology and atmospheric
processes: the role of biological particles in cloud physics. Biogeosci. Discuss. 4
(4), 2559e2591.
Molesworth, A.M., Cuevas, L.E., Morse, A.P., Herman, J.R., Thomson, M.C., 2002. Dust
clouds and spread of infection. The Lancet 359 (9300), 81e82.
Monteil, C.L., Bardin, M., Morris, C.E., 2014. Features of air masses associated with
the deposition of Pseudomonas syringae and Botrytis cinerea by rain and
snowfall. ISME J. 8 (11), 2290e2304.
Morris, C., Sands, D., Bardin, M., Jaenicke, R., Vogel, B., Leyronas, C., Ariya, P.,
Psenner, R., 2011. Microbiology and atmospheric processes: research challenges
concerning the impact of airborne micro-organisms on the atmosphere and
climate. Biogeosci 8 (1), 17e25.
Morris, C.E., Conen, F., Alex Huffman, J., Phillips, V., Po € schl, U., Sands, D.C., 2014.
Bioprecipitation: a feedback cycle linking Earth history, ecosystem dynamics
and land use through biological ice nucleators in the atmosphere. Glob. Chang.
Biol. 20 (2), 341e351.
Munday, C.I., O’Loingsigh, T., Tapper, N.J., De Deckker, P., Allison, G.E., 2013. Uti-
lisation of Rep-PCR to track microbes in aerosols collected adjacent to their
source, a saline lake in Victoria, Australia. Sci. Total Environ. 450, 317e325.
Murata, K., Zhang, D., 2014. Transport of bacterial cells toward the Pacific in
northern hemisphere westerly winds. Atmos. Environ. 87, 138e145.
Mutius, V., 2000. Exposure to endotoxin or other bacterial components might
protect against the development of atopy. Clin. Exp. Allergy 30 (9), 1230e1234.
Nguyen, T.M.N., Ilef, D., Jarraud, S., Rouil, L., Campese, C., Che, D., Haeghebaert, S.,
Ganiayre, F., Marcel, F., Etienne, J., 2006. A community-wide outbreak of le-
gionnaires disease linked to industrial cooling towersdhow far can contami-
nated aerosols spread? J. Infect. Dis. 193 (1), 102e111.
Pan, Y.L., Hartings, J., Pinnick, R.G., Hill, S.C., Halverson, J., Chang, R.K., 2003. Single-
particle fluorescence spectrometer for ambient aerosols. Aerosol Sci. Tech. 37
(8), 628e639.
Pan, Y.L., Pinnick, R.G., Hill, S.C., Rosen, J.M., Chang, R.K., 2007. Single-particle laser-
induced-fluorescence spectra of biological and other organic-carbon aerosols in
the atmosphere: measurements at New Haven, Connecticut, and Las Cruces,
New Mexico. J. Geophys. Res. Atmos. 112, D24S19.
Pasteur, L., 1861. Me
moire sur les corpuscules organise
s qui existent dans
l’atmosphe re, examen de la doctrine des ge
ne

rations spontane
es. Ann. Sci. Nat.
Zool. 16, 5e98.
Peter, H., Ho € rtnagl, P., Reche, I., Sommaruga, R., 2014. Bacterial diversity and
composition during rain events with and without Saharan dust influence
reaching a high mountain lake in the Alps. Environ. Microbiol. Rep. 6 (6),
618e624.
Polymenakou, P.N., 2012. Atmosphere: a source of pathogenic or beneficial mi-
crobes? Atmosphere 3 (1), 87e102.
Polymenakou, P.N., Mandalakis, M., Stephanou, E.G., Tselepides, A., 2008. Particle
size distribution of airborne microorganisms and pathogens during an intense
African dust event in the eastern Mediterranean. Environ. Health Perspect. 116
(3), 292e296.
Puspitasari, F., Maki, T., Shi, G., Bin, C., Kobayashi, F., Hasegawa, H., Iwasaka, Y., 2015.
Phylogenetic analysis of bacterial species compositions in sand dunes and dust
aerosol in an Asian dust source area, the Taklimakan Desert. Air Qual. Atmos.
Health 1e14.
Ravva, S.V., Hernlem, B.J., Sarreal, C.Z., Mandrell, R.E., 2012. Bacterial communities in
urban aerosols collected with wetted-wall cyclonic samplers and seasonal
221
fluctuations of live and culturable airborne bacteria. J. Environ. Monit. 14 (2),
473e481.
Rinaldi, W., Mukhriza, T., 2011. Comparative study between ADMS and CFD in
modeling dust dispersion from a blasting events in quarry. J. Rekayasa Kim.
Lingkung. 8 (2), 89e94.
Rothschild, L.J., Mancinelli, R.L., 2001. Life in extreme environments. Nature 409
(6823), 1092e1101.
Ryan, P.H., Bernstein, D.I., Lockey, J., Reponen, T., Levin, L., Grinshpun, S.,
Villareal, M., Hershey, G.K.K., Burkle, J., LeMasters, G., 2009. Exposure to traffic-
related particles and endotoxin during infancy is associated with wheezing at
age 3 years. Am. J. Respir. Crit. Care Med. 180 (11), 1068e1075.
Rylander, R., 2006. Endotoxin and occupational airway disease. Curr. Opin. Allergy
Clin. Immunol. 6 (1), 62e66.
Sands, D., Langhans, V., Scharen, A., De Smet, G., 1982. The association between
bacteria and rain and possible resultant meteorological implications. J. Hung.
Meteorol. Serv. 86, 148e152.
Santos-Burgoa, C., Rosas, I., Yela, A., 1994. Occurrence of airborne enteric bacteria in
Mexico City. Aerobiologia 10 (1), 39e45.
Sattler, B., Puxbaum, H., Psenner, R., 2001. Bacterial growth in supercooled cloud
droplets. Geophys. Res. Lett. 28 (2), 239e242.
Schuijs, M.J., Willart, M.A., Vergote, K., Gras, D., Deswarte, K., Ege, M.J., Madeira, F.B.,
Beyaert, R., van Loo, G., Bracher, F., 2015. Farm dust and endotoxin protect
against allergy through A20 induction in lung epithelial cells. Science 349
(6252), 1106e1110.
Sciple, G., Riemensnider, D., Schleyer, C., 1967. Recovery of microorganisms shed by
humans into a sterilized environment. Appl. Microbiol. 15 (6), 1388e1392.
Shaffer, B.T., Lighthart, B., 1997. Survey of culturable airborne bacteria at four diverse
locations in Oregon: urban, rural, forest, and coastal. Micro. Ecol. 34 (3),
167e177.
Stres, B., Sul, W.J., Murovec, B., Tiedje, J.M., 2013. Recently deglaciated high-altitude
soils of the Himalaya: diverse environments, heterogenous bacterial commu-
nities and long-range dust inputs from the upper troposphere. PloS One 8 (9),
e76440.
Tobias, H.J., Schafer, M.P., Pitesky, M., Fergenson, D.P., Horn, J., Frank, M., Gard, E.E.,
2005. Bioaerosol mass spectrometry for rapid detection of individual airborne
Mycobacterium tuberculosis H37Ra particles. Appl. Environ. Microbiol. 71 (10),
6086e6095.
Tong, Y., Lighthart, B., 2000. The annual bacterial particle concentration and size
distribution in the ambient atmosphere in a rural area of the Willamette Valley,
Oregon. Aerosol Sci. Tech. 32 (5), 393e403.
Tringe, S.G., Zhang, T., Liu, X., Yu, Y., Lee, W.H., Yap, J., Yao, F., Suan, S.T., Ing, S.K.,
Haynes, M., 2008. The airborne metagenome in an indoor urban environment.
PLoS One 3 (4), e1862.
Vaishnav, P., Demain, A.L., 2011. Unexpected applications of secondary metabolites.
Biotechnol. Adv. 29 (2), 223e229.
Vaïtilingom, M., Amato, P., Sancelme, M., Laj, P., Leriche, M., Delort, A.-M., 2010.
Contribution of microbial activity to carbon chemistry in clouds. Appl. Environ.
Microbiol. 76 (1), 23e29.
Vali, G., Christensen, M., Fresh, R., Galyan, E., Maki, L., Schnell, R., 1976. Biogenic ice
nuclei. Part II: bacterial sources. J. Atmos. Sci. 33, 1565e1570.
Womack, A.M., Bohannan, B.J., Green, J.L., 2010. Biodiversity and biogeography of
the atmosphere. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 365 (1558), 3645e3653.
Yamaguchi, N., Park, J., Kodama, M., Ichijo, T., Baba, T., Nasu, M., 2014. Changes in the
airborne bacterial community in outdoor environments following Asian dust
events. Microbes Environ. 29 (1), 82e88.
Yooseph, S., Andrews-Pfannkoch, C., Tenney, A., McQuaid, J., Williamson, S.,
Thiagarajan, M., Brami, D., Zeigler-Allen, L., Hoffman, J., Goll, J.B., 2013.
A metagenomic framework for the study of airborne microbial communities.
PloS One 8 (12), e81862.
Zhao, Y., Aarnink, A.J., De Jong, M.C., Groot Koerkamp, P.W., 2014. Airborne micro-
organisms from livestock production systems and their relation to dust. Crit.
Rev. Environ. Sci. Technol. 44 (10), 1071e1128.