Environment International 113 (2018) 74–90

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Environment International
journal homepage: www.elsevier.com/locate/envint

Review article

A review on airborne microorganisms in particulate matters: Composition, T

characteristics and influence factors
⁎
Yunbo Zhaia,b, , Xue Lia,b, Tengfei Wanga,b, Bei Wanga,b, Caiting Lia,b, Guangming Zenga,b
a
College of Environmental Science and Engineering, Hunan University, Changsha 410082, PR China
b
Key Laboratory of Environmental Biology and Pollution Control, Hunan University, Ministry of Education, Changsha 410082, PR China

A R T I C L E I N F O A B S T R A C T

Handling Editor: R.J. Latcher Airborne microorganisms (AM), vital components of particulate matters (PM), are widespread in the atmo-
Keywords: sphere. Since some AM have pathogenicity, they can lead to a wide range of diseases in human and other
Airborne microorganisms organisms, meanwhile, some AM act as cloud condensation nuclei and ice nuclei which let them can affect the
Particulate matters climate. The inherent characteristics of AM play critical roles in many aspects which, in turn, can decide mi-
Microbial composition crobial traits. The uncertain factors bring various influences on AM, which make it difficult to elaborate effect
Atmospheric bacteria trends as whole. Because of the potential roles of AM in environment and potent effects of factors on AM,
Influence factors detailed knowledge of them is of primary significance. This review highlights the issues of composition and
characteristics of AM with size-distribution, species diversity, variation and so on, and summarizes the main
factors which affect airborne microbial features. This general information is a knowledge base for further
thorough researches of AM and relevant aspects. Besides, current knowledge gaps and new perspectives are
offered to roundly understand the impacts and application of AM in nature and human health.

1. Introduction molecular biological techniques (Adhikari et al., 2004; Hospodsky

et al., 2010; Katra et al., 2014; Kim et al., 2008; Lee et al., 2006), re-
AM are ubiquitous in the air, which mostly exist in the shape of searchers generally have studied airborne microbial main compositions
attaching on the PM while few of individual, and they gradually be- like bacteria, fungi, viruses and archaea with their concentration, size
come hot research objects with increasing studies on atmospheric PM distribution and diversity in order to know their peculiarities. Besides,
(Munir, 2010). As important parts of PM, AM were the vital role in AM have variability caused by themselves and other factors. Common
affecting human health, atmospheric chemistry, nucleation processes, influence factors contain meteorological parameters, particles, source,
and ecosystem interactions, they have biogeochemical connection with time, location, and human and animal activities (Dallavalle, 1958; Haas
oceanic, atmospheric, and terrestrial environments (Bauer et al., 2003; et al., 2013; Peccia et al., 2001; Yadav et al., 2015), and they have
Delort et al., 2010; Fröhlichnowoisky, 2016; Walser et al., 2015), so different effects on AM. Over the last decade, the studies in field about
comprehending the microbial contents in the air has important scien- influence factors exploration have increased gradually, but the concrete
tific, health, and economic significances. Nevertheless, many traits of effect mechanisms are not clear that still need to be researched. The
microbes, such as the actual identity, diversity, and abundance of dif- objective of this paper is to review knowledge about airborne microbial
ferent types as well as microbial temporal and spatial variability, are various characteristics and their influence factors. These aspects ac-
not well studied, therefore relevant researches about airborne microbial count for the manifold importance of the microorganisms in the at-
characteristics should be taken seriously from now. In most present mosphere, provide preconditions of subsequent researches about im-
researches about airborne microbial compositions and characters, the pacts and solutions of AM on other sides like health risk assessment and
starting point is microbial integral distribution, and the emphasis is allow insight in possible applications of these organisms.
microbial constitutions and features in whole environment, but mi-
croenvironment and small environment also have high research value 2. Composition of AM
which less be studied. Size-segregated environments own study
meaning because the most harmful effects of PM are related to the size Microorganisms are omnipresent in the atmospheric environment,
of the particles (Kim et al., 2015). From culture-based methods to which mainly include bacteria, fungi, actinomycetes, viruses, pollen,

⁎
Corresponding author at: College of Environmental Science and Engineering, Hunan University, Changsha 410082, PR China.
E-mail address: [email protected] (Y. Zhai).

https://doi.org/10.1016/j.envint.2018.01.007
Received 24 November 2017; Received in revised form 8 January 2018; Accepted 12 January 2018
0160-4120/ © 2018 Elsevier Ltd. All rights reserved.
Y. Zhai et al. Environment International 113 (2018) 74–90

Fig. 1. Main sources of airborne microbes over particles.

and a little archaea (Stetzenbach et al., 2004). The atmosphere is 2.1. Bacteria
considered as one of habitats for AM originated from soil, water/sea-
water, vegetation and else places (Fig. 1). Though atmosphere owns The study topics of AM are constantly increasing, which ranged
some hard conditions such as high solar radiation, low moisture and from exploring their existence and metabolic activity in atmosphere to
nutrients and large dispersing capability, it gradually evolved into one researching their potential pathogenicity and influence on climate and
of the habitats for microbes, there are still a large amount of microbes human health (D'Arcy et al., 2012; Polymenakou, 2012; Salonen et al.,
in the air now (Henderson and Salem, 2016). According to estimation, 2015; Šantl-Temkiv et al., 2015). Bacteria are common research objects
nature has about 40 thousand bacteria, 1.5 million fungi and 130 with the concentration ranging between 10 and 107 cell per·m3 in the
thousand virus, but actually the species, found and detected by current air detected by methods like culture methods, bio-molecular technology
research methods, are little (Hawksworth, 2001). Under various set- and quick estimation model (Albrecht et al., 2007; Bertolini et al., 2013;
tings, microbial compositions are distinguishing (Fig. 2), but the trends Bowers et al., 2012; Lange et al., 1997; Lee et al., 2010; Li et al., 2010;
of scale in microbes are the similar that generally detected bacteria are Liu et al., 2017b). Bacteria can exert a certain extent influence on many
the most about 80%, next are fungi, finally are others. These microbes aspects, like Gram-negative bacterial contamination relate to en-
can exist in the air mostly depend on PM which are primary carriers for dotoxins that can bring adverse effects, and some bacteria have infec-
AM, and the pattern AM existing on PM is adhesion, a way for AM to tion and toxicity may result in various microbial diseases of human and
establish community and sustain life in a particular habitat. Meanwhile, plants when higher concentration (Liang et al., 2013; Traversi et al.,
PM can offer AM nutrients to prevent starving conditions and maintain 2011), and some may impact cloud development and atmospheric
AM's metabolism with likely high nutrients on surface of PM when air chemistry (Andreae and Rosenfeld, 2008; Burrows et al., 2009). Hence,
settings around PM haven't enough nutrients, and PM also can provide bacterial characteristics are vital for AM studies to broaden the
the occupants with a shield as decreasing harm by ultraviolet radiation knowledge and deepen the cognition.
(Kharangate-Lad, 2015; Maier and Gentry, 2015). Compared with AM
on PM, the AM that exist as individuals may be more likely to die. AM 2.1.1. Size distribution
attaching to particles gradually form many abundant and mutable Different bacteria have respective sizes ranging from 0.1–5 μm, and
communities as numerous microbial species and different shares of each each bacterium has particular shape feature that plays an important
microbial constituent, which generate microbial diversity over PM role in the adhesion on PM (DeLeon-Rodriguez et al., 2013; Grinshpun
(Lighthart, 2000). The diversity and interaction among these microbes et al., 1995). With smaller size, bacteria are easier to attach to fine
will have an effect on themselves and external environment. Airborne particles like PM2.5 even smaller particles. Generally, particle size is an
microbial composition can provide rich information about themselves, essential factor that determines PM's inhalable degree which have a
like their portions, properties and characters, and comprehensive crucial effect on human health, so bacterial size distribution is a sig-
knowledge can help researchers lay a foundation for subsequent studies nificant content of researching health risk assessment exposure to air-
about AM. borne bacteria for human (Kawanaka et al., 2009). Hot research topics
are more put on small particles including ‘inhalable coarse particles’

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Fig. 2. Airborne microbial compositions under various settings, A) in three typical sites in Beijing, RCEES: Research Center for Eco-Environmental Sciences, XZM: Xizhimen, BBG: Beijing
Botanical Garden (Fang et al., 2008); B) in a hospital environment, RICU: Respiratory Intensive Care Unit, SICU: Surgical Intensive Care Unit, ER: Emergency Room, OPD: Outpatient
Department (Tong et al., 2017); C) in different particles (Cao et al., 2014); D): in food courts, indoor and outdoor (Rajasekar and Balasubramanian, 2011).

Fig. 3. The concentration and proportion of airborne bacteria in size-segregated particles, A) (Dybwad et al., 2014); B) (Li et al., 2015); C) RCEES: Research Center for Eco-Environmental
Sciences, XZM: Xizhimen, BBG: Beijing Botanical Garden (Fang et al., 2008).

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Y. Zhai et al. Environment International 113 (2018) 74–90

with a diameter of 2.5 to 10 μm and ‘fine particles’ which smaller than 2013; Uhrbrand et al., 2017). For these pathogenic bacteria, researchers
2.5 μm in diameter. Because coarse particles, aerodynamic diameter should devise effective ways to keep them within safe limits owing to
larger than 10 μm, will be captured by vibrissa and can't enter body their obvious harm to humans. These dominant species may belong to
inner, they are less harmful to health than the former (Frąk et al., 2014; different attributes which are divided into Gram-positive and Gram-
Kim et al., 2015). To research microbial size distribution, multi-stage negative. Among cultivable bacteria, the Gram-positive bacteria, gen-
sampler is used because it can more comprehensively, concretely and erally dominant bacteria isolated from bioaerosol, take up a great part
accurately embody this characteristic than single-stage. In researches of all detected genera in different studies (Amato et al., 2007;
which studied with Andersen six stage viable particle samplers, bac- Fröhlichnowoisky et al., 2011; Raisi et al., 2012). And the proportion of
terial size distribution mainly concentrated on aerodynamic diameters Gram-positive bacteria is about 80% (Table 2). On the contrary, in
from 1.1 to 2.1 μm and larger than 7.1 μm. The distinction of the two Fahlgren et al.'s (2010) research about coastal airborne bacteria, Gram-
depended on temperature in sampling stage, diameters were 1.1 to negative bacteria were more than Gram-positive in all samples, which
2.1 μm in warm, while another in cold (Raisi et al., 2012; Rajasekar and because the dominant sources were coastal airborne bacteria that
Balasubramanian, 2011). Actually under different environments, the containing more Gram-negative bacteria (Fahlgren et al., 2010). These
size-distribution patterns have some distinctions (Fig. 3). Bacteria de- proportions are not changeless, maybe changing with other parameters,
creased with decreasing particulate size partly since the study en- but overall these trends are basically constant (Kowalski et al., 2017).
vironments were breeding settings in which bacteria had better con- These results indicated that the bacterial composition of Gram-positive
ditions to grow and propagate (Zhao et al., 2011; Zheng et al., 2013). and Gram-negative were different between various sampling locations,
Studying with 8-stage Andersen samplers at poultry-feeding operations, and were influenced by bacteria origin, if bacterial origin mostly be-
authors indicated that size-related differences occurred in the aspect of longed to marine place, Gram-negative would occupy a fairly large
airborne bacterial abundance, diversity, and concentration, and those proportion. Bacterial species composition over PM is a vital part for
bacterial features varied with particle sizes could facilitate an under- researchers to discover the microorganism potential sources by prin-
standing of potential health risk of bacteria on human and poultry (Gao cipal component analysis and backward air mass trajectory analysis and
et al., 2017b). Meanwhile, different bacteria had respective variation other methods, and dominant species are the main research objects (Lee
tendency for particle sizes, although there were some differences on et al., 2007; Seifried et al., 2015). There are several important factors in
size distribution, bacteria mainly attached to particles with diameters a health risk assessment, one of which is the nature of the microbe
larger than 2.1 μm (Blais Lecours et al., 2012). Actually, like mentioned including microbial concentration and pathogenicity, so the study of
above, single bacterial cell size is smaller than particles, there are a dominant species can provide preliminary preparation and basis.
mass of nutrients and bacterial slime coat on the bacteria that make
bacterial size bigger but still are smaller than particles, so there were 2.1.3. Diversity
bacteria presenting in smaller size range between 0.65 and 1.1 μm Over PM, bacterial composition is complex with multiple genera
(Grinshpun et al., 1995; Lighthart, 1997; Raisi et al., 2012). In present and species, so in this microenvironment, AM forming many microbial
relevant researches, there are some errors caused by sampling methods communities show their diversity. Diversity generally is analyzed by
and microbial detection means, and the short of sufficient evidences is a traditional separation culture methods and molecular biological tech-
hinder to observe bacterial size distribution on tiny particles, so further nologies, the former is skillful but restrictive, and the latter is more
researches on airborne bacterial size distribution can use optimized precise like high-throughput sequencing (pyrosequencing analysis tar-
sampling and detection approaches. geting 16S rRNA sequences and metagenome sequences). There are
some indexes can illustrate microbial diversity features. α-Diversity
2.1.2. Dominant species index, calculated by the kinds of species and abundance, is a significant
On PM, bacteria have different dominant species in various en- gist to evaluate microorganism community level. This index mainly
vironments. Atmosphere habitat is considered as an extreme environ- includes community diversity (Shannon and Simpson), community
ment, but AM can live well in the air with nutrients supported by cloud, richness (Chao and ACE), npShannon and Good's Coverage. Larger
rainwater and particles (Womack et al., 2010). Although atmosphere Shannon index values indicate the richer species in the environment
provides survival conditions for AM, due to microbial different intrinsic and the more evenly distributed the species, larger Simpson index in-
properties, different microbes can adapt themselves to one certain en- dicates that the higher the species diversity of the sample, the more
vironment better and develop into preponderant species in disparate evenly distributed among the various individuals and vice versa, and
atmospheric settings. Therefore, dominant species of bacteria is a worth larger Chao values represent more species contained in the sample. β-
research content which is effective in providing more insight into the Diversity describes the relationship between microorganisms and en-
dominant species with their features and exploring biodiversity of the vironmental factors. The both indexes are important microorganism
atmosphere. According to researches about airborne bacteria under parameters reflecting microbial community with their diversity. Gao
diverse environments, researchers can find that bacterial communities et al. (2016a) reported six PM2.5 clone libraries with average index
have respective characteristics. It is reported that bacteria exposure values of Shannon, Simpson, Chao 1, ACE and Good's Coverage re-
level mainly has correlation with various factors like human oral cavity, spectively. In this study, Simpson indexes value reflected the samples
human skin indoors, and wind, temperature, relative humidity (RH) had high evenness, while other data showed low richness (Gao et al.,
alfresco, so bacterial composition has a close correlation with one 2016a). Genitsaris et al. (2017) had a study of atmospheric bacterial
concrete environment. Streptophyta, Bacillus, Corynebacteria, Pseudo- variability in an urban area, and reported that the values of the Simpson
monas, Acinetobacter and so on often were detected in retail stores index ranged between 0.81 and 0.95 except one sample, and the
(Hoisington et al., 2016), and Sphingomonas, Staphylococcus, Bacillus Shannon index showed similar patterns with the Simpson index
were common bacteria in residences (Adams et al., 2014), in office (Genitsaris et al., 2017). This result indicated that the majority of the
buildings, Micrococcus, Staphylococcus became dominant (Bonetta et al., samples manifested relative homogeneity in the field of the sequences
2010), while in underground subway station, wastewater treatment number. Fahlgren et al. (2010) collected 8 samples, the Shannon index
plant (WWTP), suburban, hospital, coastal region, city and so on, the of them were from 1.2 to 3.9 in different sampling time, the data
dominant bacterial species had fine distinctions (Table 1). In addition, showed a high abundance and diversity in most samples (Fahlgren
pathogenic bacteria sometimes were also found on particles, such as et al., 2010; Straat et al., 1977). The abundance of AM varied in a
Enterococcus casseliflavus in a hospital WWTP and Proteus sp., Proteus degree with many factors including sampling time and site et al., and
mirabilis, Escherichia coli, Enterobacter aerogenes, Providencia alcalifaciens these indexes effectively represented the situation of diversity for bac-
and Morganella sp. commonly were detected in researches (Han et al., terial community on particles under different conditions. The diversity

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Table 1
Different dominant bacterial genera in different study environments.

Dominant bacterial genera Total amount of Detected method Study environment Reference
genera

Streptophyta, Bacillus, Corynebacterium, Pseudomonas, 788 Pyrosequencing Retail stores (United States) (Hoisington et al., 2016)
Acinetobacter
Bacillus, Kocuria, Staphylococcus, Sarina, Pseudomonas 16 cb Agricultural industry (Awad et al., 2010)
Sphingomonas, Pseudomonas, Chryseobacterium, Sejongia 30 cb and ci Vicinity of the Baltic Sea (Fahlgren et al., 2010)
coast
Vibrio, Bacillus, Pseudoalteromonas, Psychrobacter, 31 16S Coastal near-shore (Dueker et al., 2012)
Salinibacterium
Staphylococcus, Pseudomonas, Alcaligens, Corynebacterium 9 cb Food courts (Rajasekar and Balasubramanian,
2011)
Micrococcus, Staphylococcus nd cb Office building (Bonetta et al., 2010)
Staphylococcus, Bacillus 11 cb Wastewater treatment plant (Kowalski et al., 2017)
Bacillus, Micrococcus, Staphylococcus 37 cb and partial 16S Underground subway station (Dybwad et al., 2012)
Pseudomonas, Bacillus 106 DGGE Suburban (Toyama) (Tanaka et al., 2014)
Streptomyces, Bacillus, Kocuria, Corynebacterium, 26 cb Urban (Ahvaz) (Goudarzi et al., 2014)
Paenibacillus.
Micrococcus, Staphylococcus, Kocuria, Pseudomonas 55 16S Urban (Hangzhou) (Fang et al., 2016)
Afipia, Oxalobacteraceae, Methylobacterium 314 SSU Upper troposphere (DeLeon-Rodriguez et al., 2013)
Staphylococcus, Micrococcus, Corynebacterium, Bacillus 10 cb Hospital (Kiyoun et al., 2010)
Micrococcus, Staphylococcus, Bacillus, Corynebacterium, 47 cb Slaughtering plant (Liang et al., 2013)
Pseudomonas
Sphingomonas nd 16S Ocean (Seifried et al., 2015)
Staphylococcus, Micrococcus, Pseudomonas, Proteus 11 cb Poultry farms (Plewa and Lonc, 2011)
Bacillus 11 16S Free troposphere (Maki et al., 2013)

nd: no data.
cb: culture-based.
ci: culture-independent.
16S: 16S rRNA sequencing.
SSU: SSU rRNA gene sequencing.
DGGE: denaturing gradient gel electrophoresis.

Table 2 bacterial concentration diurnal variation in a great degree is shaped

Proportion of Gram-positive and Gram-negative bacteria (%). with multiplicate conditions such as sunrise, wind speed (WS), tem-
perature, solar radiation and increasing of human activities. In addition
Gram-positive bacteria Gram-negative bacteria Reference
to bacterial concentration, the size distributions also vary during a day
79 21 (Awad et al., 2010) and the temporal variation of bacteria would help to fully understand
89 11 (Goudarzi et al., 2014) the possible harm at different times. Dybwad et al. (2014) researched
80–85 15–20 (Liang et al., 2013) temporal variability of airborne bacteria at a subway station, they ob-
82 18 (Gangamma, 2014)
68 32 (Orsini et al., 2002)
served a significantly larger fraction bacterium-containing particles
between 1.1 and 3.3 μm during the daytime than night, while a sig-
nificantly greater fraction of particles of > 3.3 μm was observed at
can reflect the state of the bacteria and their relationship to the en- night than during the day. These results indicated that bacterium-con-
vironment, and microbial resources developments, ecosystem func- taining particles' diameter had an obvious diurnal variation (Dybwad
tioning, global change and human health are all closely related to mi- et al., 2014). In addition, both on non-haze and haze days, aerodynamic
crobial diversity, so microbial diversity are significant for relevant diameter of AM fluctuated from 9:00 to 21:00 h, and changeless highest
studies. To understand the diversity fully, more researches have to be concentrations of airborne bacteria were observed at size ranges of
conducted. 3.3–4.5 μm at 12:00 and 21:00 h (Gao et al., 2015). Meanwhile, bac-
terial diversity showed day-to-day variation, and dominant bacteria
2.1.4. Variation changed from daytime to nighttime. The author adopted two methods
Bacterial concentration, diversity, size distribution and pre- to analyze the diurnal variation of dominant bacteria, the results
dominant species will change following temporal and spatial variation. showed that the Andersen-derived and the SASS 3100-derived daytime
Temporal change mainly include daily shift and seasonal shift, while diversity was dominated by Micrococcus, while the nighttime diversity
spatial change generally refer to exploring microbial source and dif- was dominated by Rhodococcus, just the followed bacteria had few
ferent characteristics of AM in distinguishing regions. In most cases, differences (Dybwad et al., 2014).
microbial abundance change diurnally, the maximum concentrations Annual variation in diversity, type, ration and composition of air-
normally appear on 7:00–9:00 h and 17:00–18:00 h, and the minimum borne bacteria in the same area has a regular pattern. Selecting these
on 13:00–14:00 h in daylight, and bacterial level increase during the bacterial features for longitudinal comparison in the same site, re-
daytime compared with the nighttime. Tong (1999) detected both total searchers find bacterial characteristics in the same season do not show
and cultivable airborne bacteria reached the concentration peak at significant change, and this is owing to bacterial seasonal stability,
18:00 h (Tong, 1999). Fang et al. (2007) reported that significantly while in different sampling sites there are diverse distributions. Overall,
higher bacterial concentrations were recorded at 09:00 h and 17:00 h bacterial characteristics, especially richness and the relative abun-
than those at 13:00 h because of heavy human activities and traffic flow dance, exhibit significant seasonality patterns. Concentration distribu-
appearing in the two periods (Fang et al., 2007). In the livestock farm, tions in a year weren't uniform, considering temperature, region, ter-
due to closed environment and animals' influences, the diurnal varia- rain and bacterial autologous characters multi-factors, high
tion of bacteria was complex, and the concentration peaks of bacteria concentrations were found in winter (Alghamdi et al., 2014; Fahlgren
on working days and weekends were different (Fig. 4). In conclusion, et al., 2010), in summer (Fang et al., 2007; Wang et al., 2010),in

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Fig. 4. Diurnal variations of airborne bacteria concentra-

tions, A) (Zheng et al., 2013); B) (Abdel Hameed et al.,
2009).

autumn (Fang et al., 2016; Kaarakainen et al., 2008). Tanaka et al. but as many studies reported about microorganisms consisting in at-
(2014) didn't find significant seasonal changes in the concentration of mosphere, fungi generally just accounted for a fraction of all microbes.
airborne bacteria (Tanaka et al., 2014), and that showed bacterial in- Compared with bacteria, fungal allergen is one of the predominant al-
determinacy and variability under different researches. In addition to lergens, and fungi exposure has been more closely linked to allergic
integral concentration variation, the dominant bacteria similarly owned sensitization and symptoms of allergy and asthma (Medicine, 2000;
temporal variation, like Actinobacteridae reached maximum abundance Medicine, 2004; Swanson, 2001). Due to the pathogenicity of fungi and
in the late summer while Pseudomonadales reached their highest levels the airborne effects, researches about airborne fungi should get a
during mid-spring (Bowers et al., 2013). As the report illustrated, in comprehensive cognition of them, so that corresponding prevention
warm seasons, predominant microorganisms generally were retrieved and protection steps can be took.
in soil, while typically associated with plants in cold seasons (Gandolfi
et al., 2015). The results also indicated that bacterial communities
seemed mostly related to environmental conditions, in which season 2.2.1. Size distribution
was the significant factor. Potential sources' relative contribution on Fungal concentration and size distribution vary with sampling sites
bacterial community has a temporal variability, so bacterial commu- as bacterial. The fungal concentration is 0–107 CFU·m−3 with different
nities variance correlates to temporal transition and potential sources, sizes (Sautour et al., 2009; Yu et al., 2013). Airborne fungi have in-
especially those located close to sampling sites (Bertolini et al., 2013; equable sizes. Some large hyphal fragments and multicellular spores
Gandolfi et al., 2015). are > 10 μm in size, unicellular spores' diameters are between 1 and
Bacterial sources' spatial distributions make bacterial communities 10 μm and parts < 1 μm, and that shows airborne fungi have a broad
own respective spatial variation characteristics. Under the same season, size distribution. Size is an important parameter that decides the
different sites have their own unique bacterial communities, and local taxonomic compositions of airborne fungi and influence inherent di-
sources and atmospheric dispersal are involved in the assembling of the versity of fungi, and in all aspects fungal size distribution manifests
communities. In present researches, a Geographic Information System fungal significance (Yamamoto et al., 2012). Overall, size of fungal
is usually used to analyze the spatial distribution of bacteria, and particle generally is bigger than bacterial particle, and fungi are found
backward trajectories are used to find the sources of bacteria (Agabou occurring on the fine particles (< 3.3 μm) in the conventionally with
et al., 2013; Seifried et al., 2015), and these technologies supply more the maximum proportion and minimum proportion in the range of
information about bacterial temporal and spatial variation. Temporal 2.1–3.3 μm and 0.65–1.1 μm, respectively, while in the most areas the
and spatial variability of bacterial communities are important contents size distribution represent a unimodal distribution pattern (Yu et al.,
for scholars to gain insight into atmospheric biodiversity and biogeo- 2013). Similar results showed by Fig. 5, with other articles discovered
graphy. fungal particles being mainly distributed at 3.0–6.0 μm, 2.0–3.5 μm and
1.0–2.0 μm (Rajasekar and Balasubramanian, 2011), at 1.1–2.1 μm and
2.1–3.3 μm (Zuraimi et al., 2009), and at 2.1–3.3 μm and < 4.7 μm
2.2. Fungi (Dueker et al., 2012; Xu et al., 2011). On different size-segregated PM,
Lee and Liao (2014) researched the fungi size distribution in three size
Fungi are estimated to the most microbes contained in nature, and fractions: < 1 μm, 1–1.8 μm, and > 1.8 μm in agricultural farms and
airborne fungal spore are primary biogenic aerosol particles (PBAP), found that the median concentrations of cultivable fungi measured for

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Y. Zhai et al. Environment International 113 (2018) 74–90

Fig. 5. Average size distribution of fungi, A) a. terrestrial fungi, b. marine fungi (Li et al., 2011); B) indoor and outdoor airborne fungi (Rajasekar and Balasubramanian, 2011); C) fungi in
haze days and non-haze days (Li et al., 2015).

the size > 1.8 μm were higher than those for the sizes of 1–1.8 μm shown to be associated with asthma development, so exploring fungal
and < 1 μm (Lee and Liao, 2014). Sangkham and Sakunkoo (2014) got diversity can pave the way for subsequent researches about fungal in-
the results that the size distribution of airborne fungi were 1.1–2.1 fluence on human health. Besides dominant species researches, ana-
(19.99%), > 7 (19.86%), 4.7–7.0 (15.75%), 3.3–4.7 (15.70%), 2.1–3.3 lyzing fungal Shannon diversity index is also one of the study methods
(15.65%), and 0.65–1.1 (13.00%) μm, respectively (Sangkham and to research fungal diversity. In swine houses, Shannon index were about
Sakunkoo, 2014). These data indicated that fungi were usually found in 4.5–6.0 and 5.5–6.0 in summer and winter, respectively, the results
small one which size were about > 1 μm. Of course, fungal size dis- illustrated that the airborne had a high fungal diversity and winter was
tribution weren't invariable, the size distribution pattern of the samples more conducive to the formation of high diversity than summer
might be influenced by factors such as sources, seasons, weather si- (Kumari et al., 2016). Yan et al. (2016) showed that fungi in TSP and
tuations, sampling sites and so on, like fine fraction and coarse fraction PM10 samples had higher Chao1-values than PM2.5 which were 169.8,
showed an increase on hazy and foggy days, respectively (Dong et al., 167.43 and 94.17, respectively, this result indicated higher richness in
2016; Rajasekar and Balasubramanian, 2011). Fungal size distribution TSP and PM10 samples; Shannon index in TSP, PM10 and PM2.5 samples
is closely correlative with fungal health threat because aerodynamic were low with 1.905, 2.215 and 2.213 respectively, and a higher value
diameter is one of the master variables which determine microbial of Shannon index in heavy-haze days indicated a higher diversity than
personal exposures, it can be said that the smaller size is, the greater non-haze and light-haze days though there was no significant difference
danger is brought, so research fungal size distribution to evaluate the (p > 0.05) (Yan et al., 2016). In tropical deciduous forest, the Shannon
health risk degree. But in previous studies, size-segregated researches of index was 3.1 and 3.6 that showed high diversity (Satish et al., 2007).
fungi are insufficient, and detected methods also need to be improved The Shannon index, Shannon evenness, and Simpson's index values of
to get more accurate and abundant data. airborne fungi were similar to the fungal samples which were obtained
from soil and plants, and the result indicated fungi also owned a high
diversity in the air (Fröhlichnowoisky et al., 2009). Because many fungi
2.2.2. Diversity can't be cultured on media, using culture-dependent methods to explore
Fungal species diversity is a primary influence factor for health risk fungal diversity ineluctably would underestimate the data and produce
exposure, because fungal pathogen and allergen are ubiquitous in the great errors. However, detected by sequencing, over 86% of genera
air, clearly knowing that fungal composition can better make a health were new-found compared with culture-based methods (Pashley et al.,
risk assessment. One of the important contents of fungal composition is 2012). Tong et al. (2017) combined a culture-based method and DNA
dominant species. Cladosporium, Aspergillus and Penicillium have the sequencing analysis with the Illumina MiSeq and HiSeq 2000 sequen-
highest frequencies in relevant reports (Bezerra et al., 2014; Kumari cing systems to find high diversity of fungi in hospital, and reported
et al., 2016; Pyrri and Kapsanaki-Gotsi, 2011; Sepahvand et al., 2013; Aspergillus was the highest at species level (Tong et al., 2017). These
Sharma, 2011) (Table 3). These common genera own different degrees showed that culture-independent methods were optimal ways with
of pathogenicity and anaphylaxis, and fungal diversity have been

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Y. Zhai et al. Environment International 113 (2018) 74–90

their high efficiency. Investigation of the diversity about airborne fungi

(Rajasekar and Balasubramanian, 2011)

can provide reliable results for microbial infection control and sur-

(Bogomolova and Kirtsideli, 2009)

veillance, whilst more accurate information can make it easier for re-
searchers to develop a better solution proposal.

(Sepahvand et al., 2013)

(Yamamoto et al., 2012)
2.2.3. Variation

(Zuraimi et al., 2009)

(Pashley et al., 2012)

(Shelton et al., 2002)

(Kumari et al., 2016)

(Lee and Liao, 2014)
(Begum et al., 2011)

(Niazi et al., 2015)

(Chao et al., 2002)

Existence of fungi in the air is affected by a mass of factors, there-

(Yan et al., 2016)

(Ezikanyi, 2016)
fore, fungi vary with these influences, which are reflected in temporal
and spatial variation. Fröhlichnowoisky et al. (2011) illustrated bio-
Reference

geography in the air through analyzing fungal diversity over land and
oceans, they compared each sampling method at several locations
around the world, like Austria, Arizona, Brazil, China, Germany, Puerto
Rico, United kingdom, Ocean, and found estimates of the total species
Buildings and outdoor environments (United States)

richness of fungi ranging from about 135 to 1100 with the Chao1 es-
timator approach (Fröhlichnowoisky et al., 2011). In different regions,
Urban setting (northeastern United States)

as the difference of sources, meteorological conditions, land-use types

and anthropogenic activities, diversity of fungi are distinguishing, and
this difference reflects the spatial variation of fungi (Núñez et al.,
2016). One thing to emphasize is that land environment may be rich in
Wastewater treatment plant

fungi, which different from marine environment with rich bacteria.

Federal Capital Territory

Besides, fungal concentration, size distribution and relative abundance

Large office buildings

Underground stations

change with time, and the fungal abundance peaked in early spring,
Study environment

Agricultural farms
Campus and town

Child care centers

summer, late autumn basing on different conditions (Bowers et al.,

Swine houses

2013; Liao et al., 2004; Oliveira et al., 2005; Yamamoto et al., 2012). In
Food courts

addition, fungal concentration also varies in a day (Fig. 6). Different

Hospital

Campus
campus

fungal species had diverse diurnal distributions, like Aspergillus showed

double peak patterns at 10:00 h and 20:00 h, Penicillium and Clados-
porium's concentration peaks appeared at 20:00 h (Lin and Li, 2000),
qPCR and Illumina HiSeq sequencing

and the highest concentration of Penicillium/Aspergillus spores appeared

at 10:00 h (Gillum and Levetin, 2007). Besides, fungal size distributions
qPCR plus 454 pyrosequencing

were different in different seasons and sites, like that fungal sizes were
Illumina MiSeq Sequencing

higher in winter than summer in outdoor, while it was adverse in in-

Sequencing techniques

door (Liao et al., 2004). During heavy haze days and non-haze days, the
Photomicrographs

mean percentages of fine particles carrying cultivable airborne fungi

Detected method

were different in different seasons (Gao et al., 2015). High diversity and
cb and PCA

concentration of fungi and potentially high levels of fungal allergens

occurred in springtime (Oh et al., 2014), in summer (Chao et al., 2002),
cb

cb
cb

cb

cb
cb
cb

cb

in fall (Shelton et al., 2002) and in winter (Begum et al., 2011). Above
all, time and space are significant factors influence on fungal char-
Total amount of genera

acteristics, hence, researching fungal features needs combining time

and space, which can make researchers better understand fungal in-
trinsic traits.

2.3. Other microbes

588

368
nd
28
16
44
10

20

29
25
30
11
18

72

The proportion of viruses and archaea in the detected results are at

most 10% and at least 1% in total AM with low concentrations, but
Cladosporium, Alternaria, Fusarium, Penicillium, Sporisorium, Aspergilus
Ascomycota, Basidiomycota, Schizophyllum, Cryptococcus, Epicoccum

some of them own strong pathogenicity, which can generate bad in-
Different dominant fungal genera in different study environments.

Nonsporulating fungi, Penicillium, Cladosporium, Yeast, Aspergillus

fluence on plants, livestock and even human through their low con-
centrations, so their existences should not be ignored.
Cladosporium, Penicillium, Aspergillus, nonsporulating fungi

Penicillium, Cladosporium, Alternaria, Mucor, Ulocladium

Erysiphe graminis, Hansfordiella, Puccinia, Sporidesmium

2.3.1. Virus
Aspergillus, Candida, Penicillium, Rhizopus, Fusarium

Acremonium, Aspergillus, Cladosporium, Penicillium

Penicillium, Aspergillus, Geotrichum, Cladosporium

Viral features, infectivity and survivability are effected by particle

Penicillium, Cladosporium, Aspergillus, Fusarium,

size, and virus distribution is represented by the particle volume dis-

Fusarium, Clavaria, Rhodotorula, Mortierella

Cladosporium, Ustilago, Peniophora, Kavinia

tribution rather than the particle number distribution, therefore, in-

vestigating viral composition, concentration and other information over
Penicillium, Aspergillus, Cladosporium

Aspergillus, Penicillium, Cladosporium

PCA: principal component analysis.

particles is useful (Zuo et al., 2013). For viral perniciousness and in-
qPCR: quantitative real-time PCR.

fection, more researchers have paid attention to airborne virus' in-

vestigations. Particle size can determine physical stability of aerosols,
Dominant fungal genera

the sites of deposition and the degree of retention, and size of viral
aerosols is an immense significance because they may cause human
cb: culture-based.

virus infections and affect viral personal size, survivability, patho-

Alternaria

genicity rate and even meteorological conditions (Hogan et al., 2005;

nd: no data.

Sorrell et al., 2011). Small doses of respiratory viruses given by small

Table 3

particle aerosol were infective, and airborne viruses' transmission was

most consistent with transmission of small particle aerosol, and these

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Y. Zhai et al. Environment International 113 (2018) 74–90

Fig. 6. Diurnal variations of airborne fungi con-

centrations, A) (Liao et al., 2004); B) (Burch and
Levetin, 2002).

Table 4 containing particles ranged from 0.5 to 2 μm with the peak at around
Distribution by particle size of the quantity [geometric mean of RNA copies·m−3 (geo- 1.1 μm, but the research objects most were inactivating viral strains in
metric standard deviation)] of influenza (IAV), porcine reproductive and respiratory airborne (Agranovski et al., 2007; Pyankov et al., 2012). Sometimes the
syndrome (PRRSV) and porcine epidemic diarrhea (PEDV) viruses in air samples (Alonso
et al., 2015).
virus was evenly distributed in particles with different sizes, in some
cases, it was found predominantly in the smallest and largest, or just the
Particle size IAV PRRSV PEDV largest size fractions (Table 4). Zuo et al. (2013) researched four animal
range (μm) viruses' infectivity and survivability with its carrier particle size, and
0.4–0.7 8 × 102 (3.2)a 6 × 102 (4.1)a 1.3 × 106 (3.4)a
found that whether infectious virus or total virus were increased with
0.7–1.1 6.1 × 102 (1.7)a † ≤ 5.1 × 102 (1)a 3 × 105 (4.7)a carried particle size increasing (Zuo et al., 2013). These results testified
1.1–2.1 5.5 × 102 (2.5)a † ≤ 3.6 × 102 (1)a 1.6 × 106 (2.4)a that virus-laden particle size was one of the factors influencing viral
2.1–3.3 1.4 × 103 (4)a,b 7.8 × 102 (4.82)a 5.2 × 105 properties and the virus distribution was found to be represented by the
(3.3)a,b
particle volume distribution. Viruses distribute in different particle size
3.3–4.7 7.8 × 103 (5.1)b,c 1.8 × 103 4.5 × 107 (1.8)c
(1.26 × 101)a and change in different conditions, and these changes also include viral
4.7–5.8 2.3 × 104 (7.4)c 1.7 × 103 (4.8)a 5.5 × 107 seasonal variation. Different viruses have disparate outbreak time,
(2.2)c,d some concentrate on summer while others on winter or other time.
5.8–9.0 1.5 × 104 (6)c 1.1 × 102 (7)a 3.1 × 107 (2)b,c These viral concentration, activity and negative/positive own diverse
> 9.0 4.3 × 105 5.1 × 104 3.5 × 108
distribution with seasons. Boone and Gerba (2005) detected influenza
(1.25 × 101)d (2.8 × 101)b (2.9)d
viruses with 23 and 53% of the samples during autumn and spring,
a,b,c,d
Different superscripts between rows of the same column indicate statistically sig- respectively (Boone and Gerba, 2005). Masclaux et al. (2014) detected
nificant differences (Tukey's test, p < 0.05). airborne human adenovirus in WWTP and found that positive samples,
† LOD: Limit of q-PCR detection. exceeding the limit quantification (i.e. 2.72 × 103 genome equivalent
copies·m−3), were more in summer than in winter, and the mean
evidenced that particle size played a vital role in viral spread and in- concentration of airborne adenovirus was higher in summer than in
fection, especially small size (Knight, 1970). Scott and Sydiskis (1976) winter, but two other viruses, norovirus and hepatitis E virus, scarcely
reported airborne influenza virus had a high infectivity in small particle appeared (Masclaux et al., 2014). Although virus has a great harm to
size (2 μm) than the larger-sized particles (10 μm) (Scott and Sydiskis, humans, current understandings of virus aren't deeply enough. To get a
1976). Yang et al. (2011) sampled virus in different sites and analyzed better comprehension of airborne viral characteristics and to take pre-
them with quantitative reverse transcriptase-polymerase chain reaction ventive measures for viral harm, relevant researches about viral char-
(qRT-PCR), the results showed the amounts of total virus found in each acters can be conducted step by step.
size fraction were 36, 28, 11, 10 and 15% on size which bigger than 2.5,
1.0–2.5, 0.5–1.0, 0.25–0.5 and < 0.25 μm, respectively, and 64% of the
viral genome copies were associated with fine particles smaller than 2.3.2. Archaea
2.5 μm as mentioned above (Yang et al., 2011). The majority of virus- Archaea, accounting for up to about 10% of the prokaryotes, have
been thought to live in extreme environments, actually they have also

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Y. Zhai et al. Environment International 113 (2018) 74–90

Table 5
Contribution of spores and the results of Spearman's rank correlation test between hourly and daily concentrations of fungal spores and meteorological parameters (Grinn-Gofroń et al.,
2017).

Taxon Seasonal contribution T RH WS Precipitation

Count % Hourly Daily Hourly Daily Hourly Daily Hourly Daily

⁎ ⁎ ⁎
Agrocybe 28 0.005 0.005 0.071 0.063 0.165 0.029 −0.224 −0.024 −0.080
Alternaria 8648 1.586 0.359⁎ 0.480⁎ −0.100⁎ −0.093 0.091⁎ −0.152 −0.078⁎ −0.200⁎
Chaetomium 108 0.020 0.049⁎ 0.215⁎ 0.085⁎ 0.152 −0.026 −0.288⁎ −0.030 −0.048
Cladosporium 346,135 63,493 0.511⁎ 0.601⁎ −0.075⁎ −0.072 0.121⁎ −0.152 −0.070⁎ −0.084
Coprinus 22 0.004 0.006 0.069 −0.013 −0.066 −0.012 −0.026 0.018 0.068
Curvularia 19 0.003 −0.009 −0.020 0.047⁎ 0.262⁎ 0.008 −0.123 0.041⁎ 0.166⁎
Didymella 175,316 32,159 0.069⁎ 0.268⁎ 0.057⁎ −0.012 0.025 −0.072 0.002 0.051
Drechslera type 856 0.157 0.218⁎ 0.525⁎ −0.099⁎ −0.172⁎ 0.022 −0.066 −0.021 −0.106
Epicoccum 1413 0.260 0.162⁎ 0.169⁎ −0.077⁎ −0.038 0.033⁎ −0.205⁎ −0.042⁎ −0.112
Fusarium 30 0.006 −0.083⁎ 0.046 0.181⁎ 0.294⁎ 0.064⁎ −0.081 0.094⁎ 0.205⁎
Ganoderma 3586 0.658 0.179⁎ 0.529⁎ 0.183⁎ −0.086 −0.032 −0.325⁎ −0.027 −0.201⁎
Leptosphaeria type 7112 1.305 0.110⁎ 0.138 0.198⁎ 0.130 −0.026 0.125 −0.025 0.416⁎
Periconia 28 0.005 0.086⁎ 0.182⁎ −0.057⁎ −0.035 0.047⁎ 0.014 −0.027 0.010
Phaeosphaeria 448 0.082 0.052⁎ 0.082 0.164⁎ 0.248⁎ 0.005 −0.179 0.035⁎ 0.205⁎
Pithomyces 76 0.014 0.074⁎ 0.139 −0.026 −0.037 0.025 −0.078 −0.019 0.006
Pleospora 715 0.131 0.083⁎ 0.217⁎ −0.011 0.183⁎ 0.044⁎ −0.065 0.001 0.164⁎
Polythrincium 31 0.006 0.119⁎ 0.398⁎ −0.066⁎ −0.146 0.037⁎ −0.117 −0.040⁎ −0.185⁎
Stachybotrys 11 0.001 −0.052⁎ −0.215⁎ 0.020 0.138 −0.014 −0.056 0.022 0.025
Stemphylium 77 0.014 −0.037⁎ −0.095 0.011 −0.013 0.019 −0.015 0.019 0.300⁎
Tilletia 33 0.006 0.107⁎ 0.321⁎ −0.066⁎ −0.350⁎ −0.031 −0.017 0.002 −0.210⁎
Torula 463 0.085 0.098⁎ 0.301⁎ −0.083⁎ −0.400⁎ −0.016 0.031 −0.029 −0.194⁎

⁎
p < 0.05.

been found in the atmospheric environment with low number. In the air, microorganisms have already attracted researchers' at-
Generally, archaea have one main source - soil, but there also are other tention with their self-characteristics, and their influences on nature
habitats like freshwater, freshwater sediment, estuarine sediment, and human. Combining with PM, the microbial concentration, size
marine water, marine sediment, geothermal system, and symbiosis distribution, dominant species, diversity, temporal and spatial variation
(Fröhlichnowoisky et al., 2014). At present, abundance, diversity and are point-cuts, through which researchers can have a more particular
dispersal of archaea are ill-informed in the atmosphere. However, they knowledge of AM and clearly know the relations between PM and AM.
have research meaning in every sense, it is a remarkable thing that
research their abundance and critical function in diverse natural en- 3. Influence factors
vironments, and that explore their quintessential role in shaping the
evolutionary path of life on Earth and their pivotal role in the ni- 3.1. Meteorological parameters
trification process (Cao et al., 2013; Cavicchioli, 2010).
Fröhlichnowoisky et al. (2014) made a discussion of diversity and Microorganisms are not invariant in the air, and kinds of their
seasonal dynamics of airborne archaea, they detected 435 archaea features will change with many factors, to some extent, these factors
species that grouped into 57 OTUs with the 16S rRNA gene. In addition, decide microbial characteristics. Microorganisms live in the air with
amoA gene was used to study diversity of archaea (Fröhlichnowoisky influence of meteorological parameters, these meteorological para-
et al., 2014). Euryarchaeota and Thaumarchaeota were dominant, and meters have the most significant effect on AM, and multitudinous fac-
Thaumarchaeota accounted for over four fifth which were widespread tors affect various species with different responses. To some degree,
on Earth and detected in various environments (Pester et al., 2011). In meteorological parameters lead the microbial communities and char-
different cities and sampling sites, the result of metagenomic reads of acteristics. Weather conditions have an impact on the production, re-
archaea were different, which showed archaea have special distribution lease, dispersion and deposition of microbes, as well as influence the
and that the species composition was concerned with the airborne diversity and number of airborne bio-particles (Li et al., 2017; Şakiyan
sources (Yooseph et al., 2013). Besides, archaea mostly appeared in all and Inceoǧlu, 2003). The structures of airborne bacteria can show
coarse samples (> 3 μm), only about one fifth in fine (< 3 μm), exactly, considerable temporal variability, and these shifts were likely to be
archaea were more susceptible to attach to coarse particles like soil dust driven by changes in meteorological conditions (Bertolini et al., 2013;
particles (Jones and Harrison, 2004). Archaea inherent characteristics Lighthart, 1997; Polymenakou and Mandalakis, 2013). In many studies,
can be influenced by factors like RH, WS and temperature, and these functional relationships between AM and meteorological factors were
factors cause archaea change with temporal variation, such as archaea analyzed, and these factors generally include temperature, RH, WS,
species show various diversities in different seasons. Meanwhile, local precipitation, solar radiation, air pressure (AP) and so on (Table 5).
environment is also a variable, the abundance and distribution of ar-
chaea in coastal environment owned special physiological types that
3.1.1. Temperature
little were described (DeLong, 1992). Generally, the archaea species
Temperature is assuredly the most important part of the meteor-
richness has multiple linear correlations with these meteorological
ological parameters, because the span of temperature is so great in the
conditions. As on a long-term monthly basis, the normalized species
earth and microbes have different distribution with their optimal living
richness negatively correlated with both temperature and WS, while the
temperatures. For the influence mechanism of temperature on AM, re-
relative species richness showed a significant positive correlation with
searchers still haven't a much clear cognition, but through relevant
RH and WS. WS was found as the significant factors (negative corre-
articles, there is a preliminary comprehension. The effects generally
lation), although it played a secondary role in both cases. In different
include two main parts: i) directly, on microbes themselves, ii) in-
conditions, disparate combination of factors will exert unlike influence
directly, on other parameters. The former refers to that temperature
on archaea distribution, composition and diversity.
promotes or restrains microbial release and growth, while the latter

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Y. Zhai et al. Environment International 113 (2018) 74–90

says that temperature influences other parameters like cross-ventilation as mentioned above, microbes entranced into the atmosphere de-
which decides the suspension and diffusion of microbes. Hoeksma et al. pending on attaching on the dust and particles, thus decreasing dust
(2015) studied the effects of temperature on E. coli, M. synoviae and E. reduced microbial suspension (Sousa et al., 2008). Besides, high RH will
mundtii by observing bacterial decay and showed that temperature as- augment the probability of deposition because suspended particles
suredly had influence on bacteria (Hoeksma et al., 2015). In many re- absorb ambient moisture leading increasing particle weight and size
ports, temperature was thought having a significant positive correlation (Zhen et al., 2017). These reasons may illuminate why the majority of
with bacteria and fungi, and high temperature was the optimal condi- microbes are existing in the air at low RH.
tion for fungal spores, while low temperature was a limiting factor for
fungal development (Almaguer et al., 2014; Quintero et al., 2009; 3.1.3. WS
Rivera-Mariani and Bolaños-Rosero, 2012; Smets et al., 2016). None- As an important parameter of meteorological parameters, WS plays
theless, there was a viewpoint that cold air may facilitate the release an indispensable role in affecting ambient microbial characteristics.
and transportation of bacteria. The above conclusions manifested in The average WS, maximum and minimum WS have different impacts, in
different regions, for different microorganisms, temperature had in- which the former operates over a longer period while the latter over a
consistent impacts on them, as temperature showed a negative corre- short. Average WS was more important than maximum WS on the
lation to archaea diversity, and temperature indirectly had a close re- whole, while maximum WS may signally influence release and re-
lationship with archaea diversity by directly influencing soil conditions suspension of dry spore (Li and Kendrick, 1995). High WS can bring
which were main sources of archaea (Fröhlichnowoisky et al., 2014; more microbes into the near surface atmosphere and favor the sus-
Sousa et al., 2008; Zhen et al., 2017). When PM2.5 > 300, a negative pension of microorganisms which will lead a high concentration of
relationship was observed between AM and temperature, this result microorganisms (Jones and Harrison, 2004; Savage et al., 2012).
might because high temperature enhanced toxic compounds' release Nevertheless, in another aspect, high WS has a quite strong atmospheric
and promoted their chemical reactions which occurred on particulate dilution effect that will decrease ambient microbial levels even though
surfaces (Alghamdi et al., 2014; Gao et al., 2016b). Generally, when it can bring in exogenous microbes (Sabariego et al., 2000; Stennett and
temperature rose, viral survival rate decreased as temperature could Beggs, 2004; Zhong et al., 2016). In these studies, author didn't found
affect viral proteins even genome, famously, high temperature could linear correlations and/or significant relation of WS with AM (Li et al.,
cause protein inactivation (Tang, 2009). Some microbes had high 2011; Sousa et al., 2008), while the different results of significant re-
abundance at high temperature, some at low, but most of them oc- lations were found in some reports might due to study regions, micro-
curred at moderate values of the air temperature, appropriate tem- bial sources, inhibitory effect of microbial internal components and
perature facilitated the release and growth of microbes so that it could other factors' cooperation (Crandall and Gilbert, 2017; Grinn-Gofron
cause the increase of microbial concentration (Grinn-Gofroń et al., and Strzelczak, 2011; Harrison et al., 2005; Ma et al., 2011; Mouli et al.,
2017). Therefore, the impact of temperature on AM can't be accurately 2005; Raisi et al., 2010; Wu et al., 2012). In multiple linear regression,
summarized, it needs to take into account the different species and scale two variable sets, average temperature and RH with WS, WS just played
of AM and the interaction of other parameters. The linear correlations a secondary role in archaea diversity (Fröhlichnowoisky et al., 2014).
between AM and temperature alone are good, and in the researches of From these relevant articles, WS has different or no impacts on mi-
the multiple linear regressions between multiple parameters, tempera- crobial concentration, composition and other characteristics. In addi-
ture shows more influence. tion to WS itself, other factors, such as microbial types, study region
etc., can influence the effect on it, so the effect mechanism of WS on
3.1.2. RH microbes individually should more further researches.
RH is the ratio of the partial pressure of water vapor to the equili-
brium vapor pressure of water at a given temperature. With analogous 3.1.4. Others
function as temperature, RH has a significant impact on airborne mi- Except for the main three factors mentioned above, there are some
crobial concentration, diversity, composition and so on, and the other parameters play a role in influencing microbes. Meteorological
bonding effects combining with temperature are most likely to be parameters as the part of microbial living environments, they inevitably
produced and are more obvious (Yan et al., 2016). In previous studies, affect AM. Rain is widely known to clearing ambient environments by
single or several microorganisms were researched to explore the rela- removing aerosol particles which are microbial carriers, in that sense,
tion of RH, and most reports found that microbial release level in- precipitation theoretically will reduce the concentration of AM, but in
creased with decreasing RH. Alternaria alternata, Cladosporium, Drech- many researches precipitation increase airborne microbial concentra-
slera type, Epicoccum, Pithomyces, Polythrincium, Sphaerotheca pannosa, tion. Raindrops were significant for dispersal of slimy spores, which
Erysiphe pisi, Erysiphe graminis, influenza A virus and other AM were resisted wind dislodgement and made a dramatic increase in some
reported had negative correlation with RH (Ianovici, 2016; Sadys et al., spores, and due to the hit and shake of the air and leaves caused by the
2015; Schaffer et al., 1976; Zhen et al., 2017). There was a conclusion droplet, the chance of lifting spores from the surface into air was en-
that the conidia were released when RH decreased and the largest peaks hanced (Jones and Harrison, 2004; Li and Kendrick, 1995). Rain could
in spore release were achieved when RH reduced in the range of 60 to enrich air humidity which may be a sufficient condition for the growth
40% (Jones and Harrison, 2004). However, the discrepancies of the of microorganisms, and the vibrations caused by droplets may facilitate
conclusions were found, a high humidity values, about 70–80%, par- the aerosolization of ground microorganisms, meanwhile, rain could
ticularly assisted the release of basidiospores and ascospores, high RH enhance ambient moisture, which enhancing production and release of
could trigger spore release thus increases the abundance of spores and some AM, so precipitation played a promoting role in the concentration
improve archaea diversity (Fröhlichnowoisky et al., 2014; Gabey et al., and release of AM (Crandall and Gilbert, 2017; Heo et al., 2014). Dif-
2010; Leyronas and Nicot, 2012; Tang, 2009). Despite high RH was ferent from precipitation, solar radiation mostly has a negative relation
benefit to bacterial release and growth, it might also reduce the viabi- with AM because it may provide an unfavorable condition for the
lity of bacteria (Mouli et al., 2005). By this token, the influence of RH growth and survival of airborne microorganisms, and it can kill these
on microbial release is not clear, and different microbes have diverse microbes with microbicidal efficacy of UV. When solar radiation be-
reactions even no reaction on RH (Knudsen et al., 2017). Through these came strong, the UV generally strengthened which would enhance
data, the conclusion that RH can affect microbial release and con- microbicidal ability (Li et al., 2017; Noakes et al., 2004; Raisi et al.,
centration in the air is true, and negative effect is a main part con- 2012). Besides, there is another common meteorological parameter, AP.
sidered to be convincing. High RH levels postponed anther dehiscence Increasing AP reflected there was cold air entrance which could im-
and pollen dispersion as well as prevented dust rising from wet surfaces, prove air diffusion conditions. Cold air can facilitate the release and

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Y. Zhai et al. Environment International 113 (2018) 74–90

transportation of bacteria, and can also quickly dilute bacterial con- seasons, local sources always were dominant among the changed
centrations, so the eventual results, negative or positive relation, are dominant sources which affected temporal variability of airborne mi-
decided by the stronger one of the two. AP was the dominant factor crobial communities (Bowers et al., 2011; Gandolfi et al., 2015; Zhen
shaping bacterial communities in winter and detected the correlation et al., 2017). Also like in the built environments, there are several kinds
was negative between AP and bacterial abundance (Zhen et al., 2017). of the sources of microbes, and the intensities of these sources are
On the contrary, Exiguobacterium, Citricoccus, Nesterenkonia, Mycoplana, different leading to different indoor microbial communities (Prussin
Bacterium, Maris were positively related with AP (Ma et al., 2011). and Marr, 2015). As mentioned above, the characteristics of microbes
Therefore, different conditions bring diverse effects. Actually, the ef- have some discrepancies in different environments, and this can ac-
fects of meteorological conditions on microbes are additive, not in- count for the importance of sources on affecting air microbes. Every
dependent. Hence, considering the impact of meteorological para- environment has their particular and primary sources, like indoors, the
meters on AM, the synergistic effect of many factors is more dominant source may be the human skin and oral cavity (Blais-Lecours
meaningful. et al., 2015; Stetzenbach et al., 2006), outdoors be the vegetation and
soil, inland be the dust (Kellogg and Griffin, 2006; Prospero and Lamb,
3.2. PM 2003), and in the marine may be the sea water, these diversities of
sources provide discrepant proportions for AM, and the ultimate com-
AM mostly exist in the form of aerosol and rarely of individual, so munities certainly have differences.
they generally attach on PM. As microbial carriers, particles are con-
sidered as one of the important influence factors that decide microbial 3.4. Othersc
traits. However, in some reports, relations between AM and PM were
not found, and the reason might be that some microbial weights were AM have influences on humans, in turn, anthropic activities as well
too light to detected by the quantification method, and the big dis- as decide microbial communities and other features. Human epidermis
crepancy of shapes between PM and AM was also one of the reasons and alimentary tract carry 1012–1014 microorganisms, thus in the in-
(Raisi et al., 2010; Sousa et al., 2008). Under certain conditions, a door environments human might be the greatest sources of bioaerosol
constant relationship between biological and total PM would be found, (Luckey, 1972). In indoors environments, some microbial species were
in fact, these conditions were unstable thus the correlations were not brought in by heavy traffic and increased human activities, and the flux
strong. Nevertheless, researchers found a positive relation between of the crowd and human occupancy might be the most crucial factors
protein and coarse PM fraction, not in the fine fraction, and the positive affecting the total number and community structure of bioaerosol,
relation existed between PM10 and Gram-negative rods (Boreson et al., especially in poorly ventilated or heavily occupied environments
2004; Degobbi et al., 2011; Wu et al., 2012). Different AM have diverse (Adams et al., 2015; Bogomolova and Kirtsideli, 2009; Fang et al.,
abundance and size-distribution in different size PM, therefore many 2007). In outdoor environments, the more pedestrian volume is, the
different AM show significant difference among samples of PM which more bioaerosol are observed. Therefore, human activity is one of the
mirror the different correlation with PM. Malassezia, Fusarium and Al- crucial factors.
ternaria were more abundant in PM2.5, PM10 and TSP samples, respec- Besides, air pollutions are the influence factors which worth men-
tively, which showed microbial types might play an important role in tioning. Common air pollutions include SO2, O3, NOx and so on, though
associating microbial composition and diversity with PM, and the main there is a view that air pollutions' effect is smaller than other factors,
proportion of fungi (aerodynamic diameters between 2.1 and 3.3 μm) they still have different effects on AM. Ozone is notoriously difficult to
increased with increasing mass concentration of all three inhalable sizes control and famous for its oxidation, in high concentrations ozone, AM
of PM (PM1, PM2.5, PM10) (Raisi et al., 2012; Yan et al., 2016). A may be killed by the oxidation of ozone, and these processes can
unanimously negative correlation between cultivable bioaerosols with completely inhibit or effectively reduce the growth of fungi, but low O3
PM2.5 was observed and the reason of that was PM2.5 usually contained concentration has no evident effect on the AM (Whangchai et al., 2006).
soot, metals, and secondary inorganic components which were harmful Ozonic germicidal properties let it be toxic to AM, so ozone was found
to bioaerosol (Gao et al., 2016a). However, at the low-haze station, showing a negative effect on AM (Gao et al., 2016b; Ho et al., 2005).
different from above conclusion, PM10 was positively related to But Cladosporium and Alternaria spore abundance was observed having
bioaerosol showing that particles indeed could carry microbes and af- a positive dependence on O3, and positive statistically significant cor-
fect them under suitable conditions. Particulate characteristics in some relation coefficients between O3 and Aspergillaceae and the total fungal
degree decide the relationship between PM and microbes, but the de- spores were found (Adhikari et al., 2006; Grinngofroń et al., 2011).
finite mechanisms are certainly not clear, this could be caused by that However, Sousa et al. (2008) didn't discover ozone have significant
the effects of other parameters are great thus the influence of PM on influence on the concentration of fungal spores (Sousa et al., 2008). The
microorganisms is not obvious. difference may be caused by the neutralization of other factors and the
distinction of microbial types. SO2 and NO2 usually were considered as
3.3. Sources toxic pollutants to microorganisms (Abdel Hameed et al., 2012), theo-
retically playing an obvious negative relation with AM, but according to
To some extent, sources of microbes, both local air mass and long research by Grinngofroń et al. (2011), they thought there were no or
distance air masses, decide the airborne microbial communities weak negative significant relation between SO2, NO2 concentrations
(Innocente et al., 2017). AM are mainly derived from local source, so and the fungal spore concentrations (Grinngofroń et al., 2011). And Gao
the sampling sites are important influence factors of microbial com- et al. (2016b) observed that at different times, the effects on bioaerosol
munities, which cause the bioclimatic characteristics of the sampling were changed with a positive relationship in the morning and evening,
environment becoming one of the hot research points. AM almost come but a negative relationship at mid-day (Gao et al., 2016b). SO2 and NO2
from other environments, because atmosphere just is a temporary re- and other air pollution generally have no direct impact on the AM, and
sidence not origin, this characteristic lead to air microbial communities they have more interactions with other factors thus affect bioaerosol.
greatly depend on microbial sources, and relative contribution from According to influence factors discussed above, the correlation be-
these sources may determine the airborne microbial composition and tween them and airborne microbial characteristics are concluded in
temporal variability (Bertolini et al., 2013). Local sources played a Table 6. Except for the above factors, there are other factors of AM that
leading role in shaping airborne bacterial communities and had a larger can be researched with their impact types and mechanisms. These
impact than those caused by meteorological conditions. Besides, local factors are not independent but interactive which may be interoperable
sources influenced microbial seasonal variation, because in different or antagonistic. Because of effects of these parameters, the AM own

85
Y. Zhai et al. Environment International 113 (2018) 74–90

variability and diversity. These factors can give researchers study or-

(Crandall and Gilbert, 2017)

(Grinngofroń et al., 2011)

ientations, if they want to clearly know the AM, these factors with their

(Bertolini et al., 2013)

(Gandolfi et al., 2015)
effects should be researched.

(Seifried et al., 2015)

(Bowers et al., 2011)

(Sousa et al., 2008)
4. Perspectives
Reference

According to the above summarized in this review, advance has

already been made for the understanding of microbial composition and
–

their influence factors, but there are many other information waiting to
Correlation

be found and understood. Based on the general consideration above,

several research gaps are listed below:
Type

⊖
⊕
⊖
⊗
⊖
⊖
⊕
⊖

(1) Size decides the inhalation and deposition of particles, which is a

(Sabariego et al., 2000)
(Alghamdi et al., 2014)

(Quintero et al., 2009)

(Gandolfi et al., 2015)

key factor causing diseases and influence climate. With kinds of AM

(Gao et al., 2016a)

(Raisi et al., 2012)

(Fang et al., 2016)

in particles, the potential hazard and influence are more worth

(Yan et al., 2016)

exploring, hence, on size-segregated particles, airborne microbial

compositions and traits can be subsequent research objects. Multi-
Reference

stage sampler can achieve particulate separation, and the right

sampler should be chosen for the experiment based on the sampling
environment and conditions. About detection of AM, culture-in-
Correlation

dependent method is a better choice because the vast majority of

Variation

AM are non-cultivable. Molecular biological techniques, such as

high-throughput sequencing technology like 16S rRNA sequencing,
⊕
⊕
⊖
⊖
⊖
⊕
⊕
⊖

metagenomics sequencing and Illumina MiSeq sequencing (Gao

(Fröhlich-Nowoisky et al., 2014)

et al., 2017a), and electrophoresis technology can be used for

(Abdel Hameed et al., 2012)

analysis for their high efficiency accuracy.

(2) AM are not invariable on PM, many factors influence their char-
(Agabou et al., 2013)

(Kumari et al., 2016)

(Bowers et al., 2012)

acteristics, and relationships between the two are necessary to

study clearly. At present, the influence mechanisms of these factors
are ill-defined, researches just measured temporary relationship at a
Reference

certain circumstance. In order to take better defense and mon-

itoring measures for AM, stable relations should be established
between influence factors and AM, and influence mechanisms
–
–

should be understood. Further studies can adopt control variable

Correlation
Diversity

method and appropriate simulation to research influence mechan-

isms, and create optimal multivariate linear regression model to
⊖
⊖
⊖
⊗
⊗
⊖
⊖
⊗

synthesize multi-factors' effects.

(3) PM can cause a wide range of diseases that reduce human life, and
(Yamamoto et al., 2012)
(Dybwad et al., 2014)

some AM with pathogenicity also affect human health, so detailed

(Bowers et al., 2013)
(Liu et al., 2017a)

knowledge of impact of AM on human health is of primary sig-

(Li et al., 2017)

(Li et al., 2017)

nificance. Nowadays, health risk assessment of exposure to PM and

other pollutions in particles are hot research points (Balwant et al.,
Reference

2015; Huang et al., 2014; Wang et al., 2017; Zhai et al., 2016), but
less attention about AM. The relevant research contents about AM
Size distribution

can combine with PM because particles as carriers will affect mi-

Correlation
Correlation between influence factors and airborne microbial characteristics.

crobial traits. Getting the accurate risk level can provide a basis for
people to better take protective measures and plan solutions. Re-
searchers generally just get several sets of microbial data in one
⊖
⊖
⊗
⊖
⊗
⊗
⊕
⊖

PS: the correlation described in the table is primary, not absolute.

study, which are not enough to do health risk assessment, so we can

(Jones and Harrison, 2004)

choose simulation methods to do this. As a statistical test method,

(Almaguer et al., 2014)

(Goudarzi et al., 2014)

(Degobbi et al., 2011)

Monte Carlo simulation method is applied in many experiments and

(Dong et al., 2016)

(Heo et al., 2014)

simulation with its advantages that can deal with non-linear, large-
(Gao et al., 2015)
(Lee et al., 2007)

wave problems, get more accurate and reliable results by a lot of

path simulation scenarios and so on (Safadi et al., 2015; Smid et al.,
Reference

2010). Hence, Monte Carlo simulation method is a choice for health

risk assessment of AM over PM.
Concentration

(4) Like some researchers study patience and resistance for some
“⊕”: have significant correlation.
Correlation

matters of microbes in soil and/or water, the similar contents also

can extend to the AM. Through source apportionments we can
confirm some AM experience long-distance transportation and long-
⊕
⊕
⊕
⊖
⊖
⊖
⊖
⊖

“⊖”: have correlation.

time suspension, but they still maintain survivability evidencing

“⊗”: no correlation.
Influence factors

Solar radiation

AM own resistibility to some hazardous substances in the air. These

Air pollutions
Precipitation
Temperature

properties can be used to protect environment rehabilitating da-

“–”: no data.
Sources

maged ecosystems and utilized for biological monitoring and bio-

Table 6

logical purification. Relevant researches can start from one or two

PM
WS
RH

dominant and representative species then conducted follow-up

86
Y. Zhai et al. Environment International 113 (2018) 74–90

studies. meteorological parameters. Int. J. Biometeorol. 58, 1459–1470.

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Bauer, H., Giebl, H., Hitzenberger, R., Kasper-Giebl, A., Reischl, G., Zibuschka, F.,
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This research was financially supported by a project of scientific and bacterial communities across land-use types and their relationship to the bacterial
communities of potential source environments. ISME J. 5, 601–612.
technological project of Changsha City (KQ1602029), the Bowers, R.M., McCubbin, I.B., Hallar, A.G., Fierer, N., 2012. Seasonal variability in air-
Interdisciplinary Research Funds for Hunan University (2015JCA03), borne bacterial communities at a high-elevation site. Atmos. Environ. 50, 41–49.
and a project of Shenzhen Science and Technology Funds 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 at-
(JCYJ20160530193913646). mosphere. Environ. Sci. Technol. 47, 12097–12106.
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