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Microbial Ecology of the Planetary Boundary Layer

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Microbial Ecology of the Planetary Boundary Layer atmosphere Review Microbial Ecology of the Planetary Boundary Layer Romie Tignat-Perrier 1,2,* , Aurélien Dommergue 1 , Timothy M. Vogel 2 and Catherine Larose 2 1 Institut des Géosciences de l’Environnement, Université Grenoble Alpes, CNRS, IRD, Grenoble INP, Grenoble, 38400 Saint-Martin-d’Hères, France; [email protected] 2 Environmental Microbial Genomics, CNRS UMR 5005 Laboratoire Ampère, École Centrale de Lyon, Université de Lyon, Écully, 69007 Lyon, France; [email protected] (T.M.V.); [email protected] (C.L.) * Correspondence: [email protected] Received: 17 October 2020; Accepted: 28 November 2020; Published: 30 November 2020 Abstract: Aerobiology is a growing research area that covers the study of aerosols with a biological origin from the air that surrounds us to space through the different atmospheric layers. Bioaerosols have captured a growing importance in atmospheric process-related fields such as meteorology and atmospheric chemistry. The potential dissemination of pathogens and allergens through the air has raised public health concern and has highlighted the need for a better prediction of airborne microbial composition and dynamics. In this review, we focused on the sources and processes that most likely determine microbial community composition and dynamics in the air that directly surrounds us, the planetary boundary layer. Planetary boundary layer microbial communities are a mix of microbial cells that likely originate mainly from local source ecosystems (as opposed to distant sources). The adverse atmospheric conditions (i.e., UV radiation, desiccation, presence of radicals, etc.) might influence microbial survival and lead to the physical selection of the most resistant cells during aerosolization and/or aerial transport. Future work should further investigate how atmospheric chemicals and physics influence microbial survival and adaptation in order to be able to model the composition of planetary boundary layer microbial communities based on the surrounding landscapes and meteorology. Keywords: airborne microorganisms; atmospheric microbial communities; aerosolisation; bioaerosols; biosphere-atmosphere interactions; long-range transport; aerial transport 1. Introduction Aerobiology is a growing research area that covers the study of aerosols of a biological origin (i.e., bioaerosols) suspended in the atmosphere, from the air that directly surrounds us (both indoors and outdoors) to space by going through the different atmospheric layers (Figure1). Bioaerosols include plant debris, pollen, microorganisms (bacteria, fungi, viruses, protozoans, etc.) as well as biological secretions [1,2] which are mainly emitted by natural (forests, oceans, deserts, etc.) and urbanized Earth surfaces (agricultural fields, waste water treatment plants, cities, etc.) at different emission rates [3,4]. Airborne microorganisms, especially bacteria, archaea, and fungi, are of particular interest as they represent living and potentially metabolically active cells light enough to be lifted high in the atmosphere by upward airflow [5–7]. During extreme meteorological events such as volcano eruptions and dust storms, sand-dust associated microorganisms can be ejected tens of kilometers high in the atmosphere before landing back on the Earth’s surface thousands of kilometers away [8,9]. Microorganisms from the Bacillus and Micrococcus genera are commonly recovered from the stratosphere [6,10,11]. Research on the “high life” [5] intends to evaluate the global dispersion of microorganisms around our planet as well as establish the upper limit of the biosphere boundary Atmosphere 2020, 11, 1296; doi:10.3390/atmos11121296 www.mdpi.com/journal/atmosphere Atmosphere 2020, 11, 1296 2 of 17 and infer the probability of life in the universe [12,13]. Other interests are driving investigations of microorganismsAtmosphere 2020, in11, xthe FOR PEER lowest REVIEW atmospheric layer, the troposphere, that surrounds2 of 17 the Earth’s surface. The role of airborne microorganisms in meteorological processes such as cloud formation and precipitationmicroorganisms [14–17 in ],the atmospheric lowest atmospheric chemistry layer, the [ 14troposphere,,18–21], andthat surrounds air quality the Earth’s [9,22– surface.24] are currently The role of airborne microorganisms in meteorological processes such as cloud formation and motivating multidisciplinary investigations on microbial communities in the troposphere. The capacity precipitation [14–17], atmospheric chemistry [14,18–21], and air quality [9,22–24] are currently of microorganismsmotivating multidisciplinary to be transported investigations through on themicrobial air has communities raised concern in the troposphere. about the The role airborne microorganismscapacity of might microorganisms play in public to be transported health with through the potentialthe air has disseminationraised concern about of plantthe role and human pathogensairborne as well microorganisms as allergens might [9,25 play]. The in public importance health with of airbornethe potential micro-organisms dissemination of plant should and motivate human pathogens as well as allergens [9,25]. The importance of airborne micro-organisms should the inclusion of a biological component into the existing and future observing infrastructure of the motivate the inclusion of a biological component into the existing and future observing infrastructure earth atmosphere.of the earth atmosphere. Figure 1. The different biological niches investigated in aeromicrobiology. These different niches might Figure 1. The different biological niches investigated in aeromicrobiology. These different niches exchange microorganisms and represent different physico-chemical conditions for airborne microorganisms. might exchange microorganisms and represent different physico-chemical conditions for airborne microorganisms. Subject to gravity, aerosols (or particulate matter) as well as bioaerosols become concentrated in the lower partSubject of the to gravity, troposphere aerosols that(or particulate is called matter) the planetary as well as bioaerosols boundary become layer concentrated (Figure1). in Microbial concentrationsthe lower thus part usually of the troposphere show a vertical that is stratificationcalled the planetary from boundary the bottom layer to(Figure the top 1). Microbial of the troposphere concentrations thus usually show a vertical stratification from2 the bottom7 to the top3 of the with averagetroposphere estimated with average bacterial estimated concentrations bacterial concentrations of 9 10 of 9 ×2 102 −10 2 × cells107 cells/m/m 3in in thethe planetary × − ×1 4 3 boundaryplanetary layer (based boundary on sixlayer qPCR-based (based on six studies:qPCR-based [26 studies:–31] and [26–31] 4 and10 4– × 8101 –10 8 × cells104 cells/m/m in3 in the highest × × part of thethe tropospherehighest part of the called troposphere the free-troposphere called the free-troposphere (based (based on three on three qPCR-based qPCR-based studies [32–34]). Yet, microbial[32–34]). concentration Yet, microbial concentration estimations estimations vary between vary between investigations, investigations, which which are are basedbased on on different different sampling strategies. Heterogeneity of methodology in aeromicrobiology is a current issue samplingthat strategies. will be discussed Heterogeneity in a subsequent of methodology section. The troposphere in aeromicrobiology is the most dynamic is a current layer in terms issue of that will be discussedchemistry in a subsequent and physics section. of aerosols The and troposphere harbors complex is the chemical most dynamic reactions layerand meteorological in terms of chemistry and physicsphenomena of aerosols that lead and to the harbors coexistence complex of a gas phas chemicale, liquid reactions phases (i.e., and cloud, meteorological rain, and fog water) phenomena that leadand to the solid coexistence phases (i.e., microscopic of a gas phase,particulate liquid matter, phases sand du (i.e.,st) (Figure cloud, 1). The rain, various and fogatmospheric water) and solid phases represent multiple biological niches that might harbor different microbial communities phases (i.e.,(Figure microscopic 2) and different particulate microbial matter, concentrations sand dust)that might (Figure be due1). Theto significant various differences atmospheric in phases representphysico-chemical multiple biological characteristics niches thatthat mightconstrain harbor either di microbialfferentmicrobial life within communities the niches or (Figurethe 2) and different microbialdestruction of concentrations specific members thatfrom mighttheir sour bece. due Liquid-phase to significant associated diff microbialerences communities in physico-chemical characteristics(i.e., associated that constrain to cloud, eitherrain, and microbial fog water) lifemight within be particularly the niches different or thefrom destruction the microbial of specific communities of the dry phase of the troposphere [35] (Figure 2). Reviews and field investigations that members from their source. Liquid-phase associated microbial communities (i.e., associated to cloud, rain, and fog water) might be particularly different from the microbial communities of the dry phase of the troposphere [35] (Figure2). Reviews and field investigations that are specifically related to cloud-associated microorganisms can be found in [14,36–39]. This review aims to synthesize knowledge and gaps of knowledge regarding
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