Seasonal changes in local landscapes drive airborne microbial community variation

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Interactions between physico-chemical characteristics and airborne microorganisms in the troposphere

Physico-chemical characteristics of the atmosphere that might constrain microbial life

A variety of chemical substances interact with tropospheric microorganisms and subsequently might have an effect on them. Solid and liquid aerosols can be composed of essential nutrients (carbon, oxygen, nitrogen, phosphorus, sulfur, hydrogen, trace minerals) that could be used as source of energy and matter for microbial metabolism. The troposphere also contains free radical species (the hydroxyl radical OH is the most common and reacts with nearly every chemical species) and compounds at potential toxic concentrations (heavy metals, persistent organic compounds, antibiotics) that may have negative effects on microbial development and survival. Temperature and photochemical processes constantly alter the aerosol properties as well as their chemical composition. The physical and chemical characteristics of the atmosphere that we think constitute the main constraints of microbial life in the dry troposphere are presented below.
UV radiation. UV radiation levels can be extremely high and destructive in the atmosphere. The highly energetic wavelengths (UV-C ~190-290 nm and UV-B ~290-320 nm) are responsible for direct DNA damage that could be lethal. Longer wavelengths (UV-A ~320-400 nm and visible light ~400-800 nm) contribute to intra-cellular reactive oxygen species (ROS) production that can cause subsequent oxidative damage to DNA, RNA, lipids and proteins, altering microbial metabolism and survival53,54. Some microorganisms have developed a range of protection mechanisms against UV radiation. Cell aggregation, association with particles and production of carotenoid pigments to scavenge ROS are all mechanisms used by environmental microorganisms to reduce the effects of destructive UV radiation. The stratosphere supports by far the highest levels of UV radiation found on Earth as levels increase by around 11% with every 1000 m in altitude (WHO). Data on the impact of UV radiation on airborne microorganisms comes mainly from investigations using high UV levels such as those found in the upper troposphere or stratosphere layer. Smith et al. (2011)36 showed that UV radiation was the most biocidal factor in the low stratosphere, and could kill up to 99.9% of Bacillus subtilis spores after 96 h. However, the authors pointed out that spore resistance might be dependent on the environment the cells germinated in55–57. Consequently, UV resistance might have been higher if the spores were directly isolated from the stratosphere and not germinated in culture media like was done in the study. Microbial strains isolated from the upper troposphere and lower stratosphere exhibited a higher resistance to UV radiation as compared to those from the troposphere at ground level58. Some Deinococcus and Streptomyces strains showed an extreme UV resistance and tended to form aggregates in culture medium. These aggregates were suggested to be a protection mechanism58. With the exception of sporulation and cell aggregation, no other protective mechanism against UV radiation has been observed in airborne microbial communities. UV radiation levels and consequently the need for UV protection mechanisms might depend on the height of the troposphere (i.e. planetary boundary layer or free troposphere height), geography (for example the tropics harbor higher UV levels) and surface conditioning (i.e. surface reflectance)59.
Temperature shock and freeze-thaw cycles. At the same altitude, atmospheric temperature is highly dependent on the latitude and longitude of the site. It also decreases by 0.6 to 1°C for every 100 m increase of altitude and can reach -70°C in the upper stratosphere. Upward aerial transport of microorganisms with high-speed winds could occur rapidly and airborne microorganisms might suffer large temperature shocks. Airborne microorganisms present in an air parcel transported from the surface to 1 km altitude can undergo a temperature decrease of 5 to 10°C and a substantial increase in relative humidity4. Cold temperature and freeze-thaw cycles generally occur at high latitudes, high altitudes and/or in clouds and so do the resulting impact. They slow down microbial metabolism, decrease membrane fluidity, and influence protein refolding. Freeze-thaw cycles could additionally lead to mechanical stress that might damage the cell membrane60–62. Freeze-thaw cycles were shown to alter the survival of microbial strains following UV radiation, H202 exposure and osmotic shock when these factors were tested individually on strains isolated from clouds belonging to Pseudomonas, Sphingomonas, Arthrobacter and the yeast Dioszegia8. To date, no specific mechanism of protection against cold temperature and freeze-thaw cycles known to be used by environmental extremophile microorganisms63 has been observed in airborne microbial communities.
Relative humidity and condensation/evaporation cycles. The troposphere harbors the whole range of relative humidity (RH) values, from values near 0% in the upper troposphere up to 100% above ground level. Investigations on the survival of aerosolized microorganisms under different RH showed different results depending on the species. While the survival of airborne Flavobacterium was not affected by RH ranging from 25 to 99% at 24°C64, mid-range RH negatively impacted mycoplasma survival but not RH values outside of this range65. In the environment, desiccation resistance is generally associated to ionizing radiation resistance66– 70. Yet, the mutual nature of the underlying mechanisms remains unknown. In the environment, the molecular mechanisms underlying desiccation resistance remain poorly defined and seem to involve wax ester biosynthesis71 and DNA reparation mechanisms. Desiccation, like radiation, tends to induce DNA damage70,72.
Evaporation/condensation cycles of water vapor occur in the troposphere, both in the dry troposphere and in clouds. In a water droplet, evaporation can concentrate metabolites in the near environment of the cells by up to 1000 times8. Evaporation/condensation cycles induce osmotic changes, leading to water fluxes between the intracellular and extracellular compartment of the cell to maintain osmolarity. These water fluxes can provoke cell damage, increase the concentration of metabolites in cells, and increase the concentration of compounds like radicals and metals around the cell73,74. Alsved et al. (2018)75 showed that during evaporation, Pseudomonas syringae survival was enhanced when the relative humidity rapidly reached the level where salts become solid. Hence, small and salty liquid droplets were suggested as a more suitable environment when exposed to evaporation than large and slightly salty liquid droplets75. Microbial cells could use compatible solutes that are osmoprotectants to control water fluxes. However, the effect of deleterious evaporation/condensation cycles on for airborne microbial communities and the mechanisms they use to protect themselves are unknown.
Concentration of radicals. The potential impact of the oxidizing nature of the atmosphere that is characterized by an enhanced presence of radicals (OH, O2-), nitrate radicals and OH precursors such as hydrogen peroxide (H2O2)4,11 on airborne microorganisms has been mainly investigated in cloud water. Joly et al. (2015)8 tested the effect of different concentrations of hydrogen peroxide on the survival of different microbial strains isolated from cloud water. They showed that the 50% lethal concentration of H202 was different among the strains, and ten times higher than the typical concentration found in Puy-de-Dôme cloud water. Increases in ROS (reactive oxygen species) could occur during other environmental stresses, like UV radiation, as discussed above. They could be deleterious to DNA, RNA, proteins, lipids in cells and can lead to cell death. Anti-oxidant molecules such as vitamins, glutathione, carotenoid pigments and specific enzymes could help deal with an excess of radicals. Yet, the mechanisms involved in the resistance of airborne strains to high concentration of radicals remain unknown8.

Physical selection versus microbial adaptation of airborne microbial communities

The question as to whether atmospheric chemistry and physics might be controlling factors in leading to the survival and/or development of microbial taxa with specific functions in the atmosphere remains open. On the one hand, the harsh physical and chemical conditions of the troposphere might cause the death of non-resistant cells, a process we consider as physical selection. Resistant cells might survive, and even develop if they are active and growing (discussed in a following section). On the other hand, microbial adaptation (i.e. genetic changes in the genome in response to the physical and chemical conditions) might also occur. This would increase adaptation to the tropospheric environment.
In the troposphere, microorganisms in the gas and solid phase face UV radiation, low temperature, low relative humidity and the presence of radicals which can all affect microbial survival or metabolism as discussed above. These conditions become more and more intense as altitude increases and are considered as extreme at the top of the troposphere36. UV radiation levels can be both extremely high (stratosphere) and relatively low (planetary boundary layer) at different heights. While UV radiation might be a critical factor in shaping airborne microbial communities through the selection of resistant microorganisms over a certain height of the troposphere, this remains unknown for the lower troposphere. Survival studies have mainly been done under simulated cloud and stratospheric conditions, and on isolated cultivable microorganisms of an atmospheric origin. While Smith et al. (2011)36 showed that UV radiation was the most biocidal factor in the low stratosphere, Joly et al. (2015)8 suggested that freeze-thaw cycles and osmotic shock were the most damaging factors for microorganisms in clouds when these factors were tested individually on isolated strains. Survival mechanisms such as dormancy, sporulation, aggregation between cells or with particulate matter, and microbial resistance to the extreme conditions encountered in the atmosphere are relatively common in the environment8. Fungal spores have evolved to survive and disseminate through the troposphere. They are known to be particularly resistant to atmospheric conditions, and especially to desiccation, UV radiation and oxidative stress76. Yet, their resistance might have been selected for on Earth surfaces before being aerosolized. Some might resist the physical selection but might not adapt while suspended in the air. While resistant microbial cells were observed in the air, the question about whether these resistant cells represent the majority of the airborne microbial cells remains. Little is known about the survival mechanisms of both airborne bacterial and fungal cells, and the ratio between resistant and sensitive cells in the air. We expect a higher abundance of resistant cells as conditions are more intense as altitude increases in the troposphere. Yang et al. (2008)58 showed that microbial strains isolated from the upper troposphere exhibited a higher resistance to UV radiation as compared to strains from the atmosphere at ground level.
Microbial cells resistant to extreme conditions exist in the major sources of airborne microbial cells, (e.g., in soil and water). Survival of airborne cells might be the result of an innate resistance (like fungal spores) or a resistance acquired while aerially transported. Genetic changes in airborne microbial genomes allowing a better survival and/or metabolism (and even development) in the atmosphere might be expected. However, microbial cells might face constantly changing conditions during aerial transport (i.e. changes in temperature, UV radiation, condensation/evaporation of water etc.), which could prevent their adaptation. In the ocean, a faster evolution of microorganisms than ocean currents can disperse them has been suggested in the Atlantic and Pacific oceans (oceanic surface current speed around 0.05 m/s;77,78). However, air currents could be 100 even 1000 times faster than surface oceanic currents. Inputs of new cells through aerosolization from Earth surfaces are large and continuous in the planetary boundary layer. The free troposphere might receive less cells than the layers close to the ground, and these cells might have initiated a selection process within the planetary boundary layer. We can thus expect to observe the effects of physical selection and microbial adaptation more in the free troposphere as compared to the planetary boundary layer2.
Physical selection and microbial adaptation in the troposphere, if occurring, might lead to a functional differentiation of airborne microbial communities in response to atmospheric conditions as compared to their source environments. The impact of these processes on the functional potential of airborne microbial communities will be addressed in Chapter 5 of this thesis.

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Metabolic activity and growth of airborne microbial communities

Activity and growth. Airborne microbial cells might be a mix of dead and living cells. The atmosphere harbors carbonaceous sources and inorganic components essential for microbial metabolism, but the stressful conditions (i.e. UV radiation, radicals, desiccation, low temperature etc.) might affect the microbial metabolic potential of the living cells. UV radiation in particular has been shown to be a critical factor restraining microbial activity of the oceanic surface bacterioplankton79–84. It has been shown that irradiance affected bacterioplankton more in spring and summer83 and that the activity could be suppressed up to 40% in the top five meters of the water column in near shore waters80. Metabolic activity in the atmosphere could be restricted to specific microbial cells resistant to the atmospheric conditions, as well as cells embedded in particulate matter and protected from the potential selective conditions (UV radiation, radicals, desiccation etc.)85. The first to date and still one of the rare functional metagenomic studies on airborne microorganisms from the dry troposphere was conducted in New York City and San Diego (USA), and revealed that airborne microorganisms carry a rich panel of putative functional genes86. Planetary boundary layer and cloud isolated microbial strains have been shown to metabolize the carbonaceous compounds found in the atmosphere5,87,88. rRNA-based studies identified the taxonomy of the potential active microbial taxa in the dry troposphere and cloud water7,89,90. Epiphytic, parasitic and endosymbiontes bacterial taxa (i.e. Sphingomonas, Methylobacterium, Acidiphilium, Pseudomonas, Comamonas) have been suggested as the most active organisms due to their physiological properties (resistance to temperature and humidity shifts, high levels of UV radiation etc.) compatible with their maintenance in the dry troposphere and clouds89,91. The same was observed for fungi with plant pathogens and saprophytic taxa (Pleosporales, Magnaporthales, Xylariales, Conioscyphales etc.) potentially showing the highest activities89,91. In clouds, it has been suggested that bacteria might be more active than fungi based on a transcriptomic study13.
Airborne microbial growth and reproduction have been suggested in cloud water. Half of the tested strains (11 out of 20) originating from Puy-de-Dôme (France) cloud water have been able to grow at 5°C, which is the average temperature of Puy-de-Dôme clouds7. Sattler et al. (2001)92 suggested that bacterial production in cloud water might range from 3.6 to 19.5 days (production measurement at 0°C), which was comparable to those of phytoplankton in the ocean, i.e. about a week93. Temperature in the planetary boundary layer might be higher than 0°C; consequently, microbial replication time might be less than 4 days. Residence time in the air might be a critical factor for airborne microorganisms to reproduce, as microbial replication time might be of the same order as residence time.
Role in atmospheric chemistry. Airborne microorganisms might transform atmospheric chemical compounds and play a role in biogeochemical cycles17,87. In clouds, microorganisms have been shown to use the main carboxylic compounds (monoacid and diacid compounds: formate, acetate, lactate, succinate, formaldehyde and methanol), organic nitrogen as well as the radical precursor H202 after cultivation5–7,12,88. Using a liquid medium mimicking the composition of cloud water and a temperature at 5°C (average temperature of low-altitude clouds), biological activity was shown to drive the oxidation of carbonaceous compounds during the night (90 to 99%), while contributing 2 to 37% of the reactivity during the day alongside radical reactions mediated by photochemistry5. Studies on the metabolic activity of airborne microbial cells in situ present major technical issues. Most of the studies evaluating the metabolic potential of airborne microbial communities are based on cultivable microorganisms, and in this way are studies whose conditions (physics and chemistry) are far from those found in the atmosphere. Given the high taxonomic and functional microbial diversity found in the troposphere, we suppose that airborne microorganisms could have an impact on different biogeochemical cycles. The potentially significant contribution of chemical transformations mediated by airborne microorganisms might explain the inconsistencies observed in some chemical cycles in the atmosphere, such as the cycle of secondary organic aerosols94,95. Reviews on the role of airborne microorganisms in atmospheric chemistry and more generally on the reactivity of bioaerosols in the air can be found in Ariya et al. (2002)87, Delort et al. (2010)14 and Estillore et al. (2016)96.
Distribution factors of airborne microbial communities (geography and time) in the troposphere
Research on the temporal and spatial distribution of microbial communities of the troposphere (in both the liquid and dry phases) based on studies that took place mainly at ground level have revealed that local or regional surfaces42,97, meteorology (or ground air circulation)23,98–100, seasons42,97,100,101 and global air circulation (that is, inputs from distant surfaces)25,44,100,102,103 are partly responsible for the observed composition of airborne microbial communities. However, there is a lack of understanding of the relative contribution of these driving factors on the composition of the tropospheric microbial community

Surface characteristics

Airborne microorganisms are emitted mainly by Earth surfaces, i.e. from natural (for example forests, oceans, deserts) and urbanized surfaces (agricultural fields, waste water treatment plants, cities). Burrows et al. (2009)104,105 constrained a general atmospheric circulation model using data from the literature and estimated that 1024 bacteria are emitted into the atmosphere each year at a global scale. Microscopic and molecular biology analyses showed that bacterial cells are generally in higher concentration compared to fungal cells and spores in the troposphere2,7,19,44,106,107. Observations of the microbial diversity in the planetary boundary layer showed that airborne microorganisms from one atmospheric sample might come from many different ecosystems (plants, soil, ocean etc.) that might explain the observed large taxonomic diversity of airborne microbial communities. Aerosolization from Earth surfaces depends mainly on the landscapes (i.e. forest, grassland, ocean etc.), as well as the current meteorological conditions. Oceanic surfaces were shown to emit less than terrestrial surfaces105. Among terrestrial surfaces, grasslands might be the most effective emitters of microorganisms, while ice potentially emits 100 times less microbial cells105. Meteorological conditions would impact the aerosolization mechanism of the surfaces.

Table of contents :

Chapter 1: Bibliography – Airborne microbial communities of the troposphere
Introduction
Microbiological characteristics of the troposphere
Bioaerosols in the troposphere
Planetary boundary layer versus free troposphere and vertical distribution of airborne microbial communities
Interactions between physico-chemical characteristics and airborne microorganisms in the troposphere
Physico-chemical characteristics of the atmosphere that might constrain microbial life
Physical selection versus microbial adaptation of airborne microbial communities
Metabolic activity and growth of airborne microbial communities
Distribution factors of airborne microbial communities (geography and time) in the troposphere
Surface characteristics
Physical selection of airborne microorganisms during aerosolization
Long-range transport of airborne microorganisms and contribution of local versus distant sources
Meteorology
PhD objectives, approach and working hypotheses
References
Supplementary Information
Chapter 2: Methods to investigate the global atmospheric microbiome
Section 1: Protocol optimization and quality control
Abstract
Introduction
Material and Methods
Results
Conclusion
References
Section 2: Molecular biology analyses
References
Chapter 3: Global airborne microbial communities controlled by surrounding landscapes and wind conditions
Abstract
Introduction
Material and Methods
Results
Discussion
Conclusion
References
Supplementary Information
Chapter 4: Seasonal changes in local landscapes drive airborne microbial community variation
Abstract
Introduction
Material and Methods
Results
Discussion
Conclusion
References
Supplementary Information
Chapter 5: Microbial functional signature in the atmospheric boundary layer
Abstract
Introduction
Material and Methods
Results
Discussion
Conclusion
References
Supplementary Information

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