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There is a long-standing preconception in ecology that both landmasses and bodies of water constitute habitats for living systems whereas the atmosphere does not; this preconception, however, is now beginning to change. In recent years, there has been a resurgence of interest in the ecology of living organisms found in the atmosphere. This chapter is an account of Earth's past and present-day atmospheres as habitats for microorganisms, starting with the origin of a primary atmosphere that was completely inhospitable to any life. The developmental history of the atmosphere is considered in detail, including its co-evolution with early living systems to create the only oxygen-containing atmosphere in the Solar System and also its contributions to early microbial evolution throughout the Precambrian Supereon. The composition and physical structure of the present-day atmosphere are also considered in the context of a microbial habitat, especially as they relate to the metabolic and reproductive activities of airborne microorganisms and the movement of vast numbers of microorganisms through the troposphere by global atmospheric circulation. It is this movement that is largely responsible for the worldwide dispersal of microorganisms and connecting all microbial habitats across the Planet's surface to one another. Additionally, it is the most straightforward means of accounting for the cosmopolitan distributions reported for many microbial species and, as recently suggested, might possibly give rise to biogeographic regions in the atmosphere, currently an ongoing debate among many microbiologists.

Research efforts focused on the Earth’s biota have been limited almost exclusively to land, soil and aquatic habitats; however, this focus is now beginning to change. There is a renewed and building interest in the ecology of living microorganisms found in the atmosphere. Hundreds of thousands of individual microorganisms can exist in a cubic meter of air,1  which can represent hundreds of different taxa.2,3  The atmosphere is one of our Planet’s most intriguing habitats to investigate because extreme cold temperatures, hypobaria (low pressures), desiccation and ultraviolet (UV) irradiation make it more indicative of the surface conditions on Mars rather than anywhere else on Earth.4  In a recent report,5  the atmosphere was described as “one of the last frontiers of biological exploration on Earth.”

The Planet’s atmospheric biota, however, remains one of the most challenging to investigate, which has been reflected by the many shortcomings encountered throughout the history of aerobiology. In the past, aerobiological studies relied almost exclusively on culture-based analyses that neglected the vast majority of microbes present in air samples.1,6,7  This is because only 0.1–10% of the total airborne microbial flora are able to grow in culture.8–10  Airborne microorganisms can also become damaged or killed by desiccation, UV irradiation or the extreme low temperatures that occur in the atmosphere. Acquiring culture-independent microbiological data, on the other hand, can be difficult because the density of airborne microorganisms decreases with increasing altitude.1,11  Large, or sometimes enormous, volumes of air must be collected and processed for detecting microorganisms with molecular detection assays and air-sampling systems must also be designed to prevent cell trauma and damage and sample contamination. To complicate matters, a modern, standard method for reading and scoring microorganisms in aerobiological samples does not exist, making the interpretation and inter-comparison of results difficult.12  Finally, studies of atmospheric residence times (the lifetime of particles aloft in the atmosphere) for microorganisms and their dispersal patterns rely on computer simulations based on theoretical mathematical models that are difficult to correlate with experimental data.4,6,13  Such experimental design and engineering challenges explain why the upper atmosphere is one of the least explored biological environments on Earth, rivaling deep oceanic and subsurface environments.

Given the renewed interest in aerobiology and the inherent difficulties in aerobiological research, it should be of no surprise that the field is characterized by a remarkable lack of knowledge and a great deal of speculation. Some of the most important and fundamental questions regarding microorganisms in the atmosphere cannot be answered definitively and are active topics of debate. Undoubtedly, one of the more fundamental questions concerns the contributions of the atmosphere to the origin and evolution of microbial life. A complete account of this topic should include the evolutionary history of airborne microorganisms, the details of which have never been addressed to date. Another question central to aerobiology is whether the atmosphere can be considered a true habitat for airborne microorganisms. Several recent reports allude to the atmosphere as a habitat or ecosystem,14  especially in the case of microorganisms,6,15  but others argue that the debate is far from settled4,16  and subscribe to the more traditional point of view that the atmosphere is merely a conduit for dispersing microbes to distant locations. Other important problems in aerobiology have somewhat vague and tenuous answers simply because they are difficult to answer by experimentation. For microorganisms in particular, the most fundamental of these concern deriving realistic values for atmospheric residence times17  and understanding cosmopolitan dispersal by atmospheric transport (see, for example, Fröhlich-Nowoisky et al.,18  Wilkinson et al.13  or Smith et al.19 ). Atmospheric air is the primary medium for dispersing microorganisms across the globe and connecting all microbial habitats on the Earth’s surface, but it is not known whether the atmosphere contains biogeographic regions similar to those found on the Planet’s surface.6,18  We discuss the most recent research focused on establishing more concrete answers to these questions and, when appropriate, present our own speculation. Because the developmental history of the atmosphere is intimately related to microbial evolution and because some understanding of atmospheric structure is necessary to discuss aerobiology in detail, we begin by outlining this history and the Earth’s present-day atmosphere.

The processes by which the current atmosphere arose from earlier conditions are exceedingly complex; however, evidence related to these processes, although indirect, is abundant. Ancient sediments and rocks record the past changes in the atmospheric composition from chemical reactions within the crust, and also the evolutionary history of living systems. Several processes, including plate tectonics, weathering and photosynthesis, were internal to the Planet. However, extra-planetary processes such as the slowly and ever-increasing luminosity of the Sun over billions of years, gradual changes in the Earth’s orbit over many tens of thousands of years and the rare but catastrophic impacts of giant meteorites and comets, have also played important roles. Collectively, these factors have forged three distinct atmospheres for the Earth: an initial, tremendously hot atmosphere composed principally of H2 (hydrogen) and He (helium) gases, a second, rich in gaseous N2 (nitrogen) and CO2 (carbon dioxide), and today’s atmosphere, rich in gaseous N2 and O2 (oxygen).

The oldest materials ever found in the Solar System occur in meteorites ∼4.57 Ga (gigaannum or billion years ago) of age,20  marking the starting point for the condensation of the first solids in our Solar System. At this time, Earth was tremendously hot and inhospitable due to collisions and compressions of matter during accretion (the growth of a massive object by gravitationally attracting more and more matter, typically gaseous matter), heat released from the formation of an early planetary core and the ubiquitous, constant decay of radioactive elements. The Planet’s earliest surface was molten or a thin and unstable basaltic crust with constant volcanism. This was the birth of planet Earth and, as shown in Table 1.1, marked the start of geological time. Earth’s atmosphere likely consisted of gases captured from the solar nebula (the gaseous cloud from which the Sun and planets are believed to have formed by condensation)21–23  with H2, by far the most abundant element in the Universe, as its principal component. Other atmospheric gases most likely would have included He and simple hydrides such as those now found on Jupiter, Saturn, Uranus and Neptune, with CH4 (methane), NH3 (ammonia) and water vapor being the most notable. Details of the Earth’s primary atmosphere are very difficult to determine simply because there is very little evidence of the primary atmosphere left to investigate.24 

Table 1.1

Geological time scale

EonEraPeriodMillions of years before the present
Precambrian   4500–570 
 Archean  4500–2500 
  Hadean 4500–3900 
  Early Archean 3900–2900 
  Late Archean 2900–2500 
 Proterozoic  2500–570 
  Early Proterozoic 2500–1600 
  Middle Proterozoic 1600–900 
  Late Proterozoic 900–540 
Phanerozoic   570–present 
 Paleozoic  540–225 
  Cambrian 540–500 
  Ordovician 500–430 
  Silurian 430–395 
  Devonian 395–45 
  Carboniferous 345–280 
  Permian 280–225 
 Mesozoic  225–65 
  Triassic 225–190 
  Jurassic 190–136 
  Cretaceous 136–65 
 Cenozoic  65–present 
  Tertiary 65–1 
  Quaternary 1–present 
EonEraPeriodMillions of years before the present
Precambrian   4500–570 
 Archean  4500–2500 
  Hadean 4500–3900 
  Early Archean 3900–2900 
  Late Archean 2900–2500 
 Proterozoic  2500–570 
  Early Proterozoic 2500–1600 
  Middle Proterozoic 1600–900 
  Late Proterozoic 900–540 
Phanerozoic   570–present 
 Paleozoic  540–225 
  Cambrian 540–500 
  Ordovician 500–430 
  Silurian 430–395 
  Devonian 395–45 
  Carboniferous 345–280 
  Permian 280–225 
 Mesozoic  225–65 
  Triassic 225–190 
  Jurassic 190–136 
  Cretaceous 136–65 
 Cenozoic  65–present 
  Tertiary 65–1 
  Quaternary 1–present 

As the solar nebula began to dissipate, so too did the Earth’s primary atmosphere. Atmospheric gases escaped because the early Planet’s gravity was not strong enough to hold lighter gases. Gases were also driven off by the solar wind, a stream of plasma released from the upper atmosphere of the Sun containing high-energy electrons and protons. This was a consequence of the young, premature Planet not yet having a differentiated core (a solid inner and liquid outer core) to create a planetary magnetic field capable of deflecting the solar wind.24  Other events soon followed that profoundly changed the Planet and its atmosphere.

The loss of gases from the primary atmosphere was accompanied by a loss of the Planet’s primordial heat into space, the condensation of water as rain and its accumulation on the surface of the cooling Planet to form lakes, seas and oceans. The interaction of water, heat and rock set the stage for the origin of life. Once the Earth’s core differentiated, heavier gases were finally retained in the atmosphere, ultimately giving rise to the secondary atmosphere.

Earth’s secondary atmosphere first appeared at ∼4.5 Ga, soon after the Earth and Moon completed their formational phase, and was produced by out-gassing from volcanism together with gases produced during the late heavy bombardment of the Earth by huge asteroids.24  The gases constituting this atmosphere were probably similar to those created by modern volcanoes, likely including H2, water, CO (carbon monoxide), CO2, N2, S2 (sulfur), SO2 (sulfur dioxide) and Cl2 (chlorine). The secondary atmosphere was probably several times denser than the present atmosphere and almost certainly was dominated by CO2, a major greenhouse gas. A tremendous greenhouse effect must have accompanied this atmosphere, especially since the Sun was ∼30% dimmer at this time and supplied less solar radiation to warm the Planet.25,26  Such a warming effect would have been necessary to maintain water in a liquid state and ensure that Planet would not become a frozen wasteland without any hope for the earliest forms of life to take hold.27  With the exception of one cold glacial period phase at ∼2.4 Ga, the geological record reveals a warm surface during the Archean Era (the geological era 4.5–2.5 Ga and part of the Precambrian Supereon; see Table 1.1) suitable for sustaining life. Free O2 began to appear in the atmosphere late in the Archean, apparently produced by photosynthesizing cyanobacteria (referred to as the Great Oxygenation Event).

The evolution of an O2-rich atmosphere was intimately coupled to the evolutionary history of life. As the Planet’s biosphere and atmosphere co-evolved over the following billions of years, free O2 created from photosynthesis began to dominate the chemistry of the atmosphere. Some O2 was transformed into O3 (ozone) in a process using UV radiation from the Sun, and a slow but progressive accumulation of O3 began in the upper atmosphere. During this same period, the atmospheric concentration of free CO2 progressively decreased and stabilized at its present level. The decreasing CO2 levels appear to have been a response of the environment to the Sun’s steady increase in luminosity in order gradually to attenuate greenhouse warming at the same time. The carbon cycle, which contains both biological and geological processes, began early in the evolutionary history of life as living systems took over the production of organic matter and O2 began to regulate the balance of carbon between the atmosphere and the oceans. The cycle helped to regulate the Earth’s surface temperature by balancing the CO2 output from volcanoes and weathering and the burial of organic matter in sediments. Clearly, the evolution of life was central for creating the unique conditions for habitability on Earth; life regulates the global environment.28  As shown in Table 1.2, comparisons of the Earth’s atmosphere today with those of its nearest neighbors, Mars and Venus, illustrate this concept. Our nearest neighbor planets have negligible amounts of O2 in their atmospheres, both of which are dominated by CO2. This would have been the fate of the Earth’s atmosphere also if were not for life appearing and changing the atmosphere to keep the Planet habitable. Lastly, the constant rearrangement of continents by plate tectonics influenced the long-term evolution of the atmosphere by transferring CO2 to and from continental carbonate stores. The theoretical decrease in atmospheric CO2 levels over geological time, based on the model of Kasting,29  is illustrated in Figure 1.1.

Table 1.2

Atmospheric pressure and composition of the earth in comparison with its nearest planetary neighbors. Adapted from Mojzsis.27 

PlanetPressure/barCO2/% v/vN2/% v/v36Ar/% v/vH2O/% v/vO2/% v/v
Venus 92 96.5 3.5 0.00007 <0.00003 Trace 
Earth 1.013 0.033 78 0.01 <3 21 
Mars 0.006 95.3 2.7 0.016 <0.0001 Trace 
PlanetPressure/barCO2/% v/vN2/% v/v36Ar/% v/vH2O/% v/vO2/% v/v
Venus 92 96.5 3.5 0.00007 <0.00003 Trace 
Earth 1.013 0.033 78 0.01 <3 21 
Mars 0.006 95.3 2.7 0.016 <0.0001 Trace 
Figure 1.1

Estimated CO2 concentrations in Earth’s atmosphere over geological time in response to the steady increase in solar luminosity. The shaded areas represent the range in CO2 concentrations required to keep the Earth’s surface warm enough for liquid water to exist in the presence of the lower solar output. The figure starts ∼4.5 Ga with an ocean-covered Earth and a solar flux ∼30% lower than that today and extends to present-day conditions. Major glaciation periods are indicated, as is the rise in terrestrial plants and C3 photosynthesis (the most common type of photosynthesis where CO2 is first incorporated into 3-phosphoglycerate, a three-carbon or C3 compound). PAL is the present atmospheric level. Adapted from Kasting.29 

Figure 1.1

Estimated CO2 concentrations in Earth’s atmosphere over geological time in response to the steady increase in solar luminosity. The shaded areas represent the range in CO2 concentrations required to keep the Earth’s surface warm enough for liquid water to exist in the presence of the lower solar output. The figure starts ∼4.5 Ga with an ocean-covered Earth and a solar flux ∼30% lower than that today and extends to present-day conditions. Major glaciation periods are indicated, as is the rise in terrestrial plants and C3 photosynthesis (the most common type of photosynthesis where CO2 is first incorporated into 3-phosphoglycerate, a three-carbon or C3 compound). PAL is the present atmospheric level. Adapted from Kasting.29 

Close modal

Evidence from paleosols (ancient soils) and also a variety of other geologic evidence indicates that beginning ∼2.5 Ga ago, sedimentary rocks began to become increasingly affected by the rising concentrations of free atmospheric O2 and appeared red in color as if “rusted.” Resulting from the oxidation of iron in the rock, the “rusted” appearance is possible only in the presence of O2. Atmospheric O2 concentrations are believed to have increased rapidly at about this time as a consequence of more O2 being produced through photosynthesis than was consumed by chemical reactions within the atmosphere, oceans and rocks. A threshold O2 concentration was finally reached that transformed the earlier reducing atmosphere to an oxidizing atmosphere. At about the same time, more complex microbial life evolved in response to the higher O2 concentrations, including eukaryotes, and a powerful O3 screen began to form in the upper atmosphere when the atmospheric O2 level reached ∼1% of today’s level. The theoretical increase in atmospheric O2 levels over geological time according to the model of Kasting29  is shown in Figure 1.2.

Figure 1.2

Estimated free O2 concentrations in Earth’s atmosphere over geological time. The shaded areas represent the range of possible O2 concentrations from model calculations and investigations of paleosols (ancient soils), fossil organisms and marine sediments that only form in the absence of O2. The sediments are preserved as banded iron formations (BIFs) and only appear in the geological record up to ∼1.8 Ga. The point labeled Kruman BIF represents a lower limit for the partial pressure of O2 (pO2) based on a paleoweathering rate analysis (Hollard and Beukes, 1990). Solid vertical lines represent the most probable dates for transitions between three unique stages in the development of the atmosphere and ocean as O2 reservoirs:137  (I) the atmosphere and entire ocean were anoxic, with localized O2 oases in highly productive regions of the surface ocean, (II) the atmosphere and surface ocean were O2-rich and the deep ocean remained anoxic and (III) both the atmosphere and ocean were O2-rich. The dashed vertical line indicates an earlier date for the beginning of stage II consistent with redbed (sedimentary rocks appearing red from the presence of ferric oxides) data138  and the appearance of Grypania (a corkscrew-shaped organism from the Proterozoic era likely to have been a photosynthetic alga). The dashed horizontal lines represent the theoretical pO2 limits derived from the three-stage model. Additional constraints can be imposed on the upper pO2 limit during stage I when considering the survival of uraninite and other detrital grains139  that rapidly weather in the present-day atmosphere. The lower pO2 limits, labeled Dickinsonia and Charcoal, are from Runnegar140  and Jones and Chaloner,141  respectively. PAL is the present atmospheric level. Adapted from Kasting.29 

Figure 1.2

Estimated free O2 concentrations in Earth’s atmosphere over geological time. The shaded areas represent the range of possible O2 concentrations from model calculations and investigations of paleosols (ancient soils), fossil organisms and marine sediments that only form in the absence of O2. The sediments are preserved as banded iron formations (BIFs) and only appear in the geological record up to ∼1.8 Ga. The point labeled Kruman BIF represents a lower limit for the partial pressure of O2 (pO2) based on a paleoweathering rate analysis (Hollard and Beukes, 1990). Solid vertical lines represent the most probable dates for transitions between three unique stages in the development of the atmosphere and ocean as O2 reservoirs:137  (I) the atmosphere and entire ocean were anoxic, with localized O2 oases in highly productive regions of the surface ocean, (II) the atmosphere and surface ocean were O2-rich and the deep ocean remained anoxic and (III) both the atmosphere and ocean were O2-rich. The dashed vertical line indicates an earlier date for the beginning of stage II consistent with redbed (sedimentary rocks appearing red from the presence of ferric oxides) data138  and the appearance of Grypania (a corkscrew-shaped organism from the Proterozoic era likely to have been a photosynthetic alga). The dashed horizontal lines represent the theoretical pO2 limits derived from the three-stage model. Additional constraints can be imposed on the upper pO2 limit during stage I when considering the survival of uraninite and other detrital grains139  that rapidly weather in the present-day atmosphere. The lower pO2 limits, labeled Dickinsonia and Charcoal, are from Runnegar140  and Jones and Chaloner,141  respectively. PAL is the present atmospheric level. Adapted from Kasting.29 

Close modal

The chemical composition of the present-day atmosphere is shown in Table 1.2. Water vapor concentrations vary significantly from ∼10 parts per million by volume (ppmv) in the coldest regions of the atmosphere to as much as 50000 ppmv (5% by volume) in hot, humid air masses (the value in the table is an average value). Many substances of natural origin may be present as aerosols, including dusts of different mineral and organic compositions, pollens and spores, sea spray and volcanic ash. Various industrial pollutants may also be present as gases or aerosols, including chlorine (in both elemental Cl2 and molecular forms), fluorine compounds and elemental mercury vapor. Sulfur compounds such as H2S (hydrogen sulfide) and SO2 may be derived from natural sources or industrial air pollution.

In general, both air pressure and density decrease with increasing altitude in the atmosphere. Temperature, however, has a more complex relationship with altitude and may remain constant or even increase with altitude in some regions. However, because the relationship of temperature with altitude is generally constant and recognizable through measurements such as balloon soundings, temperature behavior provides a useful means to distinguish between atmospheric layers. Based exclusively on temperature, the atmosphere can be divided into five principal layers or atmospheric stratifications: the troposphere, stratosphere, mesosphere, thermosphere and exosphere. The order of these stratifications is illustrated schematically in Figure 1.3 along with the atmospheric temperature profile. Of these, only the troposphere, stratosphere and mesosphere are considered part of the biosphere30  and are relevant to aerobiology.

Figure 1.3

Schematic structure and temperature profile of the Earth’s atmosphere. The geometric height above sea level is shown in kilometers (km) and miles (mi). Temperature is shown in kelvin (K) and degrees Fahrenheit (deg F), while pressure is shown in millibars (mb). Illustrations of cumulonimbus and cirrus clouds, and also Mount Everest, are included as vertical scale references. The horizontal dashed line at 77 km represents the highest altitude at which living microorganisms have been found.30 

Figure 1.3

Schematic structure and temperature profile of the Earth’s atmosphere. The geometric height above sea level is shown in kilometers (km) and miles (mi). Temperature is shown in kelvin (K) and degrees Fahrenheit (deg F), while pressure is shown in millibars (mb). Illustrations of cumulonimbus and cirrus clouds, and also Mount Everest, are included as vertical scale references. The horizontal dashed line at 77 km represents the highest altitude at which living microorganisms have been found.30 

Close modal

The troposphere extends from the Earth’s surface to an average height of ∼12 km (∼40000 ft) ASL (above sea level), although it actually varies from ∼8 km (∼26000 ft) ASL at the Poles to ∼17 km (∼56000 ft) ASL at the Equator, with some local variations due to weather. This atmospheric stratification contains the Planet’s boundary layer (0–2 km or ∼0–6600 ft ASL), where air is heavily mixed with the surface by wind and weather systems to create vertical mixing. Temperatures typically decrease with increasing altitude in the troposphere (see Figure 1.3) because energy transfer from the surface provides most of the heating in this stratification, creating turbulence. The troposphere contains ∼80% of the entire mass of the Earth’s atmosphere and is denser than all overlying atmospheric stratifications. Nearly all atmospheric water vapor is found in the troposphere and, therefore, is where most all of the Planet’s weather occurs. It has virtually all weather-associated cloud genus types generated by active wind circulation, although very tall cumulonimbus thunderclouds can penetrate the tropopause, the troposphere–stratosphere boundary, from below and rise into the stratosphere. The troposphere is the most important stratification of the atmosphere in the study of aerobiology by an exceptionally considerable margin. Most conventional aviation occurs in the troposphere and it is the only atmospheric stratification that propeller-driven aircraft can access.

The stratosphere extends from the tropopause to an altitude of 50–55 km (∼160000–180000 ft) ASL and contains the O3 layer. Temperatures rise with increasing altitude in the stratosphere (see Figure 1.3) because the absorption of UV radiation by O3 releases heat. Although the temperature may be −60 °C (−76 °F) at the tropopause, the top of the stratosphere is much warmer, reaching up to ∼0 °C (32 °F) with a pressure ∼0.1% that at sea level. The stratospheric temperature profile creates very stable atmospheric conditions, so the atmospheric layer lacks the weather-producing air turbulence that is so prevalent in the troposphere. Consequently, the stratosphere is almost completely free of clouds and weather. Polar stratospheric or nacreous clouds, however, are occasionally seen in the lower extremities of this stratification where the air is coldest. This is the highest atmospheric stratification that can be accessed by jet-powered aircraft.

Finally, the mesosphere extends from the stratopause, the stratosphere–mesosphere boundary, to ∼80–85 km (∼260000–280000 ft) ASL. Within the mesosphere, temperatures decrease with increasing altitude right up to the mesopause, the boundary between the mesosphere and thermosphere (see Figure 1.3). The mesopause is the coldest place on Earth, with an average temperature ∼−85 °C (−120 °F),31,32  and is considered to be the upper boundary of the biosphere. The mesosphere is usually accessed by rocket-powered aircraft and unmanned sounding rockets.

As with any habitat, the atmosphere must provide conditions amenable to the living systems that it hosts. Many of the physical and chemical features of the atmosphere that most directly impact living organisms vary tremendously with latitude, longitude or altitude and both seasonal and weather effects can also dramatically change local conditions. The atmosphere, however, can be hospitable to microbial life, especially within the troposphere; this is illustrated in the case of temperature. As revealed in the atmospheric temperature profile in Figure 1.3 (and discussed above), temperatures decrease with increasing altitude in the troposphere, ranging from an average of 15 °C (59 °F) at sea level to ≥−60 °C at the tropopause, where they increase steadily with increasing altitude right up to the stratopause at ∼0 °C. Many microorganisms grow readily at these freezing temperatures,33  with some found to be metabolically active down to 18 °C (∼0 °F).5  Both pressure and air density decrease steadily with increasing altitude, with pressure ranging between ∼1 atm (0.987 bar) at sea level to >0.1 atm (0.00987 bar) in the lower mesosphere.

UV radiation (wavelengths of 100–400 nm) is one of the only physical characteristics of the atmosphere that increases directly with increasing altitude.34  With every 1000 m increase in altitude, UV levels generally increase by 10–20%, depending upon latitude, weather and both the time of day and year.35–38  Increased UV radiation at higher altitudes, however, does not necessarily represent greater UV exposures for airborne microorganisms in comparison with those for terrestrial organisms. In addition to the suite of DNA repair mechanisms found in all microorganisms,39  airborne microbes can adopt one or more additional measures for affording UV protection. For example, it has been suggested that airborne microorganisms may become embedded within larger particles having UV-reflecting or UV-protecting properties,11,40  and some UV-resistant bacterial strains readily form cell clumps or agglomerates.41  A correlation of pigmented microorganisms in the atmosphere with high levels of solar radiation42  indicates that microbes may also use pigments for UV protection.30,43  Protective mechanisms such as these are especially important in the upper stratosphere and mesosphere, where DNA-damaging UV-B (280–315 nm) and UV-C (100–280 nm) radiation is not attenuated by the O3 layer.44  The amount of cosmic radiation also increases directly with increasing altitude,45  but is much less effective in producing biological damage than UV radiation.46 

Finally, the hydrogen ion (H+) concentrations found in clouds and rainwater fall in an acidic range between pH 3 and 7,47  which is a narrower range than that found in other microbial habitats. The acidic conditions are the result of gases and compounds from aerosols dissolving into cloud water, which varies with their underlying terrestrial sources.48  Microorganisms in general have adapted to survive a significantly broader range of H+ concentrations, from extremely acidic conditions of pH ∼049  to highly alkaline conditions of pH ≥ 11.50 

As a habitat, the atmosphere must also be able to provide nutrients for its heterotrophic life forms. Most of these nutrients are found in the troposphere, carried by water in the form of clouds and rain. For example, concentrations of sulfate and nitrate nutrients in cloud water and rainwater reach levels typically found in oligotrophic lakes.40  Several potential carbon sources are found in clouds and tropospheric air, including carboxylic acids and alcohols at concentrations ≤1 mg L−1, (see Section 1.3.2) and a variety of hydrocarbons at concentrations ≤4 ng L−1.47 

Despite considerable deficiencies in our current understanding of atmospheric ecology, the wealth of information provided by geological records, fossil records and paleobiology in general can be used as a foundation for speculation about the evolutionary history of atmospheric life. At least provisionally, and in the broadest of terms, we outline this history below, framing it around the Precambrian Supereon between 4.6 Ga and 541 Ma (megaannum or million years ago; see Table 1.1), as it accounts for 88% of all geological time and encompasses all of the early evolutionary events leading to prokaryotic and eukaryotic life forms, the colonization of land by living systems and the evolution of an O2-rich atmosphere, among other important events. The Supereon literally was the age of microbes, macroscopically expressed in colonial structures referred to as stromatolites. A photograph of an ancient fossil stromatolite, and also examples of living extant stromatolites, are shown in Figure 1.4. The structures are ubiquitous throughout the fossil record of the Precambrian, but are rare today. Except for phylogenetic determinations from conserved DNA sequences and some subtle molecular fossils, stromatolite fossils remain the only visual portal into the very early history of Precambrian life.

Figure 1.4

Photographs of (a) an ancient, fossilized stromatolite from the Strelley Pool chert in Western Australia formed ≥3.4 Ga and (b) modern living stromatolites from Shark Bay, Western Australia. Stromatolites are layered biochemical accretionary structures formed in shallow water by the trapping, binding and cementation of sedimentary grains by biofilms (microbial mats) of microorganisms. The stromatolite fossil in (a) dates back to the Precambrian age. Photograph (a) from Hallmann142  and (b) from Caldicott.143 

Figure 1.4

Photographs of (a) an ancient, fossilized stromatolite from the Strelley Pool chert in Western Australia formed ≥3.4 Ga and (b) modern living stromatolites from Shark Bay, Western Australia. Stromatolites are layered biochemical accretionary structures formed in shallow water by the trapping, binding and cementation of sedimentary grains by biofilms (microbial mats) of microorganisms. The stromatolite fossil in (a) dates back to the Precambrian age. Photograph (a) from Hallmann142  and (b) from Caldicott.143 

Close modal

Life began sometime during the Early Precambrian, the broad expanse of time starting with the formation of the Earth ∼4.6 Ga and extending over 2 billion years to 2.5 Ga. The oldest reported fossils, those discovered in the Strelley Pool Formation of Western Australia, date back 3.5–3.4 Ga and provide some idea of Early Precambrian living systems. Sedimentary rocks from the Strelley Pool Formation contain what appear to be fossil stromatolites.51–53  Microscopic forms reminiscent of bacteria can be observed within the stromatolites, indicating that if the primitive bacteria-like cells are direct ancestors of extant photosynthetic bacteria, life was already well developed at that time54  and free O2 was being added to the atmosphere on a continuous basis (see Figure 1.2). Other evidence indicates that the divergence between bacteria and archaea also occurred at about this time,55  marking the end of the last universal common ancestor.56  In general terms, it appears that the evolutionary process was well under way for microbial life during the Early Precambrian. The prevailing biota at this time consisted of primitive, unicellular prokaryotic microorganisms of limited biological diversity and relatively little morphological complexity.57  Bacteria and blue-green algae appear to have constituted a significant part of this biota, occurring earliest as isolated cells and somewhat later as components of stromatological communities. Chemical analyses of shale formations from Western Australia suggest that bacterial life migrated from the oceans onto land towards the close of the Early Precambrian at ∼2.75 Ga.58  Other evidence of terrestrial life at roughly the same time has been discovered in organic matter-rich fossilized soil59  and small, isolated wetlands that periodically became dry on a regular basis.60  This latter environment and other, shallow, aquatic environments that periodically exposed their microbial inhabitants to desiccated conditions due to changing tides, currents or evaporating water are believed to be the ancient venues where aquatic microbes first developed adaptations necessary for colonizing land.61  The periodic desiccation allowed microbial dispersion by wind and weather from these sub-aerial habitats, affording a practical mechanism for land colonization. Because fossil records place the colonization of land towards the close of the Early Precambrian, it is likely that some of the unsophisticated microorganisms at this time were just beginning to adapt for surviving sub-aerial habitats. Such adaptations probably did not become common in microbial populations until roughly the start of the Middle Precambrian.

Careful examination of early fossils lends support to the idea that microbial dispersal through the airspace, in all likelihood, occurred even during the Early Precambrian. Microfossils observed in sedimentary rocks formed during this period often reveal bacteria-like cells of sizes similar to those of extant microorganisms believed to have atmospheric residence times of ∼1 week (see Section 1.4.2). Electron micrographs of such rocks from South Africa dating to ∼3.1 Ga, for instance, contain what appear to be ancient bacterial cells that are spherical and ≪0.5 µm in diameter, rod-shaped cells ∼0.2 µm in diameter and ∼0.6 µm long, and other, rod-shaped cells ∼0.3 µm in diameter and ∼7.0 µm long.57,62  Optical photomicrographs of thin sections prepared from other sedimentary rocks from this same formation show algal-like microfossils 10–20 µm in diameter.63  Also, spiny, spherical acritarchs (small, non-acid-soluble organic structures that cannot be positively categorized) appearing 1–2 µm in diameter have been identified in electron micrographs of >2.7 Ga sedimentary rocks from Zimbabwe.57  It is not difficult to conclude that these small organisms became lofted into the Early Precambrian atmosphere, not unlike extant microorganisms that become lofted into the atmosphere today. This is especially the case when considering the 300 m (∼1000 ft) tides believed to have occurred during this time, a consequence of the Moon being much closer to the Earth than today. On the other hand, it is difficult to imagine that these organisms could have survived in the atmosphere for any significant length of time, at least for most of the Early Precambrian. Living systems were entirely aquatic and unsophisticated for essentially all of the Early Precambrian and most likely not vigorous or robust enough to survive anywhere but in their native aquatic environments. Moreover, the absence of a well-formed O3 layer would only add to the difficulties of survival in the atmosphere due to severe UV exposure. Additional complications for airborne survival during the Early Precambrian include (1) the increasing poisonous effect from free O2 on many bacteria as a result of its increasing atmospheric concentrations starting ∼3.5 Ga (see Figure 1.2) and (2) the ravages of the atmosphere’s recurring desiccant conditions on the aquatic-derived living systems. The Early Precambrian atmosphere must have been a very inhospitable environment for the primitive living systems of the time.

The best-known and most significant microfossil assemblage of the Middle Precambrian has been organically preserved in sedimentary rocks formed ∼2 Ga in the Gunflint Iron Formation64,65  of Ontario, Canada. Gunflint microfossils are diverse and abundant and typically resemble extant bacteria.66–68  These microfossils, and several others, indicate that during the Middle Precambrian between 2.5 and 1.7 Ga, stromatological algal communities flourished in shallow seas, estuaries and other littoral environments (areas of a lake, river or sea close to shore) on a global scale and planktonic algae were abundant locally. For most of the Middle Precambrian, the Planet’s biota was composed entirely of prokaryotic organisms, including members of several extant cyanophycean families, including Chroococcaceae, Nostocaceae, Oscillatoriaceae and a variety of chemosynthetic bacteria. Other taxa of less certain biological relationships were also represented; however, it is not known whether these organisms were prokaryotic, eukaryotic or somehow intermediate in cellular organization.57  Many microfossils indicate that eukaryotic cells first appeared at the close of the Middle Precambrian ∼1.85 Ga,69  derived from prokaryotic cells engulfing each other by phagocytosis to form new cells with membrane-bound organelles of diverse functions existing in symbiotic relationships. The Middle Precambrian environment was oxygenic70  on a global scale (see Figure 1.2), favoring the spread of the new eukaryotic life forms.

Evidence for the bacterial colonization of land ∼2.75 Ga58–60  carries profound implications for living systems around the turn of the Middle Precambrian. In particular, the primitive prokaryotic life forms so prevalent during the Early Precambrian must have developed reasonably high levels of vigor and robustness in order to migrate from their natural aquatic habitats on to dry land and not just survive after landfall, but also thrive. As mentioned previously, some of the most essential features for such robustness, especially tolerances against (1) an O2-containing atmosphere, (2) strong UV radiation and (3) recurring desiccant conditions, are also central for survival in the atmosphere. Bearing this in mind, it becomes straightforward to conclude that the bacterial life forms at the time must have been able to endure at least short excursions into the atmosphere. Although it is likely that most bacterial cells lofted into the atmosphere did not return to the surface alive days or even hours later, the return of living cells to the surface ultimately became possible, providing a completely new mechanism for introducing novel genes into distant gene pools. Microbial life in the atmosphere may well have had its origins in the Middle Precambrian, involving mostly prokaryotic organisms, if not entirely. However, it is difficult to understand how long their newly developed vigor and robustness could keep the prokaryotic life forms alive in the atmosphere. Water and nutrients could have been found within clouds, but the stratosphere still did not have a well-developed O3 layer to absorb harmful UV radiation. The one obvious conclusion that can be drawn from the colonization of land is that it would have allowed microorganisms to enter the atmosphere directly from land for the first time, supplementing their already established lofting into the atmosphere from sea spray.1  Because land-to-air lofting of microbial particles is more efficient than ocean-to-air lofting,1,18  the new lofting mechanism had the potential to increase appreciably the numbers and density of microorganisms in the Middle Precambrian atmosphere. However, terrestrial life is not believed to have been very pervasive at this time, leaving the Middle Precambrian landmasses barren and sterile.71–75  This point of view is not universally accepted, however, as some believe that terrestrial microbes could have existed in substantial numbers at this time.61 

The Late Precambrian, between 1.7 Ga and 541 Ma, appears to be a time of increasing complexity and diversity for microbial life. The fossil record demonstrates that stromatological communities reached their greatest numbers ∼1.25 Ga76  and subsequently declined in both abundance and diversity,77  so that by the end of the Precambrian age, they had fallen to just ∼20% of these numbers. The Late Precambrian featured diverse assemblages of prokaryotic and eukaryotic microorganisms, some of which are morphologically similar to extant taxa.57  Filamentous and coccoid blue-green algae were the dominant organisms in widespread biohermal (a mound of material laid down by marine organisms) communities and stromatolites also contained nucleated algae. Sometime ∼1.2 Ga, mitotic algae began to supplant the prokaryotic microorganisms that dominated the Early and Middle Precambrian. Eukaryotic algae gave rise to unicellular life forms during the Late Precambrian and the transition to multicellular organization occurred sometime between 1.2 Ga and 700 Ma. The constant, long accumulation of atmospheric O2 finally culminated into a well-established O3 layer ∼600 Ma,78  greatly facilitating the colonization of land by living systems. There is some fossil evidence that fungi existed during this period, but identification of these fossils is far from certain. On the other hand, DNA analysis indicates that the earliest fungi appeared just before the end of the Precambrian period ∼570 Ma.79 

It is evident that the developing complexity of microorganisms during the Late Precambrian included a further evolution of the robustness that permitted their survival on dry land and in the atmosphere. Relative to earlier living systems, Late Precambrian microorganisms almost certainly experienced improved survivability and diversity in the atmosphere, ultimately leading to larger numbers of living microorganisms aloft. For the first time in evolutionary history, prokaryotic and eukaryotic cells could coexist in the atmosphere. The rise of eukaryotes introduced sexual reproduction, enabling both genetic diversity and an enhanced ability to adapt to and survive in new or changing environments. This is particularly important because the increased atmospheric survivability would have increased the introduction of new genes into distant gene pools by aerial dispersal. The biocidal effects from UV radiation attenuated steadily with the development of the O3 layer throughout the Late Precambrian and the lofting of land-based microorganisms into the atmosphere became increasingly more common. The exact numbers of airborne microorganisms originating from landmasses in comparison with those from aquatic environments is difficult to determine, especially because evidence of early terrestrial microorganisms is rare.61  Although the overwhelming opinion is that Late Precambrian landmasses were still relatively barren and sterile,71–75  life must have become more established on land and more prevalent in the atmosphere as the dawn of the Cambrian grew increasingly closer.

Starting from ∼540 Ma, the Cambrian period (see Table 1.1) marked an extraordinary change for life on Earth. Although complex, multicellular organisms gradually became more common in the millions of years immediately preceding the Cambrian,80  a rapid and explosive diversification of life forms during this period produced the first representatives of all modern animal phyla. The age of microbes had come to an end, but microbial evolution was still an ongoing process. In terms of atmospheric life and survivability, both prokaryotic and eukaryotic organisms just might have come into their own during this time. Since the start of the Cambrian, both organisms became increasingly more diversified and established, with some becoming well suited for terrestrial life. Ultimately, these terrestrial life forms grew to be pervasive on land and flourished. There is an analogous story to tell about the evolutionary history of bacteria and fungi in the atmosphere. However, the timeline of this story is not clear because, unlike the case of terrestrial life, it cannot be extrapolated from the fossil record. However, when considering the tremendous diversity and pervasiveness of bacteria and fungi in the atmosphere today,81  it is apparent that their robustness and vigor for surviving excursions into the atmosphere and the diversity of microbial life in the airspace continued to evolve and become more sophisticated in the ∼540 Ma since the dawn of the Cambrian.

There has been some speculation regarding the extreme environmental conditions in the atmosphere and their influences on the origin and evolutionary history of life. Dobson et al.82  hypothesized that organic aerosols may have acted as pre-biotic chemical reactors during the start of the Precambrian that ultimately gave rise to primitive living cells; the general concept of their hypothesis is illustrated in Figure 1.5. Smith4  suggested that when microorganisms were first able to survive extended excursions into the atmosphere, time aloft could have accelerated the processes of natural selection and speciation by imposing unique combinations of stresses on microorganisms that cannot be found anywhere else. Longer residence times increase the impact of atmospheric stress on airborne species, especially cellular damage from desiccation and UV radiation. The suggestion has led to two opposing hypotheses concerning microbial evolution and survival in the atmosphere.4  One is that microorganisms have developed adaptations for quickly returning to the surface after billions of years of drifting perilously through the atmosphere. Examples of such adaptations include membranes that promote cloud and ice condensation and cell aggregation mechanisms to reduce residence times. On the other hand, some microorganisms could have evolved cloud condensation adaptations to collect water and nutrients to metabolize while airborne. The latter hypothesis is consistent with large number of reports on the metabolic activities of airborne bacterial and fungal strains (discussed immediately below). There have also been reports addressing potential stratospheric contributions to evolution.19,41,83,84  Wainwright et al.84  proposed that the lofting of microorganisms into the stratosphere particularly accelerates the process of evolution. Microorganisms that are mutated and not killed by exposure to stratospheric UV radiation will ultimately return to Earth, many with one or more novel mutations. When introduced into soil-derived gene pools, these mutations will increase the numbers and diversities of mutations available for natural selection. As a result, the rate of microbial evolution will have been greater than that without stratospheric influence.

Figure 1.5

Schematic representation of an organic aerosol particle (top) and a sequence of five events leading to the formation of stable vesicle in the Precambrian Ocean (bottom). The five events illustrated are the following: (1) the formation of an aerosol particle with a surfactant partial monolayer at the ocean surface, (2) its exposure to sunlight while airborne, which drives the evaporation of water from its interior to produce a complete monolayer, (3) its inevitable fallout from the atmosphere, (4) re-entry at the ocean surface and (5) acquisition of a second layer of surfactant to permit survivability in the ocean as a stable vesicle. The ocean surface acts as a global scale concentrator of surfactants, which have their polar groups in the water and their hydrocarbon chains in the air. Very large numbers of this repetitive process would have to have occurred for life to originate from the vesicles. Adapted from Dobson et al.82 

Figure 1.5

Schematic representation of an organic aerosol particle (top) and a sequence of five events leading to the formation of stable vesicle in the Precambrian Ocean (bottom). The five events illustrated are the following: (1) the formation of an aerosol particle with a surfactant partial monolayer at the ocean surface, (2) its exposure to sunlight while airborne, which drives the evaporation of water from its interior to produce a complete monolayer, (3) its inevitable fallout from the atmosphere, (4) re-entry at the ocean surface and (5) acquisition of a second layer of surfactant to permit survivability in the ocean as a stable vesicle. The ocean surface acts as a global scale concentrator of surfactants, which have their polar groups in the water and their hydrocarbon chains in the air. Very large numbers of this repetitive process would have to have occurred for life to originate from the vesicles. Adapted from Dobson et al.82 

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There is a long-standing preconception in ecology that both landmasses and bodies of water constitute habitats for living systems whereas the atmosphere does not. Early definitions of habitat focused sharply on species occupancy85,86 , but later definitions also included the survival and reproduction of the species.87  Consistent with the latter definition, Green and co-workers6  argued that the true “residents” of the atmosphere are airborne microorganisms that are active metabolically and reproductively. While this can include bacteria, archaea and fungi (including yeasts and molds), it explicitly eliminates viruses, spores and other inactive propagules that are not metabolically active, and also organisms such as birds and insects that are metabolically active, but not reproductively active, when airborne.

Similarities can be drawn between the atmosphere and other environments, especially ocean environments. Physically, both are fluid environments with currents (horizontal fluid movement) and eddies (swirling of fluid) that are influenced by locations, topographies and seasons. Environmentally, both contain microorganisms that are transported by the currents and eddies. Such transport through the atmosphere is the simplest means of accounting for the global distribution of many microbial species,88  and some have suggested that the currents and eddies associated with this transport can give rise to biogeographic regions in the atmosphere analogous to those found on the Earth’s surface.

The atmosphere is literally teeming with living microorganisms; however, direct in situ measurements of their metabolic activities while airborne are tremendously difficult to carry out. This has restricted research on the subject primarily to experimental, culture-based approaches conducted in laboratory settings. The first such investigation was reported in 1975, with Dimmick et al.89  revealing that aerosolized bacteria are capable of glucose metabolism. Over the next 4 years, the same group demonstrated that aerosolized bacteria incorporate thymidine into their DNA90  and are also capable of cell division.91,92 

Most culture-based studies addressing the metabolic activities of microorganisms in the atmosphere involve isolating bacteria or yeast from cloud water, rainwater, snow or ambient air specifically for laboratory testing. In 1987, a report by Herlihy et al.93  presented evidence for the metabolic degradation of both formic and acetic acid by bacteria isolated from rainwater, and others have reported similar findings.94  Fifteen years later, Amyot and co-workers95  presented strong evidence that airborne bacteria and fungi existing in the tropospheric boundary layer can efficiently degrade dicarboxylic acids and use them as nutrients. The same group also reported a wide range of variation in degradation lifetimes for dicarboxylic acids as a result of the microbial taxon under investigation, and also other factors such as H+ concentration and temperature.96  Other investigators97,98  revealed that bacterial activity could occur in rainwater held at sub-freezing temperatures.

Delort’s group have reported numerous investigations of bacteria and yeast strains isolated from cloud water samples collected at the Puy de Dôme station (a reference site of the European Aerosols, Clouds and Trace Gases Research Infrastructure Network at 1465 m or 4086 ft ASL). Their first investigation99  found that of a total of 17 bacterial strains isolated from Puy de Dôme cloud events, most were able to degrade various organic compounds, such as formate, acetate, lactate, methanol and formaldehyde, the major organic compounds commonly found in cloud water. This study was extended to include 60 total strains of bacteria and yeasts isolated from the cloud water samples and included succinate as an additional test compound.100  The extended study revealed that (1) all the compounds could be biodegraded when used as a single carbonaceous substrate, with activities dependent upon both the microbial strain and test compound, and (2) formaldehyde could be biodegraded through many different metabolic pathways, leading to the production of formate and/or methanol. In a somewhat related study,101  ATP concentrations measured in cloud water samples from 14 independent cloud events indicated that a significant fraction of the microorganisms present in clouds are metabolically active. Subsequently, Vaïtilingom et al.102  found that four bacterial strains and a single yeast strain isolated from Puy de Dôme clouds degraded formate, acetate and succinate when cultured in simulated cloud water at 5 and 17 °C (41.0 and 62.6 °F), temperatures representative of the clouds in winter and summer, respectively. The bacteria and yeast strains in the study were also found to have lifetimes ranging between 0.6 and 69.1 days at the two temperatures. These results suggest that biological activity alone drives 90–99% of the oxidation of carbonaceous compounds at night, and during the day, when competing with photochemistry,103,104  biological activity contributes only 2–37% of the total reactivity. A year later, Vaïtilingom et al.105  examined the contributions of photochemistry and microbial activity to the degradation of atmospheric carboxylic acids, again using bacterial strains from Puy de Dôme cloud water. Their major conclusions were that (1) some test compounds could only be photodegraded, others only biodegraded and the remainder could be degraded by both mechanisms, (2) the biodegradation rates did not decrease drastically when incubation temperatures decreased from 17 to 5 °C and (3) all the observed biodegradation rates, even those at 5 °C, are competitive with measured and calculated photodegradation rates. Around the same time, Husárová et al.106  reported that bacterial strains isolated from Puy de Dôme clouds degraded methanol and formaldehyde at 5 and 17 °C and the observed biodegradation rates were within the same range of magnitude as those from free radical chemistry. The most recent report from Vaïtilingom et al.107  investigating microorganisms from Puy de Dôme cloud water revealed that (1) cloud microorganisms remain metabolically active in the presence of ˙OH radicals photo-produced from H2O2 (reactive oxygenated species such as H2O2 and free radicals are found in clouds) and (2) cloud microorganisms can metabolize H2O2 to O2 and H2O using catalases. Lastly, Durand et al.108  reported the first pure bacterial strain capable of rapidly degrading the herbicide mesotrione, which was also isolated from Puy de Dôme cloud samples.

Considered collectively, the culture-based investigations present overwhelming evidence that microorganisms from atmospheric habitats are remarkably capable of metabolic activity. This conclusion is substantiated by the results of Sattler et al.109  and Hill et al.,110  from direct observation of pure, unadulterated cloud water. Sattler et al.109  showed that the microorganisms present in cloud water held at 0 °C (32 °F) incorporated thymidine into their DNA at (1.1–4.8) × 10−15 mol L−1 h−1 and are also capable of reproduction. The results of Hill et al.110  demonstrated the processing of atmospheric nitrogen by cloud water and also found that 76% of the bacterial cells in their cloud water samples absorbed and reduced the dye 5-cyano-2,3-ditolyltetrazolium chloride, indicating that most of the cells in the samples were living and capable of metabolic activity. There now appears to be a general consensus taking shape that although microbial metabolic activity has never been directly measured in the atmosphere in situ, at least some microorganisms in the troposphere must be metabolically active. Vaïtilingom et al.107  estimated that microorganisms in clouds metabolize the release of (51–215) × 106 tons of CO2 each year on a global scale.

In striking contrast to the case of metabolic activity, studies of microbial reproduction in the atmosphere are severely limited, with only three reported over the last 35 years.91,92,109  To complicate matters, determining whether microorganisms reproduce while airborne has relied on considering their atmospheric residence times, as they might be the principal factor limiting microorganism reproduction while airborne.17,109  In a theoretical sense, and to a first approximation, residence times for microorganisms are inversely proportional to the sizes of the particles they form when airborne, but other factors, including air temperature, relative humidity, wind and weather conditions, can contribute significantly to residence time values.17,40,111  Residence times, however, cannot be measured in situ with contemporary technologies and, therefore, are computed from virtual simulations of particle transport. Table 1.3 summarizes data from three very different simulations modeling particles as rigid spheres between 0.7 and 60.0 µm in diameter.13,17,111  Considerable variation can be seen in the table, revealed by the broad ranges of residence times for any single sphere diameter, and also the very different ranges between similar sphere diameters reported from different references such as those for the 1.0 and 1.1 µm sphere diameters. The broad nature of any one reported range is a consequence of the different conditions used for any single simulation protocol. Burrows et al.,17  for example, conducted simulations for 10 different ecosystems (costal, desert, grassland, etc.) under conditions that explicitly included or eliminated cloud condensation nucleation events to generate a total of 20 unique residence times. The variations between similar sphere diameters from different references are largely a result of their different simulation protocols. In a more general sense, the variations in the table illustrate the complexities of deriving accurate and realistic residence time values from computational approaches.

Table 1.3

Summary atmospheric residence times for 0.7–9.0 µm diameter spheres derived from virtual simulations

Sphere diameter/µmResidence time/daysReference
RangeAverageNo. of values
0.7 0.7–6.0 3.9 Williams et al.111  
0.9 0.7–6.0 2.9 Williams et al.111  
1.0 3.8–14.4 7.6 20 Burrows et al.17  
1.1 0.6–5.0 2.9 Williams et al.111  
1.4 0.6–5.0 2.8 Williams et al.111  
1.8 0.5–3.0 1.2 Williams et al.111  
3.0 2.2–10.8 5.8 20 Burrows et al.17  
9.0 2.2–57.0 13.9 12 Wilkinson et al.13  
20.0 0.6–12.8 4.5 12 Wilkinson et al.13  
40.0 0.1–9.8 2.3 12 Wilkinson et al.13  
60.0 0.03–9.0 2.0 12 Wilkinson et al.13  
Sphere diameter/µmResidence time/daysReference
RangeAverageNo. of values
0.7 0.7–6.0 3.9 Williams et al.111  
0.9 0.7–6.0 2.9 Williams et al.111  
1.0 3.8–14.4 7.6 20 Burrows et al.17  
1.1 0.6–5.0 2.9 Williams et al.111  
1.4 0.6–5.0 2.8 Williams et al.111  
1.8 0.5–3.0 1.2 Williams et al.111  
3.0 2.2–10.8 5.8 20 Burrows et al.17  
9.0 2.2–57.0 13.9 12 Wilkinson et al.13  
20.0 0.6–12.8 4.5 12 Wilkinson et al.13  
40.0 0.1–9.8 2.3 12 Wilkinson et al.13  
60.0 0.03–9.0 2.0 12 Wilkinson et al.13  

Notwithstanding these shortcomings, Table 1.3 can be used to arrive at meaningful conclusions about airborne microorganisms by relating their values to those of naturally occurring microbes in the atmosphere. Airborne bacteria can occur as individual cells but are more likely to be attached to other particles, including soil or plant fragments, or agglomerated with other bacterial cells.11,41  Whereas individual bacterial cells are ≤1 µm in diameter,112  the median diameter of airborne particles containing bacteria has been reported to be somewhere between 2 and 4 µm.17,113–116  In Table 1.3, therefore, sphere diameters between 0.7 and 3.0 µm can be considered to represent airborne bacteria and the 3.0 µm diameter can also be used to represent fungal spores in the airspace.116  The diameters in Table 1.3 between 20 and 60 µm were specifically chosen to model eukaryotic microbes,13  such as testate amoebae.117,118 

Using generation times measured for bacteria, Table 1.3 can be used to evaluate the likelihood of bacterial reproduction in the atmosphere. The most relevant data for this type of evaluation are probably those of Sattler et al.109  using cloud water collected at 3106 m (10190 ft) and temperatures of −4 and −9 °C (24.8 and 15.8 °F, respectively). Bacterial generation times were measured by culturing the cloud water at 0 °C and counting the numbers of bacterial cells over time. Ten different generation times ranging between 3.6 and 19.5 d were reported, with an average value of 10.9 d. In Table 1.3, residence times for sphere diameters between 1.0 and 3.0 µm range between 0.5 and 14.4 d with average values between 1.2 and 7.6 d. Extrapolating from the overlap between the lower range in generation times (about one new generation every 4–5 d) and the upper range of residence times (∼10–14 d), it is conceivable that at least some microorganisms could divide while aloft in the atmosphere. More specifically, the extrapolation indicates that bacterial excursions into the atmosphere could possibly include one or two cell divisions and occurrences of more divisions for a single bacterial excursion are rare. The fact that the residence and generation times do not completely overlap implies that significant numbers of bacterial excursions into the atmosphere, if not most of them, do not involve bacterial reproduction. Others1,119  using the generation time values have arrived at similar conclusions, but based their extrapolations on data suggesting that bacterial cells spend an average of only 5–6% of their time aloft inside cloud droplets120  where nutrients are available. Without more investigations, these conclusions should be considered as speculative and preliminary.

As with all particles in the atmosphere, microorganisms are consistently moving through its three-dimensional airspace. The movement is the resultant sum of two different types of motions, vertical and horizontal motion, each driven by very different mechanisms. Vertical motion includes the lofting of particles into the atmosphere and their inevitable fallout back to the surface, whereas horizontal motion, that along the east–west and north–south dimensions in atmospheric space, gives rise to particle dispersal. In a general sense, these motions do not occur separately as isolated events, but tend to be inter-related to varying extents depending largely on local conditions. Particles must first be lofted high into the atmosphere, for example, for their dispersal over appreciable distances such as across oceans or continents,4,83,121,122  and dispersal distances can be considerably enhanced by local storms or hurricanes. Particle lofting occurs mostly within the troposphere and particularly in the boundary layer, where wind, weather and solar heating of the Earth’s surface cause substantial mixing between the surface and the airspace. Surface heating causes warm air masses to form near the surface, which cool as they rise, and then fall back to the surface to be warmed again, leading to vertical mixing or convection, of atmospheric gases. The collective result of convection is the lofting of aerosol particles such as dust, smog, smoke, insects, pollen and microorganisms, with most of the microorganisms deriving from arid topsoil and marine sea spray.1,6,18,123  In addition to naturally occurring environments, bacteria may become lofted into the atmosphere from man-made point sources such as landfills, wastewater treatment facilities, farms and also construction sites, the last from the disturbance of settled dust. Airborne microorganisms and other particles fall out of the atmosphere by gravitational settling and both ice nucleation119  and cloud condensation nucleation.124 

The tropopause is thought to act as a barrier to the vertical motion of particles, but microorganisms routinely reach into the stratosphere4,41,83,84  and even the mesosphere.30  Observations such as these have driven much speculation about mechanisms that can rationalize the presence of microbes above the tropopause. Some mechanisms proposed in recent decades include strong upward winds,83,84  thunderstorms125  and blue lightning strikes,126  hurricanes127  and monsoons,128  stratosphere–troposphere exchange by deep convection in the tropics,129  electrostatic levitation,130  volcanic eruptions131  and commercial aviation. The US Bureau of Transportation Statistics132  estimates that the US airline industry alone sends ∼800000 domestic and commercial international flights into the upper atmosphere every month, with each aircraft shedding countless microorganisms into the upper troposphere and lower stratosphere.

The horizontal movement of particles through the airspace is a consequence of atmospheric circulation occurring on a global scale. Patterns for atmospheric circulation vary somewhat from year to year due to mid-latitude depressions, tropical convective cells and other individual weather systems; however, the forces driving the circulation are always acting on the airspace and their patterns are stable over longer periods of time. The patterns are a fundamental property of the Earth’s size, rotation rate, atmospheric depth and the solar heating of its surface. In the absence of thermal energy from the Sun, the Earth would be a wind-less planet. Solar energy heats the Planet’s surface, but the heating is never even across the surface and convection cell systems form in the atmosphere. The Earth’s latitudinal convection cell systems are shown schematically in Figure 1.6, which reveals three unique cell system types: Hadley cells (named after George Hadley, who first proposed the convection cell to explain the trade winds), mid-latitude cells or Ferrel cells (named after the meteorologist William Ferrel, who first proposed their existence) and Polar cells, with one of each type found in both hemispheres.

Figure 1.6

Schematic representation of the Earth’s global circulation. The parallels at 30 and 60° north (N) and south (S) of the Equator (0°) are shown. Violet lines labeled “HIGH” are areas of high atmospheric pressure. Adapted from NASA.144 

Figure 1.6

Schematic representation of the Earth’s global circulation. The parallels at 30 and 60° north (N) and south (S) of the Equator (0°) are shown. Violet lines labeled “HIGH” are areas of high atmospheric pressure. Adapted from NASA.144 

Close modal

The atmospheric circulation patterns first described by George Hadley for the tropics (latitudes within ∼30° north and south of the Equator) agree well with the trade winds observed in the region. The Hadley cell systems are closed-loop circulations driven largely by surface heating near the Equator in the ITCZ (intertropical convergence zone), where solar radiation is most intense. This causes the heated air to rise vertically towards the tropopause, creating an area of low pressure at the ITCZ. Because the environmental lapse rate changes from positive to negative (the variation in air temperature changes from decreasing to increasing with height; see Figure 1.3) at the tropopause, it acts as a ceiling and diverts much of the rising air horizontally in a either northerly or southerly direction. The air moving in a northerly direction just below the tropopause becomes part of the Hadley circulation in the Northern Hemisphere, while its southerly-moving counterpart becomes part of the Hadley circulation in the Southern Hemisphere. For both hemispheres, the air circulating towards the Poles constantly decreases in temperature and concomitantly increases in density, causing the tropopause to decrease in altitude at the same time; this is illustrated schematically in Figure 1.7a. The tropopause is ∼15 km (∼9 mi) ASL at the ITCZ but reaches only ∼10 km (∼6 mi) ASL at about the 30th parallel N/S (latitudes of 30° north and south), creating a “downhill” effect that accelerates the air moving towards the Poles. At the same time, the circulating air experiences a Coriolis force that deflects its northerly or southerly progression eastwards, a consequence of the nearly spherical Earth rotating about its axis. The Earth’s latitudinal parallels encompass increasingly less distance around the Planet with increasing latitude (progressing from the Equator towards the Poles), so that for every complete rotation about its axis, less distance is covered over the Earth’s surface as latitude increases. The velocity of rotation, therefore, is fastest at the Equator and decreases with increasing latitude, which acts to deflect or “turn” the path of air circulating in Hadley cells towards the east. Somewhere around the 30th parallel north or south, this air converges into one of the two subtropical jet streams that travel in easterly directions. Jet streams form just below the tropopause by the pressure differences resulting from two air masses of very different temperatures and densities converging around the 30th parallel N/S or 60th parallel N/S. The subtropical jets streams vary in height between 10 and 16 km (33000 and 52000 ft) ASL and often exceed speeds of 50 knots (57 mi h−1), although speeds of >240 kts (>275 mi h−1) have been measured along its meandering path around the Earth; see Figure 1.7b. Air circulating in both Hadley cells experiences the greatest descent towards the surface at about these same latitudes, creating areas of high atmospheric pressure. These high-pressure areas and the low-pressure area at the ITCZ form a pressure gradient that drives air near the surface towards the ITCZ, completing the Hadley circulation loop. The moving air also experiences a Coriolis force that turns its path towards the ITCZ in a westerly direction, creating the trade winds (see Figure 1.6).

Figure 1.7

Schematic representations of atmospheric circulation systems and jet streams. (a) Cross-sectional view of the Hadley circulation, Ferrel or mid-latitude circulation and Polar circulation cells of the Northern Hemisphere, with circulation directions shown with arrows and locations for the tropopause and both the subtropical and polar jet streams indicated. The tropopause is shown to decrease in altitude moving from the Equator to the pole. (b) The general paths of the four jet streams across the Earth are shown with their directions indicated by arrows. The jet streams take a meandering path around the Earth, dipping and rising in both altitude and latitude, splitting at times and forming eddies and even disappearing altogether to appear elsewhere in the troposphere. Adapted from NOAA.145 

Figure 1.7

Schematic representations of atmospheric circulation systems and jet streams. (a) Cross-sectional view of the Hadley circulation, Ferrel or mid-latitude circulation and Polar circulation cells of the Northern Hemisphere, with circulation directions shown with arrows and locations for the tropopause and both the subtropical and polar jet streams indicated. The tropopause is shown to decrease in altitude moving from the Equator to the pole. (b) The general paths of the four jet streams across the Earth are shown with their directions indicated by arrows. The jet streams take a meandering path around the Earth, dipping and rising in both altitude and latitude, splitting at times and forming eddies and even disappearing altogether to appear elsewhere in the troposphere. Adapted from NOAA.145 

Close modal

Polar circulation cells occur in each hemisphere roughly between their respective 60th parallel and the Polar region and are driven by the same mechanisms that drive the Hadley cells. Both the Polar and Hadley cells are thermally direct cells because they convert thermal energy directly into kinetic energy, resulting in rising branches occurring over warm temperature zones and descending branches over cold temperature zones. The vertical rise in Polar cells, however, is limited by a lower tropopause ceiling only ∼8 km (∼5 mi) ASL and contributes to the cells having substantially less vertical movement than the Hadley cells; this is represented schematically in Figure 1.7a. The rising branches in each Polar cell are found somewhere around their corresponding 60th parallel, where the rising air creates low-pressure areas. Upon reaching the tropopause, the rising air turns and begins its circulation towards the Poles, progressively becoming cooler and denser along the way and ultimately descending towards the surface at or near the Poles. The descending air creates a high-pressure area and, together with the low-pressure area at the corresponding 60th parallel, forms a pressure gradient that drives the surface circulation towards the low-pressure area, completing the Polar cell circulation loop. The circulating surface air experiences a Coriolis force on its path towards its corresponding 60th parallel that deflects it eastwards (see Figure 1.6).

Mid-latitude circulation cells are found in both hemispheres between their respective Hadley and Polar cells. In contrast to the other cell types, the mid-latitude cells are thermally indirect cells, as they are not driven by thermal forcing but by eddy forcing (weather systems). The rising branches of mid-latitude cells occur over cold temperature zones with descending branches over warm temperature zones, driving cell circulations in opposite directions as those of the thermally direct systems. Mid-latitude surface air moves towards the Poles rather than the Equator and experiences a Coriolis force that turns them in an easterly direction (see Figure 1.6). The upper branches of the mid-latitude cells are not well defined, partly because the cells occur between the Hadley and Polar cells with neither a strong heat source nor strong cold sink to drive their convection. Polar jet streams form in each hemisphere where air masses from their mid-latitude and Polar circulation cells converge. The Polar jets travel at higher speeds than the subtropical jets, but occur only 7–12 km (23000–39000 ft) ASL.

The Hadley, mid-latitude and Polar circulation cells do not act alone as major contributors to the global heat transport driving the horizontal movement of atmospheric air, as disparities in temperature also drive a set of longitudinal circulation cells. Longitudinal circulations arise because water has a higher specific heat capacity than landmasses. Large bodies of water such as lakes and oceans, therefore, absorb and release more heat than landmasses, but upon doing so, their temperatures change less than those of landmasses. We experience this phenomenon in coastal areas as sea breezes (air cooled by large bodies of water) during the day and land breezes (air cooled by landmasses) at night, but on a much larger scale, the effects are seasonal. Warm air rises over the equatorial, continental and western Pacific Ocean regions, moves eastwards or westwards (depending on its location) upon reaching the tropopause and descends onto the Atlantic and Indian Oceans and the eastern Pacific Ocean. The Pacific Ocean circulation plays an especially important part in influencing the Earth’s weather. This ocean-based circulation cell results from the marked difference in surface temperatures across the Pacific Ocean, which contains warm western waters and cool eastern waters. Strong convective activity over equatorial East Asia coupled with descending cool air masses offshore of South America’s west coast creates strong winds that force Pacific water westwards into the western Pacific Ocean. Changes in the Pacific Ocean circulation every few years generate El Niño or La Niña effects that can bring unusually warm or cold winters and changes in the frequency of hurricanes for indeterminate periods of time.

Evolutionary biologists have divided the Earth’s surface into six biogeographic regions, each of which contains unique plants and animals.133,134  It is widely accepted that these unique biotas exist because of vicariance, the evolutionary isolation of species due to historic barriers to dispersal. For microorganisms in particular, including microscopic eukaryotes, such a biogeographic distribution is currently a subject of ongoing debate. This is especially the case for biogeographic regions in the atmosphere, as only a very limited number of studies have been conducted to determine whether large-scale patterns exist in the distribution of airborne microorganisms. Womack et al.6  argued that analogous patterns are possible for the atmospheric habitat and, like others,135,136  suggested that the Hadley, mid-latitude and Polar circulation cells might be responsible in large part for creating such patterns. Proponents of this idea point out that the mixing of air is more frequent within circulation cells than between them, resulting in barriers to air movement and the potential for vicariance. Although such patterns have yet to be discovered, there has been at least one report of large-scale distribution patterns for microorganisms in the atmosphere. Fröhlich-Nowoisky et al.18  found that the ratio of species richness between Basidiomycota and Ascomycota, the two major phyla of higher fungi, is much higher in the airspace over continents than that over oceans. This is a significant discovery because it suggests that there might be biogeographic regions in the atmosphere and global atmospheric circulation is important for understanding the biodiversity of microorganisms.

Particle transport through the troposphere is especially relevant to microbial biogeography, as it is central to the cosmopolitan distribution of many microbial species on the Planet’s surface.88  This transport provides rapid, long-distance dispersal of microorganisms, allowing some species to overcome geographic barriers. The recent computer simulations of Wilkinson et al.13  illustrate the potential for the cosmopolitan dispersal of airborne microorganisms by tropospheric air circulation. Their simulations used virtual microbes with diameters of 9, 20, 40 and 60 µm released from the surface and at an altitude of 6.5 km (∼21300 ft) ASL from one site in each hemisphere. Results of their 16 individual simulations over a virtual 1 year time frame are summarized graphically in Figure 1.8. The most striking result is the extensive within-hemisphere dispersal of virtual microorganisms 9 and 20 µm in diameter, representative of smaller eukaryotic microorganisms.117,118  Because bacteria are significantly smaller in size, their dispersal can be anticipated to be at least as extensive than that for the virtual microbes with 9 µm diameters. The well-known inverse correlation between organism size and dispersal area is readily apparent by comparing the results for the 9 and 20 µm diameter virtual microbes with those for the 40 and 60 µm diameter virtual microbes, which are seen to disperse over substantially less area over the virtual 1 year time frame. Another striking result is the lack of dispersal between the Northern and Southern Hemispheres, which is a direct consequence of the atmospheric circulation patterns around the ITCZ. Other mechanisms may be important for dispersal between hemispheres, including bird migration and ship and airline travel. The results also illustrate the importance of prevailing wind directions, with long-distance dispersal from west to east more likely than from east to west.

Figure 1.8

Results from computer simulations over a 1 year period for the atmospheric dispersal of particles released from locations in both hemispheres. The simulations were conducted with the GEOS-Chem model146,147  for the year 2001, with releases from sites in Mexico and Tierra del Fuego. Both sites included releases of virtual microorganisms with 9, 20, 40 and 60 µm diameters from the surface (surf) and an altitude of 6.5 km (∼21300 ft) ASL (high). Shading illustrates the extent of dispersal for virtual microbes in each simulation on a logarithmic scale. Adapted from Wilkinson et al.13 

Figure 1.8

Results from computer simulations over a 1 year period for the atmospheric dispersal of particles released from locations in both hemispheres. The simulations were conducted with the GEOS-Chem model146,147  for the year 2001, with releases from sites in Mexico and Tierra del Fuego. Both sites included releases of virtual microorganisms with 9, 20, 40 and 60 µm diameters from the surface (surf) and an altitude of 6.5 km (∼21300 ft) ASL (high). Shading illustrates the extent of dispersal for virtual microbes in each simulation on a logarithmic scale. Adapted from Wilkinson et al.13 

Close modal

The Earth’s atmosphere is unique to the Solar System because of its intimate relationship with living systems and their evolutionary history, a relationship that has existed over geological time. The oldest known fossils suggest that this relationship was well established even 3.4 Ga, with primitive bacteria-like cells already adding free O2 into the atmosphere as a product of photosynthesis.51–54  Over the next billion years, photosynthesis completely transformed the Earth’s CO2-dominated atmosphere to one with significant concentrations of O2,29  favoring the proliferation of the new eukaryotic life forms at the time. Some hundred million years later, free O2 began to dominate the chemistry of the atmosphere and O3 formed in the upper atmosphere from the recombination of O2 by solar radiation. Finally, the formation of a powerful O3 screen ∼600 Ma78  in the stratosphere protected living systems on the Planet’s surface from the Sun’s harmful UV radiation.

Life originated in the oceans and, roughly 1 billion years later, began to colonize land. This terrestrial migration implies that the primitive, anaerobic prokaryotes so prevalent at the time must have developed reasonably high levels of vigor and robustness in order to migrate from their natural aquatic habitats onto dry land and ultimately thrive. Some of the most essential features for this robustness, especially tolerances against an O2-containing atmosphere, strong UV radiation and recurring desiccant conditions, are also central for airborne survival in the atmosphere. It is almost certain that at about this time in evolutionary history, or perhaps some time later, these primitive prokaryotic life forms were able to survive short excursions into the airspace and return to the surface alive. Microfossils reveal that living systems existing ∼3.1 Ga57,62,63  were of sizes similar to those of extant microorganisms believed to have residence times of ∼1 week,17,111  revealing that the lofting of the early prokaryotes into the atmosphere at the time was very likely. Over the following billions of years, prokaryotic life forms must have evolved to survive excursions into the atmosphere better, and eukaryotic cells, single-celled microorganisms at first followed by multicellular life forms, appeared and also became lofted into the atmosphere. The atmosphere is believed to contribute to microbial evolution in two important ways: it imposes unique combinations of stresses on microorganisms to drive mutation4  and it provides a means to disperse microorganisms over great distances and introduce novel genes into distant gene pools.84  The evolutionary history of living microorganisms surviving atmospheric excursions is exceedingly difficult to understand with certainty. Direct evidence of early living systems aloft in the airspace cannot be found in the fossil record and facts must be extrapolated from fossils of terrestrial and aquatic living systems from the distant past. Details on the subject, therefore, are largely speculative.

There is now abundant evidence that the atmosphere is indeed a true habitat for microorganisms. The present-day airspace is literally teeming with living microorganisms and a wealth of culture-based investigations present overwhelming evidence that microorganisms collected from atmospheric environments are remarkably capable of metabolic activity. These investigations, and others involving direct observations of cloud water,109,110  strongly suggest that at least some microorganisms must be metabolically active while airborne. Investigations of microbial reproduction in the atmosphere, on the other hand, have been severely limited. Generation times for microorganisms in the atmosphere are usually extrapolated from atmospheric residence times of microorganisms, as they may be the principal factor limiting microorganism reproduction while airborne.17  Residence times derived from particle transport simulations13,17,111  together with generation times measured for bacteria in cloud water held at typical tropospheric temperatures109  suggest that bacterial excursions into the atmosphere could potentially include one or two cell divisions and that significant numbers of bacterial excursions into the atmosphere, if not most of them, are likely not to involve bacterial reproduction at all. Like many investigative efforts conducted to answer intriguing questions in the field of aerobiology, the largest obstacle to studying microbial reproduction in the airspace is the difficulty of designing direct in situ methods to investigate live microorganisms aloft in the atmosphere.

Like oceans, the atmosphere has currents and eddies that are influenced by solar heating, convection, Coriolis forces and topographies. In the troposphere, the currents and eddies constitute the atmospheric circulation, which is largely responsible for the worldwide dispersal of microorganisms and connecting all microbial habitats across the Planet’s surface to one another. Microbial dispersal through the airspace is the most straightforward means of explaining the cosmopolitan distribution of many microbial species,88  as it provides a mechanism for microorganisms to overcome historic barriers to dispersal. Some have suggested6,135,136  that analogous barriers to microbial dispersal might exist in the atmosphere, possibly giving rise to its own biogeographic regions. Characterizing the microbiological variability in the atmosphere and also the forces responsible for generating them holds real promise for advancing our understanding of microbial biogeography in general, currently a subject of ongoing debate among many microbiologists.

We wish to thank Ms Joy L. Henderson and Ms Donna M. Hoffman for their support and expert assistance in preparing this chapter.

1

The opinions expressed in this chapter are the private views of the authors and are not to be construed as an official Department of the Army position unless so designated by other authorizing documents. This chapter has been approved for public release.

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