Aeroplankton

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Sea spray containing marine microorganisms can be swept high into the atmosphere and may travel the globe before falling back to earth.
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Aeroplankton (or aerial plankton) are tiny lifeforms that float and drift in the air, carried by wind. Most of the living things that make up aeroplankton are very small to microscopic in size, and many can be difficult to identify because of their tiny size. Scientists can collect them for study in traps and sweep nets from aircraft, kites or balloons.[1]

Aeroplankton is made up of numerous microbes, including viruses, about 1,000 different species of bacteria, around 40,000 varieties of fungi, and hundreds of species of protists, algae, mosses, and liverworts that live some part of their life cycle as aeroplankton, often as spores, pollen, and wind-scattered seeds. Additionally, microorganisms are swept into the air from terrestrial dust storms, and an even larger amount of airborne marine microorganisms are propelled high into the atmosphere in sea spray. Aeroplankton deposits hundreds of millions of airborne viruses and tens of millions of bacteria every day on every square meter around the planet.

Overview[]

Colourised SEM image of pollen grains
from common plants

Dispersal is a vital component of an organism’s life-history,[2] and the potential for dispersal determines the distribution, abundance, and thus, the community dynamics of species at different sites.[3][4][5] A new habitat must first be reached before filters such as organismal abilities and adaptations, the quality of a habitat, and the established biological community determine the colonization efficiency of a species.[6] While larger animals can cover distances on their own and actively seek suitable habitats, small (<2 mm) organisms are often passively dispersed,[6] resulting in their more ubiquitous occurrence.[7] While active dispersal accounts for rather predictable distribution patterns, passive dispersal leads to a more randomized immigration of organisms.[3] Mechanisms for passive dispersal are the transport on (epizoochory) or in (endozoochory) larger animals (e.g., flying insects, birds, or mammals) and the erosion by wind.[6][8]

A propagule is any material that functions in propagating an organism to the next stage in its life cycle, such as by dispersal. The propagule is usually distinct in form from the parent organism. Propagules are produced by plants (in the form of seeds or spores), fungi (in the form of spores), and bacteria (for example endospores or microbial cysts).[9] Often cited as an important requirement for effective wind dispersal is the presence of propagules (e.g., resting eggs, cysts, ephippia, juvenile and adult resting stages),[6][10][11] which also enables organisms to survive unfavorable environmental conditions until they enter a suitable habitat. These dispersal units can be blown from surfaces such as soil, moss, and the desiccated sediments of temporary or intermittant waters. The passively dispersed organisms are typically pioneer colonizers.[12][13][14][8]

However, wind-drifted species vary in their vagility (probability to be transported with the wind),[15] with the weight and form of the propagules, and therefore, the wind speed required for their transport,[16] determining the dispersal distance. For example, in nematodes, resting eggs are less effectively transported by wind than other life stages,[17] while organisms in anhydrobiosis are lighter and thus more readily transported than hydrated forms.[18][19] Because different organisms are, for the most part, not dispersed over the same distances, source habitats are also important, with the number of organisms contained in air declining with increasing distance from the source system.[12][20] The distances covered by small animals range from a few meters,[20] to several hundred meters,[12] and up to several thousand meters.[17] While the wind dispersal of aquatic organisms is possible even during the wet phase of a transiently aquatic habitat,[6] during the dry stages a larger number of dormant propagules are exposed to wind and thus dispersed.[11][20][21] Freshwater organisms that must "cross the dry ocean" [6] to enter new aquatic island systems will be passively dispersed more successfully than terrestrial taxa.[6] Numerous taxa from both soil and freshwater systems have been captured from the air (e.g., bacteria, several algae, ciliates, flagellates, rotifers, crustaceans, mites, and tardigrades).[12][20][21][22] While these have been qualitatively well studied, accurate estimates of their dispersal rates are lacking.[8]

Subject to gravity, aerosols (or particulate matter) as well as bioaerosols become concentrated in the lower part of the troposphere that is called the planetary boundary layer. Microbial concentrations thus usually show a vertical stratification from the bottom to the top of the troposphere with average estimated bacterial concentrations of 900 to 2 × 107 cells per cubic metre in the planetary boundary layer [24][25][26][27][28] and 40 to 8 × 104 cells per cubic metre in the highest part of the troposphere called the free troposphere.[29][30][31] The troposphere is the most dynamic layer in terms of chemistry and physics of aerosols and harbors complex chemical reactions and meteorological phenomena that lead to the coexistence of a gas phase, liquid phases (i.e., cloud, rain, and fog water) and solid phases (i.e., microscopic particulate matter, sand dust). The various atmospheric phases represent multiple biological niches.[23]

Pollen grains[]

Pollen grains observed in aeroplankton of South Europe[32]
Drawings of fungal spores found in air
Some cause asthma, such as Alternaria alternata. A drawing of a very small "dust" seed from the flower Orchis maculata is provided for comparison.[33][34]
    A = ascospore, B = basidiospore, M = mitospore
Spider ballooning structures. Black, thick points represent the spider’s body. Black lines represent ballooning threads.[35]
Distribution modes and possible geographic ranges of nematodes [36]
See also: Palynology

Effective pollen dispersal is vital for maintenance of genetic diversity and fundamental for connectivity between spatially separated populations.[37] An efficient transfer of the pollen guarantees successful reproduction in flowering plants. No matter how pollen is dispersed, the male-female recognition is possible by mutual contact of stigma and pollen surfaces. Cytochemical reactions are responsible for pollen binding to a specific stigma.[38][32]

Allergic diseases are considered to be one of the most important contemporary public health problems affecting up to 15–35% of humans worldwide.[39] There is a body of evidence suggesting that allergic reactions induced by pollen are on the increase, particularly in highly industrial countries.[39][40][32]

Fungal spores[]

Fungi, a major element of atmospheric bioaerosols, are capable of existing and surviving in the air for extended periods of time.[41] Both the spores and the mycelium may be dangerous for people suffering from allergies, causing various health issues including asthma.[42][43] Apart from its negative impact on human health, atmospheric fungi may be dangerous for plants as sources of infection.[44][45] Moreover, fungal organisms may be capable of creating additional toxins that are harmful to humans and animals, such as endotoxins or mycotoxins.[46][47]

Considering this aspect, aeromycological research is considered capable of predicting future symptoms of plant diseases in both crops and wild plants.[44][45] Such research may therefore form the foundation for creating models of pathogenic spore outbreaks in plants and for studying the movement of spores and other fungal organisms across larger regions.[48][49][50] Fungi capable of travelling extensive distances with wind despite natural barriers, such as tall mountains, may be particularly relevant to understanding the role of fungi in plant disease.[51][52][44][50] Notably, the presence of numerous fungal organisms pathogenic to plants has been determined in mountainous regions.[47]

A wealth of correlative evidence suggests asthma is associated with fungi and triggered by elevated numbers of fungal spores in the environment.[53] Intriguing are reports of thunderstorm asthma. In a now classic study from the United Kingdom, an outbreak of acute asthma was linked to increases in Didymella exitialis ascospores and Sporobolomyces basidiospores associated with a severe weather event.[54] Thunderstorms are associated with spore plumes: when spore concentrations increase dramatically over a short period of time, for example from 20,000 spores/m3 to over 170,000 spores/m3 in 2 hours.[55] However, other sources consider pollen or pollution as causes of thunderstorm asthma.[56] Transoceanic and transcontinental dust events move large numbers of spores across vast distances and have the potential to impact public health,[57] and similar correlative evidence links dust blown off the Sahara with pediatric emergency room admissions on the island of Trinidad.[58][33]

Pteridophyte spores[]

Pteridophyte spores, such as fern spores, similar to pollen grains and fungal spores, are also components of aeroplankton.[59][60] Fungal spores usually rank first among bioaerosol constituents due to their count numbers which can reach to between 1,000 and 10,000 per cubic metre (28 and 283/cu ft), while pollen grains and fern spores can each reach to between 10 and 100 per cubic metre (0.28 and 2.83/cu ft).[40][61]

Arthropods[]

Many small animals, mainly arthropods (such as insects and spiders), are also carried upwards into the atmosphere by air currents and may be found floating several thousand feet up. Aphids, for example, are frequently found at high altitudes.

Ballooning, sometimes called kiting, is a process by which spiders, and some other small invertebrates, move through the air by releasing one or more gossamer threads to catch the wind, causing them to become airborne at the mercy of air currents.[62][63] A spider (usually limited to individuals of a small species), or spiderling after hatching,[64] will climb as high as it can, stand on raised legs with its abdomen pointed upwards ("tiptoeing"),[65] and then release several silk threads from its spinnerets into the air. These automatically form a triangular shaped parachute[66] which carries the spider away on updrafts of winds where even the slightest of breezes will disperse the arachnid.[65][66] The flexibility of their silk draglines can aid the aerodynamics of their flight, causing the spiders to drift an unpredictable and sometimes long distance.[67] Even atmospheric samples collected from balloons at five kilometres altitude and ships mid-ocean have reported spider landings. Mortality is high.[68]

The Earth's static electric field may also provide lift in windless conditions.[69]

Nematodes[]

Nematodes (roundworms), the most common animal taxon, are also found among aeroplankton.[11][12][20] Nematodes are an essential trophic link between unicellular organisms like bacteria, and larger organisms such as tardigrades, copepods, flatworms, and fishes.[8] For nematodes, anhydrobiosis is a widespread strategy allowing them to survive unfavorable conditions for months and even years.[70][71] Accordingly, nematodes can be readily dispersed by wind. However, as reported by Vanschoenwinkel et al.,[20] nematodes account for only about one percent of wind-drifted animals. Among the habitats colonized by nematodes are those that are strongly exposed to wind erosion as e.g., the shorelines of permanent waters, soils, mosses, dead wood, and tree bark.[72][8] In addition, within a few days of forming temporary waters such as phytotelmata were shown to be colonized by numerous nematode species.[14][73][8]

Microorganisms[]

A stream of airborne microorganisms circles the planet above weather systems but below commercial air lanes.[74] Some microorganisms are swept up from terrestrial dust storms, but most originate from marine microorganisms in sea spray. In 2018, scientists reported that hundreds of millions of viruses and tens of millions of bacteria are deposited daily on every square meter around the planet.[75][76]

The presence of airborne cyanobacteria and microalgae as well as their negative impacts on human health have been documented by many researchers worldwide. However, studies on cyanobacteria and microalgae are few compared with those on bacteria and viruses. Research is especially lacking on the presence and taxonomic composition of cyanobacteria and microalgae near economically important water bodies with much tourism.[77] Research on airborne algae is especially important in tourist areas near water-bodies. Sunbathers are exposed to particularly high quantities of harmful cyanobacteria and microalgae. Additionally, harmful microalgae and cyanobacteria blooms tend to occur in both marine and freshwater reservoirs during summer.[78][79][80][81] Previous work has shown that the Mediterranean Sea is dominated by the picocyanobacteria Synechococcus sp. and Synechocystis sp., which are responsible for the production of a group of hepatotoxins known as microcystins.[82] Because most tourism occurs in summer, many tourists are exposed to the most extreme negative impacts of airborne microalgae.[77]

Airborne bacteria are emitted by most Earth surfaces (plants, oceans, land, and urban areas) to the atmosphere via a variety of mechanical processes such as aeolian soil erosion, sea spray production, or mechanical disturbances including anthropogenic activities.[83][84] Due to their relatively small size (the median aerodynamic diameter of bacteria-containing particles is around 2–4 μm),[61] these can then be transported upward by turbulent fluxes [85] and carried by wind to long distances. As a consequence, bacteria are present in the air up to at least the lower stratosphere.[86][31][87] Given that the atmosphere is a large conveyor belt that moves air over thousands of kilometers, microorganisms are disseminated globally.[88][89][90] Airborne transport of microbes is therefore likely pervasive at the global scale, yet there have been only a limited number of studies that have looked at the spatial distribution of microbes across different geographical regions.[91][90] One of the main difficulties is linked with the low microbial biomass associated with a high diversity existing in the atmosphere outdoor (∼102–105 cells/m3)[92][93][94] thus requiring reliable sampling procedures and controls. Furthermore, the site location and its environmental specificities have to be accounted for to some extent by considering chemical and meteorological variables.[95][96]

The environmental role of airborne cyanobacteria and microalgae is only partly understood. While present in the air, cyanobacteria and microalgae can contribute to ice nucleation and cloud droplet formation. Cyanobacteria and microalgae can also impact human health.[61][97][98][99][100][101] Depending on their size, airborne cyanobacteria and microalgae can be inhaled by humans and settle in different parts of the respiratory system, leading to the formation or intensification of numerous diseases and ailments, e.g., allergies, dermatitis, and rhinitis.[98][102][103] According to Wiśniewska et al.,[97] these harmful microorganisms can constitute between 13% and 71% of sampled taxa.[77] However, the interplay between microbes and atmospheric physical and chemical conditions is an open field of research that can only be fully addressed using multidisciplinary approaches.[96]

Biological particles are known to represent a significant fraction (∼20–70%) of the total number of aerosols > 0.2 μm, with large spatial and temporal variations.[104][105][106][107] Among these, microorganisms are of particular interest in fields as diverse as epidemiology, including phytopathology,[108] bioterrorism, forensic science, and public health,[109] and environmental sciences, like microbial ecology,[110][111][84] meteorology and climatology.[112][113] More precisely concerning the latter, airborne microorganisms contribute to the pool of particles nucleating the condensation and crystallization of water and they are thus potentially involved in cloud formation and in the triggering of precipitation.[114][115] Additionally, viable microbial cells act as chemical catalyzers interfering with atmospheric chemistry.[116] The constant flux of bacteria from the atmosphere to the Earth’s surface due to precipitation and dry deposition can also affect global biodiversity, but they are rarely taken into account when conducting ecological surveys.[76][117][118][119] As stressed by these studies attempting to decipher and understand the spread of microbes over the planet,[120][93][121] concerted data are needed for documenting the abundance and distribution of airborne microorganisms, including at remote and altitudes sites.[96]

Bioaerosols[]

Bioaerosols, known also as primary biological aerosols or PBAs, are the subset of atmospheric particles that are directly released from the biosphere into the atmosphere. They include living and dead organisms (e.g., algae, archaea, bacteria ), dispersal units (e.g., fungal spores and plant pollen), and various fragments or excretions (e.g., plant debris and brochosomes).[122][123][124][125][61][105][126][127][128][129][130] PBA particle diameters range from nanometers up to about a tenth of a millimeter. The upper limit of the aerosol particle size range is determined by rapid sedimentation, i.e., larger particles are too heavy to remain airborne for extended periods of time.[131][132][115]

Bioaerosols include living and dead organisms as well as their fragments and excrements emitted from the biosphere into the atmosphere.[133] [61][115] Included are archaea, fungi, microalgae, cyanobacteria, bacteria, viruses, plant cell debris, and pollen.[134][61][115][135][97] The most poorly studied organisms in aerobiology and phycology are airborne microalgae and cyanobacteria.[135][136][77] This lack of knowledge may result from the lack of standard methods for both sampling and further analysis, especially quantitative analytical methods.[97] Few studies have been performed to determine the number of cyanobacteria and microalgae in the atmosphere [137][138] A previous review [61] has shown that the average quantity of atmospheric algae is between 100 and 1000 cells per cubic meter of air. Currently, over 350 taxa of cyanobacteria and microalgae have been documented in the atmosphere worldwide.[97][98] Cyanobacteria and microalgae end up in the air as a consequence of their emission from soil, buildings, trees, and roofs.[97][139][140][77]

Historically, the first investigations of the occurrence and dispersion of microorganisms and spores in the air can be traced back to the early 19th century.[141][142][143] Since then, the study of bioaerosol has come a long way, and air samples collected with aircraft, balloons, and rockets have shown that PBA released from land and ocean surfaces can be transported over long distances and up to very high altitudes, i.e., between continents and beyond the troposphere.[144][31][145][146][147][148][149][150][151][152][89][115]

  • Global bioaerosol cycling
    After emission from the biosphere, bioaerosol particles interact with other aerosol particles and trace gases in the atmosphere and can be involved in the formation of clouds and precipitation. After dry or wet deposition to the Earth's surface, viable bioparticles can contribute to biological reproduction and further emission. This feedback can be particularly efficient when coupled to the water cycle (bioprecipitation).[153][132][115]
  • Global ecosystem interactions of bioaerosol particles
    Key aspects and areas of research required to determine and quantify the interactions and effects of biogenic aerosol particles in the Earth system, including primary biological aerosols (PBA) directly emitted to the atmosphere and secondary organic aerosols (SOA) formed upon oxidation and gas-to-particle conversion of volatile organic compounds (VOC).[115]

Bioaerosols play a key role in the dispersal of reproductive units from plants and microbes (pollen, spores, etc.), for which the atmosphere enables transport over geographic barriers and long distances.[144][120][92][61][130] Bioaerosols are thus highly relevant for the spread of organisms, allowing genetic exchange between habitats and geographic shifts of biomes. They are central elements in the development, evolution, and dynamics of ecosystems.[115]

Microbial activity and clouds[]

Impact of microbial activity on clouds [154]
Biological processes and their targets are indicated by green arrows, while red arrows indicate abiotic processes.
EPS: Exopolysaccharide              SOA: Secondary organic aerosol
Based on coordinated metagenomics/metatranscriptomics
See also: bioaerosol and whiting event

The outdoor atmosphere harbors diverse microbial assemblages composed of bacteria, fungi and viruses [155] whose functioning remains largely unexplored.[154] While the occasional presence of human pathogens or opportunists can cause potential hazard,[156][157] in general the vast majority of airborne microbes originate from natural environments like soil or plants, with large spatial and temporal variations of biomass and biodiversity.[158][159] Once ripped off and aerosolized from surfaces by mechanical disturbances such as those generated by wind, raindrop impacts or water bubbling,[160][83] microbial cells are transported upward by turbulent fluxes.[161] They remain aloft for an average of ~3 days,[162] a time long enough for being transported across oceans and continents [163][164][91] until being finally deposited, eventually helped by water condensation and precipitation processes; microbial aerosols themselves can contribute to form clouds and trigger precipitation by serving as cloud condensation nuclei [165] and ice nuclei.[166][167][154]

Living airborne microorganisms may end up concretizing aerial dispersion by colonizing their new habitat,[168] provided that they survive their journey from emission to deposition. Bacterial survival is indeed naturally impaired during atmospheric transport,[169][170] but a fraction remains viable.[171][172] At high altitude, the peculiar environments offered by cloud droplets are thus regarded in some aspects as temporary microbial habitats, providing water and nutrients to airborne living cells.[173][174][175] In addition, the detection of low levels of heterotrophy [176] raises questions about microbial functioning in cloud water and its potential influence on the chemical reactivity of these complex and dynamic environments.[175][116] The metabolic functioning of microbial cells in clouds is still albeit unknown, while fundamental for apprehending microbial life conditions during long distance aerial transport and their geochemical and ecological impacts.[154]

Venus clouds[]

After the tantalizing detection of phosphine (PH3) in the atmosphere of the Venus planet, in the absence of known and plausible chemical mechanism to explain the formation of this molecule, the presence of micro-organisms in suspension in the Venus atmosphere has been speculated by Greaves et al. (2020) from Cardiff University.[177] They have formulated the hypothesis of the microbial formation of phosphine, envisaging the possibility of a liveable window in the Venusian clouds at a certain altitude with an acceptable temperature range for microbial life.

Hallsworth et al. (2021) have studied the conditions required to support the life of extremophile micro-organisms in the clouds at high altitude in the Venus atmosphere where favorable temperature conditions might prevail. Beside the presence of sulfuric acid in the clouds which already represent a major challenge for the survival of most of micro-organisms, they came to the conclusion that the Venus atmosphere is much too dry to host microbial life. Indeed, Hallsworth et al. (2021) have determined a water activity ≤ 0.004, two orders of magnitude below the 0.585 limit for known extremophiles.[178] So, with a water activity in the Venus clouds 100 times lower that the threshold of 0.6 known in Earth conditions the hypothesis envisaged by Greaves et al. (2020) to explain the biotic origin of phosphine in the Venus atmosphere is ruled out.

The approach developed by Hallsworth et al. (2021) also applies to the Earth atmosphere. To support microbial activity for a prolonged period of time, the water activity (or the relative humidity, their definition is the same) in the air must be higher than 0.6. Therefore, on Earth, the half upper stratosphere is too dry to support microbial activity.

However, if after desiccation, some micro-organisms are well preserved in the dry state, they could be revived once they become rehydrated in the troposphere, or after their deposition on the ground. Beside a low relative humidity of the air, the higher intensity of ultraviolet (UV) light with altitude also represents a severe limitation for the survival of aeroplanktons at high elevations in the atmosphere.

New generation technologies[]

See also: Pollen DNA barcoding

Over the last few years, next generation DNA sequencing technologies, such as metabarcoding as well as coordinated metagenomics and metatranscriptomics studies, have been providing new insights into microbial ecosystem functioning, and the relationships that microorganisms maintain with their environment. There have been studies in soils,[179] the ocean,[180][181] the human gut,[182] and elsewhere.[183][184] In the atmosphere, though, microbial gene expression and metabolic functioning remain largely unexplored, in part due to low biomass and sampling difficulties.[154] So far, metagenomics has confirmed high fungal, bacterial, and viral biodiversity,[185][186][187][188] and targeted genomics and transcriptomics towards ribosomal genes has supported earlier findings about the maintenance of metabolic activity in aerosols [189][190] and in clouds.[159] In atmospheric chambers airborne bacteria have been consistently demonstrated to react to the presence of a carbon substrate by regulating ribosomal gene expressions.[191][154]

Gallery[]

  • Pteridophyta spores, including fern spores, in the air of Lublin

  • Airborne fungal spores

  • Detail of the formation of a dense aeroplankton cloud at sunset, over the river Loire in France

See also[]

References[]

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General reference[]

  • Cox, Christopher S.; Wathes, Christopher M. (25 November 2020). Bioaerosols Handbook. ISBN 9781000115048.

External links[]

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