Aeroplankton and the Need for a Global Monitoring Network

“How many times must a man look up before he can see the sky?” sang Bob Dylan. Although you do not perceive it, about 1 ton of invisible force is pressing on the surface of your body right now. However, because our species evolved with atmospheric pressure, we often forget that we are residing underneath an enormous ocean of air. Clouds are a helpful visual reminder that a protective gaseous blanket has allowed life to spread to every corner of the planet. Much like the oceans, the atmosphere is a physical medium, with currents and eddies that vary with location, topography, and season over diverse spatial and temporal scales. And much like plankton within the ocean, the air overhead is teeming with microorganisms—aeroplankton swept up from the surface.

Microbes are small, ubiquitous, and prone to atmospheric dispersal. Well before humans understood the invisible world, there was a sneaking suspicion that certain diseases were airborne. Influenza (first cited in the Oxford English Dictionary in 1734) comes from the Latin word influere, a term steeped with roots in the sky. It was thought that sickness must have been flowing down from the stars above. Even after microbiology emerged as a field in later centuries, the atmosphere remained essentially unexplored, because obtaining samples was so costly and difficult. Only within the last decade have research teams figured out how to efficiently collect samples and employ modern molecular methods (reviewed by Gandolfi and colleagues [2013]). In doing so, we can finally begin studying how aeroplankton affect global processes and ecosystems.

Griffin and colleagues (2002) were the first to postulate that distant continents can sneeze on each other. Our planet spins on a relatively stable axis, creating predictable wind patterns, and Griffin and colleagues (2002) suggested these atmospheric bridges would not only exchange small particulates, such as dust, but microbial hitchhikers as well. The Earth's atmosphere is like a conveyor belt for microbes, with seasonal winds moving cells thousands of kilometers away from source regions. Some dust storms from the largest deserts on Earth are so gigantic that they are visible from orbit. Over 56 million metric tons of dust from Asia crosses the Pacific Ocean each year and arrives in North American air (Smith et al. 2013)—just one of many intercontinental trajectories. With millions of microbes in a typical gram of surface soil, the atmospheric bridge hypothesis from Griffin and colleagues (2002) was intuitive but difficult to prove, because air masses at low altitudes were challenging to track.

However, new work at higher altitudes provided a breakthrough for aerobiology. Using aircraft and mountaintop observatories in North America, microbes from Asian and African source regions have been detected recently, including taxa capable of surviving the rigors of transport (Creamean et al. 2013, Smith et al. 2013). It is now understood that even dead cells can play a functional role in weather and climate as cloud and ice condensation nuclei (Creamean et al. 2013, Šantl-Temkiv et al. 2013). Some researchers (e.g., Vaïtilingom et al. 2013) have suggested that cellular activity may be plausible in long-lived clouds at lower (warmer) altitudes, but measuring metabolism, growth, or replication has not been achieved while microbes are airborne. Soon, monitoring short-lived ribonucleic acid transcripts in situ should help settle the debate about whether the atmosphere is, in fact, its own ecosystem.

Now that we know aeroplankton can travel between continents (Favet et al. 2012, Creamean et al. 2013, Smith et al. 2013), some can survive the trip, and some can cause disease (reviewed by Polymenakou [2012]), it is imperative to establish a global sampling network for building models and forecasting areas of increased risk. We need to monitor microbes just like we monitor other types of common air pollution. The key is sampling in the free troposphere, a layer of the atmosphere in which long-range transport is more efficient and easier to trace. Measurements from aircraft or balloons can provide valuable regional data, but flights are too infrequent. High-altitude mountaintop observatories, in comparison, offer around-the-clock access to the upper atmosphere, improved air-pumping capabilities, additional atmospheric and meteorological instrumentation, along with crucial controls for aseptic sampling.

The infrastructure for high-altitude observatories is already in place, through air quality stations supported by the US National Oceanic and Atmospheric Administration's Earth System Research Laboratory's Global Monitoring Division. All that is needed is the installation and upkeep of microbiological instruments at these stations, modeled after the successful campaign at the Mount Bachelor Observatory in central Oregon (Smith et al. 2013). Baseline stations are located in Alaska, Hawaii, and American Samoa, with other platforms distributed across Europe, Asia, and Africa. To get an unparalleled data set from across the Northern Hemisphere, it would take only a modest amount of start-up funding and organization. Once international teams are in place, a workshop should follow to reduce variation across field sites. Useful discussion topics were reviewed by Gandolfi and colleagues (2013), including the standardization of sampling techniques, cleanliness protocols, and analysis methods.

Aerosols cotransported with microbes can suggest the origin of cells and how long they have been aloft. Combining microbial and atmospheric aerosol data (type, ratio, and concentration) from ground stations will help determine global highways and traffic patterns. Most recent studies have been focused on the relationship between dust and colofted microbes (Favet et al. 2012, Creamean et al. 2013, Smith et al. 2013), but aeroplankton originate from a variety of other natural and artificial environments. Systematic, regional measurements of microbes emitted from landfills, wastewater treatment plants, and farms could also provide valuable geochemical signatures for disentangling long-range transport.

As we inject higher numbers of microbes into the atmosphere each year and as deforestation potentially transforms more of Earth's surface into deserts, our burgeoning population may become increasingly vulnerable to airborne disease and allergens. Even if aeroplankton were harmless before, the combination of new weather patterns with higher cell concentrations could have unpredictable consequences. It is also worth noting how vulnerable we are to the intentional release of pathogens into our atmosphere. From August 1944 to April 1945, during World War II, Japan launched over 9000 balloon bombs into the Pacific jet stream and let the winds finish the job. Although this was an inefficient act of warfare (only about 300 explosives landed in North America), the deadlier bomb today would carry an infectious biological agent, capable of causing disease in cities or on croplands. The global monitoring network proposed here could serve as an early-warning and forecasting system, capable of saving countless lives following an act of atmospheric bioterrorism.

Molecular methods will continue providing important information about aeroplankton overhead, but we must not neglect basic viability assays and the need to understand what types of cells can propagate after surviving the rigors of atmospheric transport. Efforts to take a more comprehensive census of the upper atmosphere may unlock major breakthroughs in biotechnology and medicine. Prospecting for microbes in seemingly inhospitable environments has paid dividends before: When the boiling-hot springs of Yellowstone National Park were explored, a thermostable enzyme was isolated from Thermus aquaticus that enabled the polymerase chain reaction technology that virtually all life sciences depend on today. Perhaps, enzymes that guard or restore radiation-damaged DNA molecules will be discovered within atmospheric microbes capable of enduring the most ultraviolet-intense environment on Earth.

The atmosphere is but one of several microbiological frontiers yet to be explored on our planet. Is it a vector for intercontinental disease? Is it an ecosystem in its own right? Can aeroplankton influence global weather patterns or contribute radiation-resistant genes for biotechnology? Bob Dylan and the latest aerobiology literature seem to be in agreement: The answer is blowin' in the wind.

Author notes

David J. Smith () is a microbiologist at the NASA Kennedy Space Center, in Florida.