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The High Life: Transport of Microbes in the AtmosphereBy David J. Smith, Dale W. Griffin & Daniel A. Jaffe
Microbes (bacteria, fungi, algae, and viruses) are the most successful types of life on Earth because of their ability to adapt to new environments, reproduce quickly, and disperse globally. Dispersal occurs through a number of vectors, such as migrating ani- mals or the hydrological cycle, but trans- port by wind may be the most common way microbes spread.
General awareness of airborne microbes predates the science of microbiology. Peo- ple took advantage of wild airborne yeasts to cultivate lighter, more desirable bread as far back as ancient Egypt by simply leaving a mixture of grain and liquids near an open window. In 1862, Louis Pasteur’s quest to dis- prove spontaneous generation resulted in the discovery that microbes were actually single-celled, living creatures, prevalent in the environment and easily killed with heat (pasteurization). His rudimentary experi- ments determined that any nutrient medium left open to the air would eventually teem with microbial life because of free-floating, colonizing cells. The same can happen in a kitchen: Opportunistic fungal and bacterial cells cause food items exposed to the air to eventually spoil.
Unknowingly, Pasteur founded the field today referred to as aerobiology, the science that studies the diversity, influence, and survival of airborne microorganisms. Sci- entists now have the ability to monitor the movement of atmospheric microorganisms on a global scale. But long-term molecular- based measurements of microbe concen- trations are still missing—such information is needed to improve understanding of microbial ecology, the spread of disease, weather patterns, and atmospheric circulation models.
Single-celled microorganisms have direct contact with the outside environ- ment through a relatively thin plasma cell membrane, which allows them to be extremely efficient metabolic machines. The trade-off is that when environmental con- ditions worsen (e.g., the disappearance of water or nutrients, increased exposure to solar radiation, etc.), that thin barrier is all that stands between life and death.
Bacteria have developed a variety of defense mechanisms that enable them to endure the physical threats associated with airborne transport. For example, one of the most successful protective strategies for some bacteria during periods of stress is to form a dormant endospore (more commonly referred to as a “spore”; see Figure 1), a phase somewhat analogous to hibernation in ani- mals. The metamorphosis from a normal par- ent cell into a dormant spore is controlled by the entire cell population (via “quorum-sens- ing” pathways). During the spore-building process, cells shrink and harden, intercellular contents are dehydrated, and an imperme- able cell wall coating is reinforced to shield the interior. The rate at which a microbe forms a spore is temperature and species dependent, and, when completed, parent bacterial cells have been transformed from a size of 3–5 micrometers down to 1 microm- eter. In many regards, a spore is a microbio- logical fortress, completely dormant with no active growth or metabolism, constructed for the purpose of indefinitely protecting DNA and conserving energy.
But spores can rapidly reactivate and resume normal cellular activity upon con- tact with water or nutrients, provided that certain biomolecules have not been dam- aged during the dormancy period. Ultravio- let (UV) radiation (particularly in the wave- length range of 200–315 nanometers) tends to be the main lethal factor for airborne microorganisms, but spore-forming bacteria have developed defenses against that prob- lem too. Many species have the ability to sta- bilize DNA strands with small acid-soluble proteins (SASP), perform active repairs to damaged macromolecules, or synthesize photoprotective pigments
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Implications
The distances microorganisms can travel before returning to the surface depend primarily on (1) the size of the cell and attached particles, (2) rates of cloud formation, and (3) wind or other meteorological forces. Most microbes larger than a few micrometers that find their way into the troposphere (below an altitude of 12 kilometers) fall out rela- tively quickly due to gravitational settling or precipitation. Numerous studies [Bur- rows et al., 2009a, and references therein] have shown that many cloud condensation nuclei (CCN) and ice condensation nuclei (ICN) responsible for climate and precipi- tation patterns are in fact airborne micro- organisms (living or dead). It is antici- pated that more dust (and microbes) will be introduced into the atmosphere with each passing year as worldwide deforesta- tion increases desert acreage. Exactly how higher concentrations of airborne micro- organisms will interact with other vari- ables that drive weather and precipitation (temperature, location, winds, and season) is another major unknown in the climate change equation.
While lower tropospheric microorganisms fall or rain out, cells that reach the upper troposphere or the stratosphere (between 12 and 45 kilometers in altitude) can stay aloft much longer and travel signifi- cantly greater distances around the globe. Although no stratospheric sampling mis- sion has been able to identify the exact source of sampled microbes or measure precise residence times at those higher alti- tudes, it is thought that volcanic eruptions, strong storms (thunderstorms, hurricanes, and monsoons), and air traffic probably all contribute to the biological content in the upper atmosphere. The residence times for microorganisms might depend on domi- nant atmospheric circulation patterns (e.g., Brewer-Dobson cycles that eventually send stratospheric air back to the surface at the poles). Micron-sized stratospheric aero- sols were observed during the 1991 erup- tion of Mount Pinatubo, with some particles remaining airborne for 5 years before fall- ing out. If used as a proxy, this event dem- onstrates the potential for stratospheric microorganisms to stay aloft for years and be globally dispersed [Smith et al., 2010]. However, to test ecological hypotheses related to this possibility, more frequent missions to the stratosphere to measure microbial origin, concentration, and viabil- ity are needed.
The potentially long residence times of microorganisms in the atmosphere are important to the health of human popula- tions, crops, and livestock, because it takes only one viable microbial pathogen to prop- agate disease. As a result, understanding airborne transport, movement, and dilu- tion of microbes is an interesting and rel- evant scientific problem. Already there are documented examples of the long-distance spread of pathogens blowing in the wind. For example, the foot-and-mouth disease virus (FMDV) has traveled across the Eng- lish Channel on airborne desert dust [Grif- fin et al., 2001]; wheat stem rust has floated from the Mississippi River valley to regions of Canada; and, more recently, scientists have identified elevated concentrations of influenza viruses in the atmosphere when dust emanating from China reached the island of Taiwan [Chen et al., 2010].
Although the ability to identify and iso- late the spread of disease has improved sub- stantially in the past few decades, the genetic diversity of modern crops is smaller than at any time in recent history. Most industrial agri- culture is based on growing monocultures— producing one single crop over a large area— often clones with identical genes. Although naturally diverse plant populations can have genetic variants resistant to disease, in agri- cultural fields the homogeneity allows for invading pathogens to conquer quickly. From a national security perspective, if context is shifted from agriculture to biological warfare, then there is a clear need to research, develop, and implement measures that mitigate or pre- vent the spread of airborne pathogens. This may include improving the ability to track the movement of airborne microbes with fixed-site monitoring, aircraft, and satellite technologies.
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