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Clouds Provide AtmosphericOases for Microbes
Estimated to total 10
19
cells, microorganisms in clouds appear sufficientto affect physicochemical processes in the global atmosphere
Pierre Amato
W
hen thermodynamic conditionsprove favorable in the atmo-sphere, water vapor condenseson aerosol particle surfaces,forming micrometer-sized drop-lets or ice crystals constituting clouds. Eventhough clouds gather only 0.03% of the freshwater on Earth, they are important componentsof climate, acting as filters to solar and infraredradiationenteringandleavingtheplanet.More-over, they provide a multiphasic mixture of liq-uid,solid,andgastosupportchemicalreactionsaffecting the composition of the atmosphere.When scientists began collecting air samplesathighaltitudesfrommountains,balloons,and,later, airplanes, they learned that living bacteriaand fungi are present within the atmosphere.Because condensed water can protect airbornemicrobial cells against desiccation, aerobiolo-gists consider clouds atmospheric oases. On aglobal scale, the total number of microorgan-ismsincloudsreachesabout10
19
.Althoughthisestimate seems low compared with the 10
26
microorganisms estimated to occupy lakes andriversandtothe10
29
microorganismsinoceans,microbial levels in clouds appear sufficient toaffect physicochemical processes in the atmo-sphere. Additionally, clouds could play a majorrole in disseminating microbes over long dis-tances.
Clouds Host Metabolically Active Cells
The concentration of microorganisms incloudstypicallyrangesfrom10
2
to10
5
cellsper milliliter. Although only a small frac-tion—typically less than 1%—of such cellscan be recovered by culture, bacteria ac-tively grow in clouds, according to BirgitSattler and colleagues of the University of InnsbruckinAustria.Becauseactivegrowthentails the uptake of nutrients, living cellspresumably change the chemistry in clouds,acting through processes that are likelydriven by sunlight and that generate freeradicals, notably hydroxyl and superoxide,OH
and HO
2
, respectively.Clouds are acidic, with pH ranging from3to7,andhaveconductivityvaluesrangingfrom 1 to 300
S cm
1
. This chemistryresults from compounds from gas and aero-sols dissolving into the aqueous phase of clouds,andvarieswithunderlyinglocalter-
Summary
•
Although low in number compared to the 10
29
microbes estimated in oceans, the 10
19
micro-bial cells in clouds are sufficiently plentiful toaffect the atmosphere.
•
Bacteria in clouds actively metabolize nutri-ents—for example, about 1 million tons of or-ganic carbon per year—but only about 1% of such cells can be cultured.
•
Even though clouds play an important role dis-persing microbes over long distances, they ap-parently do not serve as long-term microbialreservoirs.
•
In theory, a single ice-nucleating bacteriumwithinacloudcaninduceprecipitationandthuscause its own deposition.
•
Little is known about rates of emission of bac-teria from surfaces into the atmosphere, andsuch data are not easy to generate.
Pierre Amato is a staff scientist at the Institut de Chimie de Clermont- Ferrand, Clermont- Ferrand, France.
Volume 7, Number 3, 2012 / Microbe
Y
119
 
restrial sources. The main ions within clouds—nitrates, sulfates, chloride, ammonium, andsodium—are present at micromolar concentra-tions. Cloud water also contains organic com-pounds, including carboxylic acids, aldehydes,and alcohols, from natural and anthropic ori-ginsthatbacteriacanuseasnutrients.Addition-ally, other elements, including phosphorus,iron, copper, and magnesium, are dissolvedwithin cloud water and can sustain microbialmetabolism.In 2003, my colleagues and I in Clermont-Ferrand, France, began sampling cloud waterfrom samples that we collect along the puy deDoˆmesummit,whichis1,465mabovesealevel.We are studying interactions between organiccompounds and microbes in those samples, ad-dressingwhethercloudbornemicrobesaffectat-mospheric chemistry.To estimate biodegradation rates in clouds,we constructed microcosms in solution whosechemical compositions approximate what oc-curs in cloud water. We inoculated these micro-cosms with microorganisms isolated from cloudwater, and then monitored their behavior aswell as changes in organic compounds by
1
Hand
13
CNMRandbyionchromatography.Ourobservations surprised us: In some cases, mi-crobes metabolize organic compounds at ratessimilar to or higher than they are changed bysimulated solar light, on the order of 10
11
M s
1
.The relative contributions of biology andphotochemistry vary for each chemical species,ranging from 0 to 100%. Where the two typesof reactions combine, the rates are additive, asis the case in natural situations. Microorga-nisms catalyze some reactions exclusively—forinstance, reducing formaldehyde to methanol.However, cloud-borne microbes do not take upoxalate, which was degraded exclusively photo-chemically.In addition and perhaps more importantly,microorganisms partly shut off photochemicalreactions by lowering the concentration of hy-drogen peroxide, the major source of free radi-cals in the atmosphere, likely degrading it viaoxidative stress enzymes and antioxidant spe-cies. Although we continue to refine our esti-mates, we estimate that microorganisms inclouds metabolize about 1 million tons of or-ganic carbon each year on a global scale.
Clouds Disseminate Microbes,Which Can Drive Precipitation
Eventhoughindividualmicrobialcellsareactivein cloud droplets, microbial communities likelydo not form within this, for them, transitoryenvironment. Thus, clouds are not long-termmicrobial reservoirs, even though clouds canplay an important role dispersing microbes overlong distances. Indeed, wet deposition is themain process leading to removal of 1-
m parti-cles, the size range of bacteria, from the atmo-sphere, and clouds likely are the best “shuttles”for moving airborne microorganisms back tothe ground.To disseminate by air means that microbesmust survive the harsh conditions that they en-
F I G U R E 1
The 1,465-m puy de Doˆme mountain, situated near Clermont-ferrand in France, has hosted an atmospheric observatory for more than acentury; it is also being used as a sampling site and field laboratory for studying microorganisms in clouds.
120
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Microbe / Volume 7, Number 3, 2012
 
counter in the high atmosphere, including lowtemperature, desiccation, high levels of UVlight, repeated freeze-thaw cycles, and osmoticshock. Hence, it is not surprising that microbesin clouds resemble those recovered from otherharsh environments where such stresses occur,includingalongplantsurfacesandglaciers.Twogenera of bacteria frequently recovered alivefrom cloud water collected at the puy de Doˆmesummit are
Sphingomonas
spp. and
Pseudo-monas
spp. These hardy, cloud-borne microbesuse the atmosphere and clouds as conveyorsto reach distant terrestrial environments.The
Sphingomonas
species are oligotrophic
Amato: Head in the Clouds Investigating Microbes,Feet Treading Forested Mountains
Friends of Pierre Amato tell himthat he has his head is in theclouds. “It is teasing, of course,but at the same time it relates tosomething poetic, and maybeeven romantic in some ways,” hesays, adding a more serious note:“Increasing concerns related toepidemiology and bioterrorismhave aroused a particular atten-tion to the atmosphere as a con-veyor of microbes, and clouds ap-pear to be essential.”Amato, a staff scientist at theInstitut de Chimie de Clermont-Ferrand in France studies micro-organisms in clouds. “My workshould lead us to better under-stand and predict the formationof clouds, their behavior, and thechemicalprocessestakingplaceinthese floating aquatic environ-ments,”hesays.“Whatmotivatesme the most is the role these envi-ronments may have as filters tothe long-distance disseminationof organisms. Some can survive,somecan’t,andIbelievethis. . .iscontributing, to the evolution of microorganisms.”Amato,33,grewupnearwherehe works, in a small village calledBonnac, whose population totalsabout30.“Thisis,tomymind,anidyllic place, with a small riverrunning through it, and sur-rounded by mountains, forests,and meadows, including sheepand cows managed by shepherddogs,” he says. His parents, nowin their 60s, moved there duringthe 1970s, seeking a home “farfromthecivilizedworld,”hesays.His father was born in Tunisia of Italian parents who moved toFrance in the 1950s. He has anolder sister and a younger brother.HismothertaughtFrench,andhisfather held a variety of jobs, in-cluding artisan and forest man-ager, and later began doing socialwork. “My mother was a teacherof French in high school, and sheloves literature and books in gen-eral, so we had tons of books athome,” Amato says. “My fatherused to listen to good music mostof the time, so I had [an early]musical education.”Living in that village “certainlyshapedmyvisionoftheworldandof the place of humans on Earth,”Amato says. As a child, he spentconsiderable time outdoors, espe-cially around the nearby riversand lakes. “I had to have a realaquatic bestiary at home: sala-manders, crawfishes, a frog thatI kept more than a year feedingit with flies before letting it go,and many kinds of fish, includingeven trout and a baby pike that Iwatched growing up,” he says.He still hikes the mountains nearhis home, goes fishing, gathersforest mushrooms, and continuesto “dig into lakes and rivers tolook for their inhabitants.”Amatoreceivedabachelor’sde-gree in science in 1996 from theLyce´e Lafayette, Brioude, andthen a series of graduate degreesleading to a doctorate in 2006,all from Blaise Pascal Universityin Clermont-Ferrand. Amato thenmoved to Louisiana State Univer-sity in Baton Rouge to do post-doctoral research in 2007–2008,studying microbial activity in ice,including an excursion to the DryValleys, Antarctica. He spent thenext two years studying land-scape, microclimate, and dynam-ics of microbial populations of plants at the French Food Re-search Institute in Avignon.While a Ph.D. student, Amatorecalls taking samples fromclouds from an observatory at thesummit of the Puy de Doˆme, avolcano near Clermont-Ferrand.“There are places like this thatyou know have a history,” hesays.“Thewind,thefog,thecold,the ruins of the Roman temple of Mercury just in front of the build-ing, the inside of the building,with old furniture and an olddrawing of Emile Alluard, the di-rector of the observatory at theearliest stages, made it very mysti-cal. I guess this contributed to mydesire to know more about whatwas going on in those clouds.”
Marlene Cimons
Marlene Cimons lives and writes inBethesda, Md.
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