GEOPltYSICAI,
RESI;At•,Ct I I,I¾I"I'I:!RS, V()I,. 28, NO. 2• I•AGI•-œS
239-242, ,IANUARY
15, 2001
Bacterial growth in supercooledcloud droplets
Birgit Sattier
Instituteof ZoologyandLimnology,Universityof Innsbruck,Austria
Hans Puxbaum
Institutefor AnalyticalChemistry,ViennaUniversityof Technology,Austria
Roland Psenner
Instituteof ZoologyandLimnology,Universityof Innsbruck,Austria
Abstract. It is well known that the atmosphereis a conveyorof
microorganisms,and that bacteria can act as ice or cloud
47ø03'N). The observatoryitself is suppliedwith electricityand
condensation nuclei, but clouds have not been considered as a
Cloud water sampleswere taken with an active collectorfor
hydrometeorsconsistingof a single stage impactorbacked by a
largewind shield.Cloud watersampleswere kept frozenin sterile
polyethylenebagsuntil analysis.
Aerosols were sampled with a Quartz fiber filter (47mm,
Pallflex TISSUQUARTZ 2500QAT-UP). The collected air
site whereorganismscan live and reproduce.Here we showthat
bacteriain clouddropletscollectedat high altitudesare actively
growingand reproducingat temperatures
at or below 0øC. Since
-60% of the earth surface is covered by clouds, cloud water
should be considered as a microbial
habitat.
thus not a source of exhausts.
volumeswereabout30 to 32m',the usedflow ratesabout45 i
min-•. To excludeanycontamination,
fieldblanksweretaken
1. Introduction
which were sampledin the same way as aerosol samplesbut
samplingtime was limited to 30 seconds.Filters were storedin
Dispersalof bacteriaandevenlargerorganisms
by windhas petri-disheswith a parafilm-capat 4øC.
been known since long time (Gisldn, 1948, Gregory, 1967,
Surfacesnowsampleswere takenby collectinga snow layer
Schnell and Vali, 1972). Living microorganismshave been of approximately10cm thicknesswhich was put in a sterile
collectedevenin the stratosphere
(Imshenetsky
et al., 1978), and polyethylene bag. Samples were handled with a sterilized
there is one observationthat bacteriamay divide on airborne polyethyleneshoveland kept frozen until analysis.All materials
particles
(Dimmicket al., 1979).Studies
onbiological
particles
in which cameinto contactwith clouddroplets,snow,hail and rime
cloud water, however, are scarce(Casareto et al., 1996) and have been carefully washed with hydrochloricacid and rinsed
bacteriain the atmosphere
havebeencollectedmostlyby the use with sterileparticlefree distilledwater (PFDW).
of air samplers
(Matthias-Maser
anddaenicke,1992).Recently,
Bacterial abundance,morphologyand biomass.Thirty ml of
Hamiltonand Lenton(1998) hypothesized
that marinealgaeand samplewere fixed with prefiltered(0.2[tm) formalin to a final
bacteria induce water condensation and ice nucleation in order to
concentrationof 2% v/v. Twenty ml were filtered onto Poretics
improvetheir dispersaland transportby the atmosphere,
thus filters (0.2[tm pore size), stainedwith the fluorochromeDAPI
influencing
not only distanceanddestination
of thejourneybut (4' 6-diamidino-2phenylindole)at a final concentrationof 0.2%
also the world climate(Gislen, 1948). Airbornemicroorganisms v/v accordingto Porter and Feig (1980) and countedin a Zeiss
were termed "spora",assumingthey were inert or inactive, Axioplan epifluorescence
microscope.Image analysiswas done
consequently,the atmosphericenvironmentwas considered with an Optotronics ZVS-47EC camera and LUCIA_D
primarilyasa mereconveyor,
although
rainandfogwaterrichin (LaboratoryImaging, Prague, Czech Republic) accordingto
nutrientsmay providea good substratum
for microorganismsPosch et al. (1997). Biomasshas been estimatedas describedin
(Herlihyet al., 1987,Fuzziet al., 1997).The relativelycleanand Loferer-KrOfibacher
et al. (1998).
coldatmosphere
of highaltitudes,however,wasnot regardedasa
Bacterial production. Cell multiplicationrates and protein
suitable place for bacterial growth. We were, therefore, synthesiswere measuredaccording to Simon (1990) with
astonishedto find actively growing bacteria suspendedin
supercooled
clouddroplets.
[methyl-3H]thymidine
(specific
activity70-90Ci mmol
-•) and
•4
[ C]leucine(specificactivity 310 mCi mmol
-• - both
2. Methods
RadiochemicalCentre,Amersham,England). Cloud water was
diluted (1:7) with sterileparticlefree distilledwater in order to
measuretriplicatesamplesand 1 blank. Twenty ml were marked
Sampleswere collectedin late April and early May 1997 at
the Sonnblick Observatory(SBO), a meteorologicalstation
located on top of mount Sonnblick (3106m a.s.l., Austria,
Salzburg) in the main ridge of the Austrian Alps (12ø57'E,
with[3H]thymidine
(5 nmol1-1)
and[14C]leucine
(20nmol
1-1)
and
Copyright
2001bytheAmericanGeophysical
Union.
3. Results
incubatedfor 20 hours at 0øC in a high precisionwaterbath
(HAAKEm). Bacterial carbon production was calculated
accordingto SimonandAzam (1989).
and Discussion
Clouddropletscollectedat SBO containedca. 1.500 bacteria
Papernumber2000GL011684.
ml-• (Table1), whereas
the abundances
in snowandgraupel
0094-8276/01/2000GL011684505.00
239
240
Table1. Abundance,
meancellsize,biomass,
3H-thymidine
and•4C-leucine
uptakerates,carbon
production
andgeneration
t•mesof
bacteriafrom cloudwater (CW), snow and graupel samples collectedat SonnblickObservatory(3.106m a.s.I.) in April and May 1997; all
rates have been measured at 0øC; n.d. = not detectable. CW ... cloud water
Sample
Date
BacteriaCellsize Biomass 3H-thymidine 3H-thymidine•4C-Leucine Carbon Generation
uptake rate
uptake rate per
uptake rate
production
time
cell
1997
(Nml'•)
(IJm
3) (ngC I-•)
(fmolI'• h'•)
(10-24molh'•
cell-1)
CW 1
29 April
1,180
0.159
CW 2
30 April
2,470
CW 3
1 May
920
CW 4
29 April
CW 5
(fmolI-• h-•) (ngC I-• h-•)
(days)
37
4.8
4.07
263
0.61
0.030
32
4.2
1.70
391
0.91
8.5
0.025
13
1.2
n.d.
126
0.29
19.5
790
0.029
9
1.1
1.39
153
0.36
10.4
29 April
1,090
0.038
14
1.1
1.01
505
1.17
14.3
CW 6
29 April
1,490
0.048
25
1.9
1.28
278
0.64
11.8
CW 7
29 April
2,060
0.037
25
2.4
1.17
139
0.32
12.4
3.6
CW 8
30 April
1,640
0.068
30
n.d.
n.d.
104
0.24
n.d.
CW 9
1 May
1,060
0.110
23
3.0
2.83
46
0.11
5.1
CW 10
4 May
1,620
0.036
28
n.d.
7.41
131
0.30
n.d.
CW 11
5 May
1,160
0.019
13
1.6
1.38
289
0.67
10.5
CW 12
6 May
2,080
0.026
33
2.4
1.15
n.d.
n.d.
12.5
Mean
(CW)
1,463
0.052
24
2.4
2.34
221
0.51
10.9
Snow 1
27 April
11,200
0.027
168
9.2
0.82
76
0.18
17.6
Snow 2
27 April
10,900
0.018
120
7.8
0.72
113
0.26
20.2
Snow 3
29 April
11,100
0.033
233
2.6
0.23
n.d.
n.d.
61.7
Snow 4
29 April
12,400
0.046
273
1.2
0.097
n.d.
n.d.
107.5
Snow 5
29 April
9,500
0.029
143
4.5
0.47
n.d.
n.d.
30.5
Snow 6
30 April
10,500
0.051
263
2.2
0.21
n.d.
n.d.
68.9
Snow 7
30 April
13,100
0.026
183
2.2
0.17
45
0.10
86.0
Mean
(snow)
11,243
0.033
198
4.2
0.39
78
0.18
56.1
Graupel 1
29 April
6,900
0.025
90
3.2
0.46
n.d.
n.d.
31.1
Graupel 2
29 April
11,500
0.035
173
2.1
0.18
79
0.18
79.1
Mean
(graupel)
9,200
0.030
132
2.7
0.33
79
0.18
55.1
collectedat the same occasionwere five to ten times higher.
Nonetheless,theseare amongthe lowest abundancesfound in
aquaticenvironmentsand comparableto unpollutedgroundwater
(Al)qeider et al., 1997). The uptake rates of tritium labelled
thymidineinto DNA, which is generallyused to measurecell
Which naturalfactorscouldlimit bacterialproductivityin the
atmosphere.'?
Air temperatures
duringsamplingwere between-4
oceans.
temperatures.
and-9øC, and it is well known that cloud water can remain
supercooled
at temperatures
of-15øC or even less(Pruppacher
and Klett, 1978; Rosenfeldand Woodley,2000). We have no
growth,
showed
average
valuesof 1.1to 4.8 10-ismol1-1h'l. direct measurementsof bacterial uptake rates at in situ
Although
measured
at 0øC,uptake
ratespercell(2.34-10-2]mol temperaturebecausethe labelledsubstratescan only be usedin
thymidine
h'l cell'l) in cloudwaterwereas highas in typical liquid water. Snow and ice bacteriafrom a high altitudesite in
lakewater samples(Fig. 1). Accordingly, generationtimes in Tyrol showeda 1.5 fold increasein growth rates if samplesare
cloudwaterrangedfrom 3.6 to 19.5 days,comparableto thoseof gradually warmed from ambient temperaturesof 0øC to 5øC
phytoplankton
in the ocean,i.e. aboutoneweek(Falkowskiet al., (Sattier, unpublisheddata). Thus, in situ growth rates in
1998).Theincorparation
of •4C-leucine
showed
valuesof upto supercooleddropletsmay be only 50-70% of thosemeasuredat
0.5 pmol1-1h'l (Table1). Bacteria
in cloudwaterproduced
on 0øC(Table 1). Priscuet al. (1998) who studiedprokaryotesliving
average
12ngC 1-1d-1,witha maximum
of 28 ngC 1-• d'l. They at temperaturesaround 0øC in the ice of permanentlyfrozen
were generallysmallerthan 0.5 [tm in length,the averagecell Antarctic lakes, found that low temperaturesalone and freezevolume
was0.052!am
3,corresponding
to 17fg C cell-1.Thisisa thaw cyclesdo not seemto inhibit microbialgrowth.As shown
typical value for marineand freshwaterecosystems,
whereasthe by Felip et al. (1995) for the winter coverof alpine lakes,high
biomasswas up to threeordersbelow valuesfound in lakesand substrateconcentrations
can partly compensatethe effect of low
241
surfaceof a highmountainlakewerequitedifferentfromthosein
slush layers and in lakewater(Alfreider et al., 1996). It has
lOO
•
lO
become evident that much of the microflora in remote environ-
ments is transportedby air currents(Marshall, 1996, 1997,
Psennerand Sattler, 1998) providingan importantway of
•'
Ol
colonization
.•
oOl
•
oOOl
o OOOl
,
10 2
10 3
10 4
10 5
10 6
,
10 ?
Bacterial
abundance
IN ml'1]
ß
O
ß
?
ß
O
e
•
•
of otherwise isolated environments. Taxonomic
studiesaboutairborneorganisms
are very scarce- Sandset al.
(1982) identifiedPseudomonas
syringaewhichis probablythe
most abundantice nucleatingbacteriain air, rain and hail. An
._
V•nter cover of Gossenk011esee,Austna, 2 417m
Lake water of Gossenk011esee
(Sattier 1996)
Lake water of P•burgerSee, Austria,913m
(Sattier 1993)
Lake water of Ta• Hu, China (Sattier 1993)
Cloud droplets of SonnbhckObservatory,
Austria (this study)
Snow from SonnbhckObservatory(th•sstudy)
Snow from Gossenk011esee(Sattier 1996)
Ice commud•es•n East Lobe Bonney,
Antarcbca(Sattier et al unpubhsheddata)
Average Lake water Thy uptakerate per cell
Figure1. Bacterial
abundance
andSH-thymidine
uptake
ratesin cloudwater,freshlyfallen snow,and slushlayersof
lake ice measuredat 0øC, and in lakewater measuredat in situ
temperatures(Sattier, 1993, 1996).
Solidline:meanthymidine
uptakeratepercell(1.96 '10-2]
molh-])in lakewater
atinsitutemperatures.
earlier studydealingwith microorganisms
in hailstonesby
Mandrioliet al. (1973)identifiedvariouscolonies
of fungiand
pollen - the remainderwas a singletype of gram-positive
streptococcus.
The number of bacteria observed in snow was around 10.000
ml-], Table1, andan estimate
for a typicalnumberof snow
crystalsforming 1 ml water is around 10.000 (Pruppacherand
Klett, 1978, Mishima and Stanley, 1998). From this and current
views aboutthe role of bacteriain the atmosphere(Lenton, 1998,
Gisldn, 1948, Hamilton and Lenton, 1998) it appearslikely that
the observedbacteriawere actingas ice nuclei. Schnell statedin
1976 that bacteriaattachedto mineralparticleswere responsible
for ice nucleation rather than the mineral particles itself as
Tscherwenkaet al. (1998) argue.A closeup look on our bacterial
observations,however, revealed that bacteria are frequently
attachedto particles- which indicatesthat there is possiblyno
contradictionbetweenour andthe previousinterpretations.Since
thenumber
of bacteria
in cloudwater(-1500ml-], Tab.1) is far
Thenutrient
conditions
of cloudandrainwaterandfleshly lower than the averagenumberof cloud dropletsforming 1 ml
fallen snow(Brantnetet al., 1994) can be evenbetterthan in water(-2.10•) it appears
thatbacteria-although
growingin
many freshwaterlakes. Cloud water at the SBO containedrather
highamounts
of organic
acids,i.e. upto 0.3 mg1-] of formiate
cloud droplets - are not an important source of cloud
condensation nuclei.
and2.1mg1'] of acetate
(Brantnet
etal.,1994),butalsoseveral The consistentlydifferent numbers of bacteria in cloud
[tg1-] of alcohols,
suchasdodecanol,
tetradecanol,
hexadecanol
dropletsand snow seemto dependon the conditionsin "mixed"
and octadecanol
(Lirabeckand Puxbaum,2000). CI 2-C18 supercooledclouds- where supercooledcloud dropletsand ice
alcohols
havebeenascribed
to bacterialsources
(Simoneit
and crystalscompetefor the available water. In this process- the
Mazurek, 1982), and bacterial utilization of formic and acetic
seeder/feedermechanism- the higher vapor pressureof liquid
acidin rainwaterwasshownby Herlihyet al. (1987).It is not cloudwateras comparedto the vaporpressureoverthe ice phase
clear, however, whether alcoholsin cloud water and snow are
fayourscrystalgrowthon the expenseof droplets.Later, during
produced
or usedby microorganisms.
Hexadecane,
for instance, the fall of the ice crystals,cloud dropletsare scavengedby the
canbe usedby Arthrobacter
sp. whichproduces
hexadecanol,crystalsformingaccretions(Pruppacherand Klett, 1978, Bryant,
andArthrobacter
sp.isoneofthemostabundant
andactive
types 1997). Magonoand Lee (1973) observedin snowstormsin Japan
of bacteriain dry soilswhichcouldbe suspended
by wind. that ice water concentrations were around 10 times lower than
Another
possible
candidate
isRhodococcus
sp.,a psychrotrophic
liquid cloud water. Thus a liquid water content(LWC) of 0.5
bacterium
whichis ableto degrade
variable
chain-length
alkanes g/m3 would imply-750 bacteriaper m3 incorporatedin cloud
at low temperatures
(Whyteet al., 1998). The concentration
of water and an ice water concentrationof 0.05 g/m3 would imply
alcohols,
however,
largelyexceeded
bacterial
cloudbiomass,
thus -550 bacteriaper m3 incorporatedin ice particles(i.e. snow).
suggesting
a terrestrialsourcefor alcohols,but it indicatesthat
Cloud systemsbearingdropletsof 10 to 100 [tm diametercan
persistfor hoursor longerin the atmospherealthoughthe lifetime
farlarger
thantheamount
needed
tosupport
bacterial
growth
of individual cloud droplets is normally much lower. If we
ThepH, whichcouldseverlyimpedebacterial
metabolism, assumea residencetime of one day and an ambienttemperature
wasratherfavourable
in all samples,
withvalues
between
pH 5.4 of 0øC,bacterialbiomassin clouddropletscan increaseby up to
the concentration
of dissolved
organiccarbonin cloudwateris
and6.8, and dissolved
organiccarbonconcentrations
canreach 20%(Tab.1). A meancloudwatercontent
of 0.3 g m-3anda
several
mg1-], astypicalforlakewater
conditions.
Naturalsolar cloudthickness
of 2 km yields•600 g waterm'2, although
radiation
athighaltitudes
maystrongly
inhibitmicrobial
activity Rosenfeld
and Woodley(2000) foundnearly2 g m-3 of
(Sommaruga
et al., 1997),but cloudsthemselves
canprovide supercooledliquid cloud water in deep convectivecloudsof a
shading
fromdamaging
UV radiation.
continentalstorm.If our measurements
of bacterialproductionin
Thesource
of airborne
organisms
is stilluncertain
butthey clouddropletswererepresentative
andconsidering
the percentage
mayoriginate
fromplantsurfaces
(Lenton,1998),watersurfaces of cloudedsky,i.e. 60% of the earthsurface(Bryant, 1997), we
or soilsandfromreplicating
bacteria
withinclouds.
Transport
of
air masses
fromthewell mixedboundarylayerto the highAlpine
siteshasbeenfrequentlyobserved,in particularduringthe warm
season(Tscherwenka
et al., 1998). A previousstudydoneby in
situ hybridisationwith RNA probesclearlyshowedthat bacterial
communities in freshly fallen snow collected on the frozen
caninfer a bacterialproductionof organiccarbonin the rangeof
1-10 Tg carbonper year.This is a smallnumbercomparedto the
primary productionin the oceans(Falkowski et al., 1998) of ca.
45-50PgC yr-] ortotheemissions
of organic
carbon
(ca.1 PgC
yr-]).An interesting
point,however,
is whether
airborne
bacteria
carryout or affectkey processes
in cloudchemistryor physics.
Concluding,we considerthe atmospherenot only as a
conveyorof organisms
but as a sitewheresignificantmicrobial
processes
cantakeplaceduringtransport.How stronglybiologic
processes
influencetransformations
of organicand inorganic
components
of the atmosphere
has still to be explored,but
bacteriagrowanddivide,andproduceproteinsanda plethoraof
Magono,C. and C.W. Lee, d. Meteorol.Soc.Japan.,51,176,
1973.
Mandrioli, P., G.L. Puppi, and N. Bagni, Distributionof
microorganisms
in hailstones,
Nature,246, 416-417,1973.
Marshall, W.A., Biologicalparticlesover Antarctica,Nature,
383, 680, 1996
Marshall, W.A and M.O. Chalmers,Airborne dispersalof
antarcticterrestrialalgaeand cyanobacteria,
Ecography,20,
metaboliteswithin the atmosphere,even at temperaturesof or
585-594, 1997.
below 0øC. The limiting stepfor microbialprocesses
in cloud Matthias-Maser, S. and R. Jaenicke, in Nucleation and
droplets may thus be neither temperaturenor nutrient
Atmospheric
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413-415,DeepakPublishing,
Hampton,Virginia,1992.
concentrations
but their residencetime in the atmosphere.
After
betweenliquid,
deposition,airbornebacteriawill influencethe composition
of Mishima,O. andH.E. Stanley,The relationship
supercooled
andglassy
water,Nature,396,329-335,1998.
microbialassemblages
in snow,soils,lakewaterandoceans,and Porter,
K.G. andY.S. Feig,The useof DAPI for identifyingand
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Acknowledgements.We wish to thank Andy Limbeck,Christina
Gr011ert and Werner Tscherwenka for field work and discussions. Heidi
Bauer earnsa thanksfor intensiveliteratureinvestigations.
Furthermore
we are in debt of Alois Halswanter,Anton Wille, Tom Battin, Thomas
Posch,andReinholdP0derfor helpfulideas.The studywassupported
by
the AustrianScienceFoundation(FWF Project11685-MOB).
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