Life in Darwin's dust: intercontinental transport and survival of microbes in the nineteenth century.

Abstract

Charles Darwin, like others before him, collected aeolian dust over the Atlantic Ocean and sent it to Christian Gottfried Ehrenberg in Berlin. Ehrenberg's collection is now housed in the Museum of Natural History and contains specimens that were gathered at the onset of the Industrial Revolution. Geochemical analyses of this resource indicated that dust collected over the Atlantic in 1838 originated from the Western Sahara, while molecular-microbiological methods demonstrated the presence of many viable microbes. Older samples sent to Ehrenberg from Barbados almost two centuries ago also contained numbers of cultivable bacteria and fungi. Many diverse ascomycetes, and eubacteria were found. Scanning electron microscopy and cultivation suggested that Bacillus megaterium, a common soil bacterium, was attached to historic sand grains, and it was inoculated onto dry sand along with a non-spore-forming control, the Gram-negative soil bacterium Rhizobium sp. NGR234. On sand B. megaterium quickly developed spores, which survived for extended periods and even though the numbers of NGR234 steadily declined, they were still considerable after months of incubation. Thus, microbes that adhere to Saharan dust can live for centuries and easily survive transport across the Atlantic.

Full text

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Life in Darwin’s dust: intercontinental transport and
survival of microbes in the nineteenth century
Anna A. Gorbushina,1Renate Kort,1Anette Schulte,1
David Lazarus,2Bernhard Schnetger,3
Hans-Jürgen Brumsack,3William J. Broughton4* and
Jocelyne Favet4
1Geomicrobiology, ICBM, Carl von Ossietzky Universität,
Oldenburg, Carl-von-Ossietzky Str. 9-11, 26111
Oldenburg, Germany.
2Museum für Naturkunde, Humboldt Universität zu
Berlin, Invalidenstrasse 43, 10115 Berlin, Germany.
3Microbiogeochemistry, ICBM, Carl von Ossietzky
Universität, Oldenburg, Carl-von-Ossietzky str. 9-11,
26111 Oldenburg, Germany.
4LBMPS, Université de Genève, 30 quai
Ernest-Ansermet, 1211 Genève 4, Switzerland.
Summary
Charles Darwin, like others before him, collected
aeolian dust over the Atlantic Ocean and sent it to
Christian Gottfried Ehrenberg in Berlin. Ehrenberg’s
collection is now housed in the Museum of Natural
History and contains specimens that were gathered at
the onset of the Industrial Revolution. Geochemical
analyses of this resource indicated that dust col-
lected over the Atlantic in 1838 originated from the
WesternSahara,while
methods demonstrated the presence of many viable
microbes. Older samples sent to Ehrenberg from
Barbados almost two centuries ago also contained
numbers of cultivable bacteria and fungi. Many
diverse ascomycetes, and eubacteria were found.
Scanning electron microscopy and cultivation sug-
gested that Bacillus megaterium, a common soil bac-
terium, was attached to historic sand grains, and it
was inoculated onto dry sand along with a non-spore-
forming control, the Gram-negative soil bacterium
Rhizobium sp. NGR234. On sand B. megaterium
quicklydeveloped spores,
extended periods and even though the numbers of
NGR234 steadily declined, they were still consider-
able after months of incubation. Thus, microbes that
molecular-microbiological
whichsurvivedfor
adhere to Saharan dust can live for centuries and
easily survive transport across the Atlantic.
Introduction
Although ancient mariners experienced intercontinental
dust storms that blew west-wards across the Atlantic
Ocean from Africa (see Ehrenberg, 1849; Husar, 2004),
one of the first scientific observations of these phenom-
ena was presented by Charles Darwin (1845) who wrote
‘On the 16th of January, 1832, we anchored at Porto
Praya, in St. Jago, the chief island of the Cape de Verd
archipelago. Generally the atmosphere is hazy; and this
is caused by the falling of impalpably fine dust, which
was found to have slightly injured the astronomical
instruments. The morning before we anchored at Porto
Praya, I collected a little packet of this brown-coloured fine
dust, which appeared to have been filtered from the wind
by the gauze of the vane at the masthead. Mr Lyell1has
also given me four packets of dust which fell on a vessel
a few hundred miles northward of these islands’. These
samples were passed on to Christian Gottfried Ehren-
berg, a pioneer of aerobiology (Krumbein, 1995) at the
Royal Prussian Academy of Sciences in Berlin. Darwin
further wrote that ‘In five little packets which I sent him he
(Professor Ehrenberg) has ascertained no less than 67
different organic forms’ (Ehrenberg, 1845; Darwin, 1846).
Shortly before Ehrenberg’s death in 1876, this collection
was donated to the Prussian Academy and it is currently
housed in the Museum für Naturkunde der Humboldt-
Universität Berlin (Lazarus, 1998; Lazarus and Jahn,
1998).
Dust that originates from deserts is now known to be a
vehicle for the spread of microbial communities via natural
atmospheric pathways (Griffin et al., 2002; 2006; Kellog
et al., 2004; Weir-Brush et al., 2004; Prospero et al.,
2005). Early in the 21st century, scientific curiosity about
what dust storms may carry has been supplemented with
worries about accidental or intentional spread of contami-
nants and diseases (Brown and Hovmoller, 2002). As
Ehrenberg’s collection provides snapshots of a more
Received
*For correspondence. E-mail william.broughton@bioveg.unige.ch;
Tel. (+41) 22 3793 108/9; Fax (+41) 22 3793 009.
13July,2007;accepted6September,2007.
1‘I must take this opportunity of acknowledging the great
kindness with which this illustrious naturalist has examined
many of my specimens. I have sent (June, 1845) a full
account of the falling of this dust to the Geological Society’
(Darwin, 1846).
Environmental Microbiology (2007) doi:10.1111/j.1462-2920.2007.01461.x
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pristine world, we studied the microbiology of dust that
was collected before the globalization of industry. Here we
describe the microbiological properties of some of these
samples and discuss their possible role in global seeding
terms.
Results
Microbial characterization of the historic dust
Obviously, the Ehrenberg collection is irreplaceable, and
for this reason sampling was restricted to the most abun-
dant samples. Fortunately, sufficient material of two of the
oldest accessions (which fell over Barbados in 1812) was
available along with four others that were sent to Darwin
(Table 1). Lieutenant R.B. James, in command of his Brig
‘The Spey’, was travelling south-south-west over the
Atlantic Ocean in 1838, when he encountered a four-day
dust storm. On three separate days, James and his crew
collected four distinct samples, and sent them to Charles
Lyell, a close personal friend of Darwin. Darwin examined
the samples himself, recorded all relevant details and
eventually passed the packets of dust on to Ehrenberg.
Light- and scanning-electron-microscopy (SEM) clearly
showed that contemporary museum dust (data not
shown) is full of pollen and other particulates not found in
the ancient samples (Fig. 1B–E). To cultivate these micro-
organisms five different culture media were tried. All per-
mitted colony development, but plating out on R2A gave
rise to the largest numbers of different colonies (Table 2).
The numberof cultivatablemicroorganisms varied
between 104and 105colony-forming units (cfu) g-1historic
dust (Table 2). Even some of the oldest samples in the
Ehrenberg collection (#938 and #939b) that were col-
lected over Barbados in 1812 (see Table 1) still pos-
sessed more than 104cfu g-1dust (Table 2). Plating out
the re-wetted historic dust samples on nutrient-poor
media resulted in 48 bacterial isolates belonging to 17
different positively identified species (based on 16S rRNA
gene sequences) (Table 3). All were spore-forming bacilli
(Fig. 1I–K). Most bacteria recovered were rod-like but with
variable morphologies, with or without spores, and were
generally Gram-positive (+) (or Gram variable). By
sequencing about 750 bp of the 16S rRNA gene of the
historic dust isolates we were able to classify three prob-
able Bacillus species that it was not possible to name,
along with nine distinct species of Bacillus (Table 3).
Brevibacillis, Cohnella and Paenibacillus were also found,
all of which are also capable of forming spores.
Surprisingly, we were only able to cultivate three, very
slow-growing fungi belonging to two different species
(Aspergillus versicolor and Davidella tassiana) from the
historic dust (Fig. 1F and G; Table 4). This contrasts to
the broad palette of fungi found in museum air/dust. The
fungal isolates were closely related to normal, cosmopoli-
tan, air-borne species however (Figs 1H and 2B). The
dust aggregates themselves were extremely porous offer-
ing multiple attachment sites for microbes (Fig. 1B and E).
Bacterial cells and fungal hyphae including characteris-
tic spores (Fig. 1C and D) were attached to them
(Fig. 1B–D).
Table 1. Origins, collectors, history and descriptions of historic aeolian dust samples.
Sample description/where
collectedDate/place collectedCollector
No. in
MfNa
Material/origin
May dust (aerial) over Barbados
May dust (aerial) over Barbados
1812
1812
R.H. Schomburgk
R.H. Schomburgk
938
939b
Collected during a dust
storm that blacked out the
sun (b) over Barbados on
1 May 1812.
Dust event described in
Ehrenberg5
Passat dust, collected over the
Atlantic Ocean, onboard a ship
Passat dust, collected over the
Atlantic Ocean, onboard a ship
10 March 1838
9 March 1838, 17°43′N
25°54′W 380 miles off
African coast (not
volcanic ashes)
R.B. James, through
C. Lyell to C.R. Darwin
R.B. James, through C. Lyell to
C.R. Darwin, CRD handwriting –
sent to C.G. Ehrenberg
2894a
2895
Dust event described in
Darwin (1846): ‘. . . numerous
irregular transparent
variously coloured
particles of stone 1/1000th
of an inch square and
much fine matter’. Event
lasted 4 days (7–10 March
1838)
Passat dust, collected over the
Atlantic Ocean, onboard a ship
9 March 1838, 17°43′N
25°54′W 380 miles off
African coast
7 March 1838, 21°40′N
22°14′W 330 miles
off African coast
(most coarse fraction)
R.B. James, through C. Lyell
to C.R. Darwin, CRD passed
on to C.G. Ehrenberg
R.B. James, through C. Lyell
to C.R. Darwin and C.G.
Ehrenberg
2896(a + b)
Passat dust, collected over the
Atlantic Ocean, onboard a ship
2897a
a. Museum für Naturkunde (Natural History Museum) der Humboldt-Universität zu Berlin, Invalidenstraße, 10115 Berlin.
b. ‘Tag in Nacht verwandelt’ – original description of C.G. Ehrenberg (1845).
2 A. A. Gorbushina et al.
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Excluding the possibility of contamination of historic
dust in museums
As the Ehrenberg collection was passed from museum to
museum during Berlin’s turbulent past (Lazarus, 1998:
Lazarus and Jahn, 1998), it was essential to check
whether the re-packed samples shown in Fig. 1A and
listed in Table 1 had been contaminated in Berlin. To do
this, air and dust from the museum (collected on two
separate occasions in 2006) was analysed microbiologi-
cally and compared with isolates from the original
samples (see Tables 2–4). A number or striking observa-
tions were made, including:
(i) The density of cfu in museum dust was about 10
times higher than that found in the historical samples
Fig. 1. A sample of historic aeolian dust,
scanning electron micrographs of the dust
and microorganisms cultivated from them.
A. Original glass vial from the collection at the
Museum für Naturkunde, Berlin (vial # 2895,
collected on 9 March 1838).
B and E. Microbes on mineral surfaces
visualized by SEM (vial 2987a, coarse dust,
collected on 7 March 1838).
C and D. Fluorescent micrographs of the
samples shown in (B) after Calcofluor White
staining (vial # 938).
F and G. Slow-growing colonies of the
Davidiella/Cladosporium-like strain F6 (F) and
Aspergillus versicolor (strains F7 and F8) (G).
H. Fast-growing Aspergillus ochraceus (F12)
isolated from museum air and dust.
I–K. Bacterial colonies isolated from historic
dust. (I and J) Different morphotype of
Bacillus subtilis(I – isolate B27, J – isolate
3IIB7). (K) Bacillus licheniformis B37.
Table 2. Number of microbes [in colony-forming units per gram dust (cfu g-1)] isolated from historic aeolian dust as well as from museum dust.
Medium/probe
TSAR2A
20°C37°C 20°C 37°C
938
939b
2894a
2896
2897a
1
2
3
3.4 ¥ 102
1.1 ¥ 102
9.3 ¥ 105
2.5 ¥ 104
6.1 ¥ 104
8.2 ¥ 104
6.3 ¥ 105
2.3 ¥ 105
3.0 ¥ 103
6.8 ¥ 102
3.2 ¥ 104
4.6 ¥ 103
5.8 ¥ 104
n.d.
1.9 ¥ 105
2.8 ¥ 104
3.8 ¥ 104
1.1 ¥ 104
?
2.5 ¥ 104
9.0 ¥ 104
2.2 ¥ 105
7.3 ¥ 105
7.5 ¥ 105
4.8 ¥ 104
?
?
2.3 ¥ 104
?
1.5 ¥ 104
2.7 ¥ 105
5.7 ¥ 104
Duplicate Petri dishes containing one of two media were incubated at 20°C or 37°C for 12 days. Samples 1, 2 and 3 were collected from shelves
and storage cabinets at the Museum für Naturkunde using a sterile brush on two separate occasions in 2006. Sample sizes of historic aeolian dust
ranged from 71 to 257 mg, samples collected in the museum from 33 to 74 mg.
n.d., not detected. ?, too many to count (colonies over-grew each other).
Life in Darwin’s dust3
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Table 3. Identity and description of bacterial isolates from historic aeolian dust samples, as well as contemporary museum air and dust.
Identification Appearance in cultureGram reaction, form Sample Isolation #
Historic dust
Bacillus sp.
DQ448759 99% 1¥
EF522795 99% 1¥
DQ993299 99% 1¥
AM419753 99% 1¥
DQ993299 100% 1¥
Bacillus barbaricus
AJ422145 99% 1¥
AJ422145 98% 1¥
Bacillus cereus
EF178440 99% 1¥
Bacillus firmus
AY833571 99% 1¥
AY833571 99% 1¥
Bacillus fusiformis
DQ333300 99% 1¥
Bacillus funiculus
AB271137 98% 1¥
Bacillus licheniformis
AY871102 99% 1¥
EF059752 91% 1¥
AY871102/EF059752 99% 1¥
AY871102/EF059752 99% 1¥
Bacillus megaterium
DQ660362 99% 1¥
DQ660362 99–100% 3¥
DQ660362 99% 1¥
Bacillus pumilus
AF526907 99% 1¥
AF526907 99–100% 3¥
AF526907 100% 2¥
AF526907 99% 1¥
AF526907 99% 1¥
Bacillus simplex
DQ275178 99% 1¥
DQ275178 99% 2¥
DQ275178 99% 1¥
Bacillus subtilis
AY881638 99–100% 2¥
AY881638 99% 1¥
AY881638 99% 4¥
AY728013 99% 1¥
EF433403 90% 1¥
Brevibacillus brevis
AY591911 99% 1¥
Cohnella ginsengisoli
EF368010 93% 1¥
Paenibacillus sp.
DQ512475 99% 2¥
AM162326 96% 1¥
Paenibacillus pocheonensis
AB245386 96% 1¥
AB245386 95% 1¥
Paenibacillus panaciterrea
AB245385 99% 1¥
Paenibacillus chitinolyticus
AB021183 94% 1¥
Museum dust
Arthrobacter sp.
AJ639830 98% 1¥
Bacillus subtilis
EF532601 99% 1¥
Cocci-like Micrococcus luteus
Cocci
Cocci
Thick, white
+ rods
939b
938
938
938
938
1
3
3
4
4
Clear
- rods
938
938
1
3
Thick, mat
+ large rods
9383
Cream-orange
+ rods
938
938
1
4
Small colonies, brown Rods strangely stained
9383
Thick, white, mat
+ long rods in chain
9384
Thick, mat
+ rods central spore
938
938
939b
2896
1
4
1
1
Yellowish, mat
+ large rods, central spore
938
938
939b
3
4
1
Rough, thick
+ small rods, deforming spore
938
938
938
938
2897a
1
2
3
4
2
Mat, pigmented brown-orange
? rods
938
938
2897a
3
4
2
Thick, mucous
or
Cratered, mucous
+ large rods
938
2894a
2896
2897a
2897a
4
1
1
1
1
+ rods
Thick, yellowish
- large rods
9381
Clear, veil-like
- fine rods
939b1
Fine, clear
- rods
938
938
1
1
Mucous, cream
- long, fine rods
938
938
1
2
Mucous, clear
- long, fine rods, terminal spore
9381
Small colonies, clear
+ fine rods
9382
Cream, thick
+ small rods
Cream, thick
+ rods, spores
Yellow
Rose
Cream, mucous
+ small cocci
+ medium cocci
+ small cocci
4A. A. Gorbushina et al.
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(Table 2). Due to the limited availability of the historic
probes, statistical comparisons could not be made
however.
(ii) We were only able to isolate bacteria that are capable
of forming spores from the historic samples, whereas
museum air/dust carried a wider variety (Table 3),
including Arthrobacter sp. and Micrococcus luteus
(Micrococceae); Curtobacterium sp. and Labdella
kawkjii (Microbacteriaceae); Rhococcus sp. (Nocardi-
aceae); as well as various unidentified cocci.All these
bacteria, which are related to the Actinobacteria, are
Gram-positive, and are unable to form spores.
(iii) Only one bacterial species, Bacillus subtilis, was
common to dust of both the Ehrenberg collection and
the museum (Fig. 2A, Table 3).
(iv) In comparison with museum air/dust which contains a
Table 3. cont.
IdentificationAppearance in cultureGram reaction, form SampleIsolation #
Museum air
Arthrobacter sp.
AJ785761 97% 1¥
AY512633 99% 1¥
Bacillus subtilis
EF433403 99% 2¥
Curtobacterium sp.
AM410688 99% 1¥
Labdella kawkjii
DQ533552 99% 1¥
Rhococcus sp.
AJ244659 99% 1¥
Mucous, cream
+ small rods
Rough, white
+ large rods
Mucous, brown-rose
+ fine rods
Mucous, cream-orange
+ small rods
Orange
+ rods
Isolations #1 and #2 were performed in Oldenburg, isolations #3 and #4 (after heating to 70°C) in Geneva. Suffixes (1¥, 2 ¥, 3 ¥) represent
the number of times a particular isolate was found in the sample.
Table 4. Identity and description of fungal isolates from historic aeolian dust as well as contemporary air and dust from the Museum für
Naturkunde.
Closest GenBank similarity
(partial SSU rDNA)
Similarity
score Morphological peculiaritiesIsolated from:
Amylomyces rouxii AB250171 99%Very fast growing, white mycelia, dark sporangia Museum air
and dust
Museum dust
Museum dust
Aspergillus niger NW_001594105
Aspergillus ochraceus AF548065
100%
99%
Fast growing, black conidiophores, white mycelia
Fast growing, sand-coloured, concentric sporulation
structures (Fig. 1H)
Restricted growth, white growing edge, orange mycelia
(Fig. 1G)
White growing edge, orange mycelia, restricted growth
Fast growing, white growing edge, green sporulation
structures, orange mycelia
Yeast-like, glossy, beige submerged colony with
brown patches
Orange mycelia, flocculate, very fast spreading
Dark brown colonies, velvet surface
Aspergillus versicolor AF548069 99%939b
Aspergillus versicolor AF548069
Aspergillus versicolor/sylvaticus AF548069/8/7
100%
99%
939b
Museum air
Aureobasidium pullulans DQ471004.198% Museum dust
Chrysonilia sitophila
Davidiella tassiana DQ678022
or Cladosporium cladosporioides AF548071
Davidiella tassiana DQ678022
Morpha
99%
98%
98%
LSUb
90%
Morpha
Morpha
Morpha
100%
Museum air
Museum dust
and air
938Dark brown colonies, velvet surface, restricted
growth (Fig. 1F)
Orange, slimy, hyaline mycelia
White mycelia, dark-green sporulation structures
Brown-beige, green sporulation structures
White mycelia, dark-green sporulation structures,
Dark-green, smooth surface, abundant sporulation
structures
Dark-green, abundant aerial mycelia with spores
White mycelia, fluffy, with bluish-green sporulation
structures
Dark green, concentric sporulation zones
Greyish-white, fluffy mycelia
White mycelia, flocculate
Lecythophora mutabilis AJ496247
Penicillium sp.
Penicillium sp.
Penicillium sp.
Penicillium sp. NS051-06 DQ810190
Museum dust
Museum dust
Museum dust
Museum dust
Museum dust
Penicillium brevicompactum AF548085
Several Penicillium sp., e.g. P. italicum AF548091
99%
100%
Museum dust
Museum dust
and air
Museum air
Museum dust
Museum dust
and air
Penicillium namyslowskii D88319
Phoma sp. AB252869
Trichoderma viride AF548104
93%
98%
95–99%
a. Morphological identification.
b. Partial LSU rDNA. Shaded rows represent isolates unique to aeolian dust.
Life in Darwin’s dust5
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broad spectrum of fungi, the historic samples only
contained two species – A. versicolor and D. tassiana
(Fig. 2B, Table 4) which grew much slower than
strains isolated from museum air/dust.
(v) All these differences are listed in Table 5 where it is
apparent that the microbiological properties of the
two sets of probes are so different that one cannot
have contaminated the other.
Geochemical characterization, transport-connected
fractionation and possible origins of historic dust
Winds transport huge amounts of desert material though
the Sahara-Sahel dust corridor over the Atlantic Ocean
and often onto the Americas (Moreno et al., 2006).
During these long flights, fractionation of the air-borne
minerals occurs in which the heavier particles precipitate
0.1
Caldaterra satsumae
AB250968
Brevibacillus brevis AY591911
B11 938
3IIB11 938
Bacillus funiculus AB271137
Bacillus barbaricus AJ422145
B3 938
Bacillus megaterium DQ660362
B13 938
B38 2897a
3IIB3 938
Bacillus simplex DQ275178
3IIB10 938
Bacillus sp. DQ993299
Bacillus fusiformis DQ333300
3IB8 938
Bacillus cereus EF178440
3IB13 938
Bacillus sp. DQ448759
B12 938
Bacillus firmus AY833571
B2 938
3IIB4 938
Bacillus pumilus AF526907
B42 2897a
B25 2896
Bacillus licheniformis AY871102
B5 938
Bacillus licheniformis EF059752
B37 2897a
3IIB16 938
Bacillus subtilis EF433403
B29 2894a
B68 MA
B27 2896
B41 2897a
B53 MD
B28 2896
3IB1 938
Bacillus subtilis EF532601
3IIB7 938 (2ndmorphotype)
Bacillus subtilis AY881638
Paenibacillus sp. DQ512475
B10 938
B31 938
Paenibacillus chitinolyticus AB021183
Paenibacillus pocheonensis
B8 938
Paenibacillus sp. AM162326
B14 938
Paenibacillus panaciterreae AB245385
B15 938
100
AB245386
Cohnella ginsengisoli
EF368010
B17 938
100
100
100
83.7
79.8
100
100
75.6
74.9
74.9
100
100
100
100
89.6
100
67.0
76.2
91.2
98.792.5
99.0
97.2
92.9
61.7
100
100
94.8
71.3
89.9
99.8
99.7
94.4
A
Fig. 2. Phylogenetic relationships of dust isolates presented as neighbour-joining bootstrap trees with Kimura correction.
A. Bacteria, based on 16S rDNA sequences (~750 bp) using Caldaterra as the out-group.
B. Fungi, based on 18S rDNA (~700 bp).
Each taxonomic name is followed by its GenBank accession number. The scale indicates the average number of substitutions per position.
MA, museum air; MD, museum dust.
6 A. A. Gorbushina et al.
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0.1
F34 MA
Amylomyces rouxii
AB250171
Aspergillus versicolor AF548069
F8 939b
F7 939b
F43 MA
F12 MD/ML
Aspergillus ochraceus AF548065
F9 MD/ML
Aspergillus niger AF548064
Paecilomyces variotii AF548080
Penicillium namysslowskii D88319
F30 MD/SR
Penicillium brevicompactum AF548085
F29 MD/SR
Penicillium chrysogenum AF548086
Penicillium sp. DQ810190
F27 MD/SR
F15 MD/SR
F42 MA
Davidiella tassiana DQ678022
Cladosporium cladosporoides AF548071
F13 MD/DL
Aureobasidium pullulans DQ680682
F32 MD/DL
Phoma sp. AB252869
F39 MA
Trichoderma sp. DQ443000
F10 MD/DL
F35 MA
Trichoderma viride AF548104
F2 MD/DL
Lecythophora mutabilis AJ496247
100
99.7
93.4
99.0
94.9
98.1
83.8
100
71.3
100
70.8
95.3
99.9
60.5
99.8
100
B
Fig. 2. cont.
Table 5. Microbiological differences between historic dust and that of the Museum für Naturkunde in Berlin.
Characteristic Historic dustMuseum air/dust
Microbial density
Bacteria
Common bacterium
Fungi
Common fungus
~104cfu g-1
Twenty species, all spore-forming
Bacillus subtilis
Two species
Davidiella tassiana
~105cfu g-1
B. subtilis plus seven species, all non-spore-forming
B. subtilis
Seventeen species
D. tassiana
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first. Vertical fractionation also takes place (Husar,
2004), a process that is dependent on the water content
of the atmosphere. In other words, the dust becomes
more homogeneous the further and higher it travels.
Fractionation is reflected in its chemical and mineral
composition. Mineralogical comparisons of historical
dust with samples taken recently as well as with soils
from possible source areas were made. The four
samples collected over the Atlantic Ocean in 1838 have
comparable enrichment factors (EF) for a large number
of elements (close to 1) indicating that little fractionation
from average shale (Fig. 3) has occurred. Notable
exceptions exist however. Although enrichment of Si is
only moderate, SiO2 is the major component of all the
dust samples examined. Enrichment of quartz relative to
source materials is the most important indicator of
aeolian processes (e.g. in the genesis of loess – Schnet-
ger, 1992). As the soils of the Western Sahara contain
large amounts ofCretaceous
Fig. 3), they are the most likely source of the dust col-
lected over the Atlantic. Other possible sources including
the Hoggar Mountains (Algeria – sandstone) and the
central Chad Basin (Cameroon, Chad, Niger, Nigeria –
sand, silt, clay) do not contain significant amounts of
carbonates (Moreno et al., 2006). As the samples col-
lected in the 20th century do not contain high concen-
trations of Ag, Bi, Cu, Pb and Sn, it seems unlikely that
soils in the source areas were rich in these elements.
Several possible sources of Ag, Bi, Cu, Pb and Sn exist.
Food on ships was preserved in tins that were sealed
with solder, which probably contained all these metals.
Bronze, a Cu-Sn-alloy, was widely used onboard sailing
ships in bells, cannons, fittings, etc. Graphite pencils
were invented towards the end of the 17th century.
Flakes of lead from a pencilled note on the packet con-
taining the dust could easily have contributed this
carbonates(WS1-3,
element. Undoubtedly, one or more of these sources
explains the presence of these elements in 19th century
dust.
In contrast, the Barbados samples, which also have
similar EFs, show a distinct fractionation of minerals due
to the long-range transport across the Atlantic Ocean.
Relatively, these samples were depleted in elements
related to coarse grained K-feldspar (Ba, Cs, K, Rb, Tl) as
well as to heavy minerals like cassiterite (Sn), chromite
(Cr), monazite (Ce, La, U) and zircon (Zr). As expected of
samples collected over land, neither of the Barbados
samples was enriched inAg, Bi, Pb or Sn, lending support
to our suggestion that these elements found their way into
the 1838 samples onboard ‘The Spey’.
Survival of a Gram-positive and a Gram-negative
bacterium on dry sand
Both cultivation and SEM suggested that Bacillus mega-
terium, a common soil bacterium, is attached to historic
sand grains (Fig. 4B). As an experimental means of
testing the long-term viability of microorganisms on inert
substrates, a B. megaterium isolate from historic dust was
inoculated onto dry sand, and its survival studied at
regular intervals using both cultivation and microscopic
methods (Fig. 4). In less than 1 week, all the vegetative
cells of B. megaterium had developed spores (cf. Fig. 4A
and D), which clearly cling to the grains of sand (Fig. 4C).
As far as can be judged from this 10-week experiment,
once formed the spores remained viable (Fig. 4D).
Obviously, controlled experiments in which soils of the
Western Sahara are inoculated with genetically marked
bacteria and their dispersal across the Atlantic Ocean
followed are impossible to perform. As an alternative, we
sought a common soil bacterium that is unable to form
spores, and can therefore only survive in the vegetative
Fig. 3. Elemental compositions of historic versus modern aeolian dust along with those of soils from possible source areas (Moreno et al.,
2006). Similar enrichment factors are shown for the four samples collected over the Atlantic in 1838. The Barbados samples from 1812 also
plot close together and show a distinct fractionation of minerals caused by the long-range transport across the Atlantic Ocean.
8 A. A. Gorbushina et al.
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Page 9

state. Gram-negative rhizobia (Rhizobiales) are ubiqui-
tous symbionts of legumes including the Acacia species
that dot the Sahara/Sahel. Rhizobium sp. NGR234 is
known not only for its ability to nodulate many legumes,
including Acacia spp. (Pueppke and Broughton, 1999),
but also for an inherently unstable genome (Flores et al.,
2000), stocked with insertion and mosaic sequences
(Freiberg et al., 1997) as well as complex, repeated ele-
ments (Perret et al., 1997). It was selected as a negative
control for these reasons, but especially because a
genetically unstable bacterium would not be expected to
survive long periods of desiccation. In a similar experi-
ment to that performed with B. megaterium, the numbers
of NGR234 steadily declined with time, but the dry sand
still contained almost 104viable cells g-1after 9 weeks of
desiccation (Fig. 4E). Even more surprisingly, given the
instability of NGR234 mentioned above, these bacteria
maintained perfect symbiotic competence when cultivated
in sterile pots containing all essential elements except
nitrogen (Fig. 4F).
Discussion
Ehrenberg himself wrote ‘Probably even in 100 years
research will find interest in carefully collected (dust)
material be it on behalf of meteorology or of the study of
organic life within’ (Ehrenberg, 1851). Although the exact
beginnings of the industrial revolution are hard to pinpoint,
in 1812 they were mostly confined to the UK, and the
textile industry. Thus, dust that was blown from the
Western Sahara to Barbados early in the 19th century
was unlikely to be affected by manmade pollution. As we
were able to positively identify most of the isolates and
align them with modern-day species, the types of bacteria
and fungi cannot have appreciably changed over the
centuries. Rather, any differences that exist must repre-
sent subtle changes in genomes but unfortunately, there
is no simple way to ascertain whether and how much the
modern day microbial variants have evolved.
Other aspects of this intercontinental transport of dust
and accompanying microorganisms have changed little
too. Our geochemical data show that the most likely
source of the samples collected over the Atlantic Ocean
and Barbados is the Western Sahara. Then as now,
long-range aeolian transport strongly fractionated the
dust, resulting in depletion of coarse grains and heavy
minerals. Just as dust is depleted in certain elements and
large grains during long-range transport, adherent micro-
bial populations are also ‘fractionated’ both because of
varying sensitivities to travel and due to the attachment
abilities of individual microbes.
Fig. 4. Survival of Bacillus megaterium B13
and Rhizobium sp. NGR234 on dry sand.
A, D and E. Vertical axes – number of
bacteria in cfu g-1sand; horizontal axes –
time in weeks (w). Blue and burgundy colours
represent two separate replicates.
A. Numbers of B. megaterium as a function of
time.
B. B. megaterium-like cells on the surfaces of
a historic sand grain (vial # 2987a).
C and D. After 1 week of desiccation, spores
dominate on dry sand (C – SEM, and D –
numbers after heating to 70°C and plating
out).
E and F. Non-spore-forming Gram-negative
bacteria (here Rhizobium sp. NGR234)
survive extended periods of desiccation
without loosing their capacity to form
functional nitrogen-fixing symbioses with
legumes.
E. Numbers of rhizobia on the sand grains.
F. Vigna unguiculata inoculated with wild-type
NGR234 (centre), and NGR234 taken from
sand grains held for 9 weeks at 20% relative
humidity (pot at left – non-inoculated control).
Life in Darwin’s dust9
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Page 10

The largest, single source of dust on the planet is the
Bodélé Depression in Northern Chad (Giles, 2005; Engel-
staedter et al., 2006; Todd et al., 2007). There, a gap
between two mountain ranges funnels winds onto the
chalky white diatomaceous desert. Unlike other sources
of dust, the Bodélé is active all the year, and the diatoma-
ceous dust clouds can stretch for thousands of kilometres.
Such a source fits well with our findings of strong enrich-
ment in calcium.
Like Sneath (1962) who studied the microbiology of soil
attached to roots of ancient herbarium species and
Nicholson’s group who isolated different bacilli including
B. subtilis from granite (see Nicholson et al., 2000;
Fajardo-Cavazos and Nicholson, 2006), our analyses of
authentic samples, gathered by pioneers of modern
biology, prove beyond doubt that members of the Bacil-
liales can live for centuries. Assuming a distance of about
7500 km from the Bodélé to Miami and moderate winds of
30 km h-1, the travelling time from Africa to the Americas
would be ~10.5 days. Intercontinental-scale transport of
dust mostly occurs in the free troposphere (2–10 km
elevation) however, where the winds are much stronger
(Husar, 2004), and the journey is quicker. Rhizobia and
similar microorganisms present in the topsoil of the
Sahara/Sahel could thus probably be transported to, and
survive in the Americas.
Prospero and colleagues (2005) wrote ‘There is,
however, only anecdotal indirect evidence for the long-
range transport of viable microorganisms on interconti-
nental scales’. By trapping air over Barbados during a
dust storm, by isolating fungi from it and by correlating
African dust plumes with the appearance of microbes in
Barbados, these authors contributed several pieces to the
puzzle of intercontinental transport of microbes. Like Lyell
169 years ago, Griffin and colleagues (2006) sampled a
probableAfrican dust storm onboard a ship anchored over
the mid-Atlantic Ridge. Using polymerase chain reaction
(PCR)-based methods, they were able to identify both
fungi and bacteria, adding the latter to the puzzle. Only
by combining geochemical, microbiological, microscopic,
modelling and molecular methods to analyse almost 200-
year-old samples, were we able to show beyond doubt
that dust, which clearly originated from West Africa, trans-
ported viable microorganisms across the Atlantic Ocean,
at least as far as the Caribbean. Obviously, part of this
longevity is due to the microbes’ ability, under adverse
conditions, to quickly form spores, but we suggest that
fine inorganic dust also aids survival. Much of the historic
calcareous dust is porous (Fig. 1E) and/or possesses
convoluted surfaces that provide a refuge for microorgan-
isms, especially from desiccation and UV radiation. Once
established within the pores or between the grains, bac-
teria and fungi have probably always hitch-hiked their way
across oceans.
Satellite imaging has shown the global extent of these
storms in real time (Washington et al., 2003). As the
amounts of fine particles carried are enormous (e.g. Free,
1911; Shinn et al., 2000), this means that those regions
where dust lands are both extensively fertilized with min-
erals and inoculated with desert microorganisms. In other
words, dust has probably always played a role in global
microbial ecology. Given this constancy of transport,
induced changes in the seeding areas (Shinn et al., 2000;
Gardner et al., 2003; Weir-Brush et al., 2004) must reflect
differences in the types of microbes carried (Brown and
Hovmoller, 2002). As much of the dust carried across the
Atlantic Ocean comes from the Bodélé depression in
Northern Chad (Goudie and Middleton, 2001; Giles,
2005), we will examine whether soils from this area
contain known pathogens.
Experimental procedures
Historic dust
Posterity demands that the Ehrenberg collection, which is
both irreplaceable and of extreme scientific interest, should
only be sampled when technological progress permits a vast
increase in understanding of its contents. We felt that this was
the case and small samples were taken aseptically (in
April 2006) and subdivided for: (i) light as well as fluores-
cence microscopy, (ii) scanning SEM and (iii) microbial
characterization. In addition, the air in the museum rooms
that housed the collection was sampled on two occasions
(in April and December 2006) using a Merck MAS-100 air-
sampler (Darmstadt, Germany). On the same occasions, a
sterile brush was used to collect dust that had settled on
shelves and storage cabinets.
Microbiological techniques
Subsamples (< 50 mg) of historic dust were aseptically
weighed and suspended in physiological saline containing
0.001% (v/v) Tween 80. The tubes were shaken (1 h, 160
rev min-1, 26°C), kept overnight at 4°C, and the next day
shaken for 2 h. Portions were streaked out on 10 different
media [CzD, DG18, DRBC, ECA, Maxted, MEA, Plate
Count Agar (PCA), PYGV, R2A and Tryptone Soya Agar
(TSA)]. Afterwards, the suspensions were incubated at
70°C for 30 min; then portions were plated on R2A and
TSA. Different fungal types were studied morphologically
and further identified by partial sequencing of the nuclear
rRNA genes. Polymerase chain reaction primer pairs: (i)
nSSU97b (Kauf and Lutzoni, 2002) + NS22 (Gargas and
Taylor, 1992) or (ii) LR0R (5′-ACCCGCTGAACTTAAGC-3′)
(R.Vilgalys,http://botany.duke.edu/fungi/mycolab) + lR5
(Vilgalys and Hester, 1990) were used. Universal prokaryote
primers (27F-1385R) were used to amplify almost the
entire 16S rDNA gene fragment (c. 1400 bp) and se-
quenced by Fasteris SA, 1228 Plan-les-Ouates, Switzerland
(info@fasteris.com). Sequences were blasted against the
EMBL and GenBank accessions (NCBI BLAST: http://
www.ncbi.nlm.nih.gov/blast/Blast.cgi).
10 A. A. Gorbushina et al.
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Page 11

Microscopy
Fungal isolates were classified according to typical colonial
andconidialmorphologies
(Samson et al., 1996). Samples for SEM (Hitachi S-2300 N,
Tokyo, Japan) were air-dried, and coated with platinum
(Gorbushina et al., 2004).
usingastereomicroscope
Geochemistry
Triplicate acid digestions of 25 mg dust were analysed for Al,
Ba, Ca, Cr, Fe, K, Mn, Na, P, Sr, Ti, Y, Zn and Zr by Inductively
Coupled Plasma-Optical Emission Spectrometry (ICP-OES).
Sc was used as an internal standard for all elements except K
and Na. Inductively Coupled Plasma-Mass Spectrometry
(ICP-MS) was used to analyse the trace elements Ag, Bi, Cd,
Ce, Co, Cu, Cs, La, Li, Lu, Mo, Ni, Pb, Rb, Sb, Sn, Tl, U, V, Y
using In as an internal standard (Schnetger, 1997). Cu, Ni and
V were measured at medium resolution. All other isotopes
were analysed at low resolution which necessitated correcting
107Ag(91Zr),109Ag(93Nb),111Cd(95Mo)and114Cd(98Mo)foroxide
interference(interferingisotopesinbrackets).Oxideformation
was calculated from blanks containing only the interfering
isotope. Due to the cooled double-spray chamber used, oxide
formation for Mo, Nb and Zr was typically low (0.3–0.8%).
Analytical precision was better than 3% relative standard
deviation for all elements and both methods. Accuracy was
? 7% for Cd, Cu, K, Na, Ni, P, Pb, U, V, ? 11% for Ag and Sn
and ? 5% for all other elements. Owing to the low amount of
material available, SiO2was calculated as the difference of all
other constituents to 100%. An EF, calculated as the ratio of
the element to Al in the sample divided by the ratio of the
element to Al in shale, was used to cancel-out dilution effects
caused by, for example, carbonate and quartz (Brumsack,
2006). Average shale was used as the standard as it is a
well-proven, terrestrial mineral with high carbon content. An
EF > 1 indicates relative enrichment of the element, whereas
samples in which the element has been depleted have an
EF < 1.
Bacterial survival on sand
To test whether B. megaterium (and as a control Rhizobium
sp. NGR234) are capable of surviving extended periods of
desiccation, 1 g of quartz sand was weighed into 3 cm diam-
eter watch glasses, and autoclaved. Then, the watch glasses
containing sand were individually transferred to multiwell
plates, inoculated with or without 109cfu ml-1bacteria. After
1, 2, 4 and 10 weeks of incubation (at 26°C, first week at
100% relative humidity, thereafter at 20% relative humidity),
two replicate watch glasses representing three different treat-
ments were removed, and divided into two portions – one to
count the numbers of viable cells (and spores), the other for
observation under both the scanning electron and fluores-
cence microscope. Similar experiments were performed with
Rhizobium sp. NGR234. Symbiotic competence was tested
by inoculating Vigna unguiculata (Pueppke and Broughton,
1999).
Acknowledgements
Wolfgang E. Krumbein is acknowledged for his inspiring idea
of addressing the historial collection of C.G. Ehrenberg and
bringing together people responsible for both the custody of
the collection as well as microbial, geochemical and molecu-
lar analyses. We thank Yin-Yin Aung, Arlette Cattaneo and
Dora Gerber (Université de Genève) for their help with many
aspects of this work, Christa Krüger and Ingrid Jonetzko (Carl
von Ossietzky University) for collating the figures, Klaus-
Peter Götz (Humboldt University) for his support, W.J. Deakin
and X. Perret for their comments on the manuscript. Financial
assistance was provided by the Université de Genève, the
Fonds National Suisse de la Recherche Scientifique (projects
3100AO-104097/1 and 3100AO-116858/1), and the Ministry
of Science and Culture of Lower Saxony. André Puiz
(Muséum d’histoire naturelle de la Ville de Genève) and
Laurent Farinelli (Fasteris SA) helped with scanning micros-
copy and sequencing respectively.
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