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Environmental Microbiology Reports (2015) 7(3), 388–394
doi:10.1111/1758-2229.12261
Discovery and microbial content of the driest site of
the hyperarid Atacama Desert, Chile
Armando Azua-Bustos,1,2* Luis Caro-Lara3 and
Rafael Vicuña1
1
Faculty of Biological Sciences, Department of
Molecular Genetics and Microbiology, Pontificia
Universidad Católica de Chile, Santiago, Chile.
2
Centro de Investigación Biomédica, Universidad
Autónoma de Chile, Santiago, Chile.
3
Universidad Santo Tomás, Santiago, Chile.
Summary
The Atacama Desert is the driest and oldest desert on
Earth. Eleven years ago, the Yungay region was
established as the driest site of this hyperarid desert
and also close to the dry limit for life on Earth. Since
then, much has been published about the extraordinary characteristics of this site and its pertinence as
a Mars analogue model. However, as a result of a
more systematic search in the Atacama here, we
describe a new site, María Elena South (MES), which
is much drier than Yungay. The mean atmospheric
relative humidity (RH) at MES was 17.3%, with the RH
of its soils remaining at a constant 14% at the depth of
1 m, a value that matches the lowest RH measurements taken by the Mars Science Laboratory at Gale
Crater. Remarkably, we found a number of viable bacterial species in the soil profile at MES using a combination of molecular dependent and independent
methods, unveiling the presence of life in the driest
place on the Atacama Desert reported to date.
Introduction
The Atacama Desert is the driest and oldest desert on
Earth (Hartley et al., 2005; Azua-Bustos et al., 2012). A
groundbreaking report published 11 years ago led to the
recognition of the Yungay region of the Atacama Desert as
one of the driest places on Earth harbouring extremely
low contents of culturable heterotrophic bacteria and
also a pertinent Mars analogue model (Navarro-González
et al., 2003). Thereafter, many studies further described
Received 12 October, 2014; revised 2 December, 2014; accepted 8
December, 2014. *For correspondence. E-mail [email protected];
Tel. +56229573881; Fax +56229573881.
© 2014 Society for Applied Microbiology and John Wiley & Sons Ltd
the characteristics of Yungay, (Maier et al., 2004; Neilson
et al., 2012) and nearby areas (Azua-Bustos et al., 2009;
2010; 2011; 2014; Paulino-Lima et al., 2013).
However, the original selection of Yungay was not the
result of a systematic search of the most arid sites of
the Atacama, but from logistical reasons (Chris McKay,
pers. comm.). Therefore, we explored the Atacama in
search of the legitimately most hyperarid places by
looking for sites displaying a combination of three key
environmental factors: (i) the regular absence of clouds,
(ii) the regular absence of fogs and (iii) the regular
presence of wind.
Results and discussion
Atmospheric temperature/relative humidity (RH) loggers
set in a 4-year interval (2008–2012) allowed us to detect
three of such sites that showed to be drier than Yungay:
Moctezuma, Cerritos Bayos and María Elena South
(MES) (Fig. 1).
MES, located 275 km northeast of Yungay, was the
driest site among them (Fig. 2A). The mean atmospheric
RH at Yungay was 28.8%, whereas at the same period at
MES, it was only 17.3%. Previous reports had shown
even higher mean atmospheric RH values (36.9%) at
Yungay (de los Ríos et al., 2010). Minimum atmospheric
RH values were extremely low both at Yungay and MES
(1% and 0%, respectively), but maximum atmospheric RH
values were much lower at MES (54.7%) compared with
Yungay (86.8%) (Fig. 2B and Table 1A).
RH and temperature in the soil profile were then measured up to 1 m down the surface at MES. Interestingly, the
loggers that were buried deeper in the soil profile registered the lowest and more unvarying mean RH values in
time (Fig. 2C). The lowest mean RH was found 80 cm
down (14.2%), with minimum and maximum values of only
12.7% and 17% respectively (Table 1B). To our knowledge, this is the enduringly driest site on Earth reported
to date. In comparison, other sites like the Dry Valleys of
Antarctica show mean atmospheric RH values in the
range of 55–74% (Doran et al., 2002). RH values found in
the soil depth at MES also match the lowest RH values
recorded by the remote environmental monitoring station
on National Aeronautics and Space Administration’s Curiosity rover (Gomez-Elvira, 2013).
Earth driest site
389
Fig. 1. Geographic location and aspect of the sites studied. Map modified from Drees et al., (2006).MES: María Elena South. C.B.: Cerritos
Bayos. MOC: Moctezuma.
Temperatures followed a similar pattern, with significantly lower and more unvarying values at increasing
depths. Although mean temperatures were similar in
the soil profile up to 1 m depth, surface soils usually
approached near 60°C during the day and 9°C during the
night. In contrast, soils 100 cm deep were at a constant
temperature of about 27°C (Table 1C).
Soil samples showed extremely low, albeit variable
levels of organics (0.04% to 1.1), variability that may be
caused by dissimilar microbial colonization levels along
the soil profile (Table S1). Regardless of their magnitudes,
levels of Mg, N, K, Mn, Zn, Cu and B increased in depth,
in contrast to those of Fe, S, Ca and Na (Table S1). The
highest values were found for SO4, Ca, Na, Cl and K, in
agreement with the reported prevalence in these soils of
gypsum, sodium chloride and jarosite, typically found in
the nearby caliche processing plant of Pedro de Valdivia
(Anderson, 2009). Gypsum has been reported as a frequent habitat for life in Yungay (Wierzchos et al., 2011).
However, we did not observe any colonization of gypsum
samples at MES, which also suggests the extreme
dryness of this new site.
The potential microbial content of these extremely dry
soils was then analysed through culture-dependent and
-independent methods. DNA extracted from samples rep-
resenting each depth was extremely low, with the highest
values being 1.2 μg DNA per gram of soil.
Denaturing gradient gel electrophoresis (DGGE)
band analysis unveiled an unforeseen diversity of
bacteria, primarily from the Actinobacteria (Actinobacterium, Aciditerrimonas and Geodermatophilus),
the Proteobacteria (Caulobacter, Sphingomonas), the
Firmicutes (Firmicutes, Clostridiales) and the Acidobacteria (Acidobacterium). Among other 16S rRNA
sequences detected by this technique, close matches
were found in the surface and 5 cm down soil samples
related to an uncultured Firmicutes bacterium reported in
the deep-subsurface hydrothermal aquifer, feeding the
giant gypsum crystal-bearing Naica Mine, Mexico (Ragon
et al., 2013), a finding consistent with the high day surface
temperatures typical of MES, which can get up to 58°C in
the afternoon.
In parallel, culture-dependent methods allowed to
isolate several additional species not detected by DGGE.
We found that Actinobacteria were present along the soil
profile, with a few species of Bacillus at 1, 5 and 80 cm
of depth (Table 2). In total, 30 distinct 5 isolates were
identified, representing 16 novel species of the genus
Streptomyces, 5 of the genus Bacillus, and 1 of the
genus Geodermatophilus (Figs 3–5). Species of this
© 2014 Society for Applied Microbiology and John Wiley & Sons Ltd, Environmental Microbiology Reports, 7, 388–394
390 A. Azua-Bustos, L. Caro-Lara and R. Vicuña
Fig. 2. Representative relative humidity (RH) conditions of three new hyperarid sites of the Atacama Desert. Ticks in the x axis mark 24-h
periods at noon.
A. Representative week profile (RH) of the three sites compared with Yungay. MOC, Moctezuma; C.B., Cerritos Bayos; MES, María Elena
South.
B. Representative time profile (RH, 18 days) of MES compared with Yungay.
C. Representative week profile (RH) of soils in depth at MES. S, surface. Numbers in the inset are cm of depth.
latter genus are frequently isolated from extremely stressful environments such as desert rock varnish, exhibiting
high Ultraviolet C (UV-C) tolerance and manganese oxidation (Ivanova et al., 2010), a finding that agrees with
one of the highest concentrations of manganese found in
our soil profile at this depth.
Several species found at MES showed an intense
orange colour when grown in vitro (Figs 3 and 4), suggesting the synthesis of beta-carotenes typically produced by other Bacillus species of the Atacama isolated
by us in response to UV-C radiation (Paulino-Lima et al.,
2013).
© 2014 Society for Applied Microbiology and John Wiley & Sons Ltd, Environmental Microbiology Reports, 7, 388–394
Earth driest site
391
Table 1. Statistics of the atmospheric and soil relative humidity (RH) and temperature (°C) measurements taken at three new hyperarid sites of
the Atacama Desert.
A
B
C
Site
Mean RH
RH Max
RH Min
Δ Mean RH Yungay
RH Max–Min
Yungay
Moctezuma
Cerritos Bayos
MES
28.8
25.8
21.5
17.3
86.8
94.4
74.6
54.7
1.0
0.6
0.0
0.0
3.0
7.3
11.5
85.8
93.8
74.6
54.7
Depth (cm)
Mean RH
RH Min
RH Max
ΔRΗ Max–Min
Surface
5
20
50
80
100
27.5
18.4
16.0
16.9
14.2
15.2
2.2
6.2
11.1
14.1
12.7
14.2
72.5
33.6
24.1
22.3
17.0
16.6
70.3
27.4
12.9
8.2
4.3
2.3
Depth (cm)
Mean T (°C)
T° Min
T° Max
ΔΤ° Max–Min
Surface
5
20
50
80
100
27.2
28.6
29.2
28.6
27.7
27.1
9.3
15.0
24.0
27.3
27.0
26.6
57.8
45.4
32.9
28.8
27.7
27.1
48.4
30.4
8.9
1.4
0.7
0.6
RH is expressed as %. A: ‘Δ Mean RH Yungay’ shows the differences between the mean RH of the new sites compared with the mean RH of
Yungay. B: Statistics of the RH measurements taken in soils of MES. C: Statistics of the temperature measurements taken in soils of MES.
In general terms, the diversity of microbial species
found at MES is comparable with those reported in other
sites of the Atacama Desert (Neilson et al., 2012) in the
McMurdo Dry Valleys in Antarctica (Smith et al., 2006;
Cary et al., 2010) and the Gobi and Taklamaken deserts
(An et al., 2013).
No decrease in the number of species was observed
at deeper soil levels (Table 2). This is surprising when
Table 2. Isolates found at each soil profile in María Elena South.
Streptomyces
Soil depth
Unique
Synonym
Surface
S1
S2
S3
S3
S4
S5
S1 TB, S2 TB, S3 TB, S.5 TB
MAR
MAR
TB
MAR
MAR
TB
1
5
5.1 TB
20
20.1 TB
80
20.2 TB
80.2 MAR
100
100.2 LB
100.5 LB
100.8 LB
100.9 LB
100.11 LB
Bacillus
Geodermatophilus
Unique
Synonym
1.1 LB
5.1 MAR
5.2 MAR
80.1 TB
Unique
Synonym
20.1 LB, 100.1 LB, 100.2 LB,
100.3 LB, 100.5, 100.5 LB, 100.7
LB, 100.9 LB, 100.12 LB
80.1 MAR
80.1 LB
100.1 MAR
Note that several isolates, after 16S rRNA identification, were found to be the same (synonym) species. Codes in bold identify species that were
found in two different soil depths. The identity of each isolate is shown in Figs 1–3.
© 2014 Society for Applied Microbiology and John Wiley & Sons Ltd, Environmental Microbiology Reports, 7, 388–394
392 A. Azua-Bustos, L. Caro-Lara and R. Vicuña
Fig. 3. Phylip NJ (Phylip neighbor joining) phylogenetic tree obtained from the aligned 16S rRNA Streptomyces and related gene sequences
using Bosque. Numbers on the nodes represent bootstrap values with 10 000 replicates. The physical aspect of the colonies formed by each
isolate is shown in the inset.
considering the increasing dryness in the soil depth, suggesting an acute tolerance of these species to extreme
desiccation.
In addition, only two of the species isolated were found
in more than one specific soil depth (20.1 LB (Luria
Broth) = 100.1 LB and 5.1 MAR (marine broth) = 80.1 TB
(Terrific Broth)), an observation that suggest that other
factors such as the availability of specific chemical energy
sources could be more critical in the habitability limitations
of this site.
We could not detect any Archaea in our soil samples,
although we used the same approach that successfully
allowed us to detect member of this domain in other
regions of the Atacama (Azua-Bustos et al., 2011; 2014).
If similar results stand in time in other sites as dry as the
one hereby described, it could imply that there may be a
dry limit for this domain of life on Earth.
For more than 10 years, the Yungay region of the
Atacama Desert has been considered as the paradigm of
the driest sites on Earth, and probably close to the dry
Fig. 4. PhyML maximum likelihood phylogenetic tree obtained from the aligned 16S rRNA Bacillus and related gene sequences using
BOSQUE. Numbers on the nodes represent bootstrap values with 1000 replicates. The physical aspect of the colonies formed by each isolate
is shown in the inset.
© 2014 Society for Applied Microbiology and John Wiley & Sons Ltd, Environmental Microbiology Reports, 7, 388–394
Earth driest site
393
Fig. 5. PHYML maximum likelihood phylogenetic tree obtained from the aligned 16S rRNA Geodermatophilus and related gene sequences
using BOSQUE. Numbers on the nodes represent bootstrap values with 1000 replicates. The physical aspect of the colony formed by the
isolate is shown in the inset.
limit for life. However, as a result of a more systematic
survey, we show in this work that there are other sites in
this desert that are much drier than Yungay, and thus,
better Mars analogues. It is remarkable that although the
site hereby reported is extremely dry, microbial life may
still be found in its soils, thus leaving the question still
open as to whether (and if so, where) there is a place on
Earth that is so dry that no microbial life is able to endure.
Acknowledgements
Armando Azua-Bustos received a scholarship for graduate
studies from CONICYT Chile, and additional financial
support from the Millennium Institute for Fundamental and
Applied Biology (MIFAB), Chile, from FONDECYT project
n° 1110597 and from Francisco Silva, from Kingston
Technology-Chile.
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Supporting information
Additional Supporting Information may be found in the online
version of this article at the publisher’s web-site:
Supporting Information. Materials and Methods.
Table S1. Geochemical determinations taken in soils of
María Elena South. O.M.; organic matter, mS; milli Siemens.
All elemental compositions are shown in mg/kg of soil.
© 2014 Society for Applied Microbiology and John Wiley & Sons Ltd, Environmental Microbiology Reports, 7, 388–394