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JOURNAL OF GEOPHYSICAL RESEARCH, VOL. 112, G02030, doi:10.1029/2006JG000385, 2007
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Endolithic cyanobacteria in soil gypsum: Occurrences in Atacama
(Chile), Mojave (United States), and Al-Jafr Basin (Jordan) Deserts
Hailiang Dong,1 Jason A. Rech,1 Hongchen Jiang,1 Henry Sun,2 and Brenda J. Buck3
Received 4 December 2006; revised 10 April 2007; accepted 9 May 2007; published 21 June 2007.
[1] Soil sulfates are present in arid and hyperarid environments on Earth and have been
found to be abundant in soils on Mars. Examination of soil gypsum from the Atacama
Desert, Chile, the Mojave Desert, United States, and Al-Jafr Basin, Jordan, revealed
endolithic cyanobacteria communities just below the surface of soil gypsum samples.
Optical and scanning electron microscope observations of the colonized layers indicated
that the unicellular Chroococcidiopsis is the dominant cyanobacterium in all studied
communities. 16S rRNA gene analysis revealed that in addition to Chroococcidiopsis,
a few other cyanobacteria are present. Heterotrophic bacteria are also abundant in the
colonized zones of the fine-grained gypsum from the Atacama and Mojave Desert, but
insignificant in the fibrous gypsum from the Jordan Desert. Endolithic life forms similar to
these described here may exist or have existed on Mars and should be targeted by the Mars
Science Laboratory and future in situ missions.
Citation: Dong, H., J. A. Rech, H. Jiang, H. Sun, and B. J. Buck (2007), Endolithic cyanobacteria in soil gypsum: Occurrences in
Atacama (Chile), Mojave (United States), and Al-Jafr Basin (Jordan) Deserts, J. Geophys. Res., 112, G02030,
doi:10.1029/2006JG000385.
1. Introduction
[2] Endolithic cyanobacteria have been reported to be
present in a diverse range of environments on Earth, ranging
from the frigid Dry Valleys of Antarctica to the hyperarid
Atacama Desert of Chile [Friedmann, 1980; Friedmann et
al., 1967; Wierzchos et al., 2006]. The types of rocks
suitable for colonization by endolithic microorganisms are
also diverse and include halite, sandstone, quartz, limestone,
granite, and dolomite [Friedmann et al., 1967; WarrenRhodes et al., 2006; Wierzchos et al., 2006]. Because these
organisms typically inhabit cold and hot desert environments, some researchers have speculated that these or
similar life forms may have existed on Mars (assuming life
existed on the planet) [Friedmann and Ocampo-Friedmann,
1994; McKay, 1997; Warren-Rhodes et al., 2006; Wierzchos
et al., 2006], as the planet changed from a warm, waterabundant world to a cold desert. However, some of these
most preferred habitats for endolithic cyanobacteria on
Earth (such as quartz and sandstone) are not likely widespread on Mars [Christensen et al., 2000], thus this Earthbased endolithic ecosystem model does not necessarily
imply presence of similar life forms on Mars. There is a
need to know whether the rock types known to be present on
Mars are suitable for colonization by endolithic organisms.
1
Department of Geology, Miami University, Oxford, Ohio, USA.
Division of Earth and Ecosystem Sciences, Desert Research Institute,
Las Vegas, Nevada, USA.
3
Department of Geosciences, University of Nevada, Las Vegas, Nevada,
USA.
2
Copyright 2007 by the American Geophysical Union.
0148-0227/07/2006JG000385$09.00
[3] Recent reports indicate that gypsum rocks may also
support endolithic communities. Parnell et al. [2004] observed cyanobacteria in impact-generated hydrothermal gypsum deposits in Devon Island, Canada. Hughes and Lawley
[2003] reported a microbial endolithic community within
gypsum crusts on sandstone boulders from Alexander
Island, Antarctic Peninsula. Boison et al. [2004] studied
N2 fixation activities of cyanobacteria living in gypsum rock
shards in the Harz Mountains in Germany. Gypsum and
potentially other sulfates can provide a microenvironment
that protects these organisms from exposure to extreme
temperature, UV flux, and desiccation, yet they are sufficiently translucent to allow photosynthesis and N2 fixation to
occur in the rock [Boison et al., 2004; Rothschild et al.,
1994]. Despite the fact that sulfate deposits are widespread
on Mars [Clark et al., 1982; Clark and Van Hart, 1981;
Cooper and Mustard, 2002; Klingelhofer et al., 2004;
Gendrin et al., 2005; Langevin et al., 2005; McLennan et
al., 2005; Squyres et al., 2004] and may be potentially
important habitats for Martian life, endolithic life in soil
gypsum has not been systematically studied, especially in dry
desert environments.
[4] Sulfate minerals in the form of gypsic crusts are
common within soils located in semiarid to hyperarid
deserts on Earth [Buck and Van Hoesen, 2002; Buck et
al., 2006a, 2006b; Herrero and Porta, 2000; Nettleton,
1991]. These crusts form as a result of either upward
capillary migration and evaporation (per ascendum) and/or
per descendum processes of downward leaching of soil
waters. In both cases, sulfates accumulate in the soil
because of a lack of sufficient water to remove the soluble
salts. Sources of sulfate ions include in situ weathering of
parent material or sulfide minerals [Carter and Inskeep,
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1988; Mermut and Arshad, 1987; Mrozek et al., 2006], fluvial
or eolian input [Buck and Van Hoesen, 2002; Taimeh, 1992],
and an atmospheric source from seawater [Podwojewski and
Arnold, 1994; Rech et al., 2003; Toulkeridis et al., 1998].
[5] In this study, we report endolithic cyanobacteria in
soil gypsum crusts from several major deserts on Earth to
identify if these surfaces may be a potential area to look for
the presence of past life on Mars. Soil gypsum samples were
collected from the Atacama, Jordan, and Mojave Deserts.
Thin green layers (colonized zones) a few millimeters below
the exposed surface were observed in all three samples. The
microbial community within these colonized zones was
studied by cultivation and molecular analysis. Our results
indicate that photosynthetic cyanobacteria are either a
predominant or a significant component in the total community, depending on the texture of gypsum. Heterotrophic
bacteria are also present as important members in the
community.
2. Methods
2.1. Samples and Study Areas
[6] Soil gypsum was examined for evidence of endolithic
cyanobacteria during field work in the Atacama Desert,
Chile, al-Jafr Basin, Jordan, and the Mojave Desert, United
States. At all locations, samples were collected after thin
green layers (colonized zones) were observed within 1 cm
from the top of the gypsic surface crust. Sample AT326b
from the Atacama was collected in 2000 and samples JB1
(Jordan) and DG (Mojave) were collected in 2005. All
samples were stored in sterile plastic bags until analysis in
2005. It is difficult to assess how much the microbial
community in the Atacama sample changed during storage
time, but we speculate any change should be minimal based
on several reasons: (1) the sample had been stored dry at
room temperature in a sealed zip-lock bag; (2) external
layers were removed before any molecular analysis. Internal
portions of the sample should have been isolated from any
contact with air or moisture; (3) published literature documents that microbial community in low-permeability solid
samples does not change in any significant way over an
extended time period [Haldeman, 1997].
[7] The Atacama Desert is located in northern Chile
between the Andes and the Pacific Ocean and is one of
the driest locations on Earth. The core of the desert receives
<10 mm/yr precipitation and lacks vascular plants [Houston
and Hartley, 2003; Navarro-Gonzalez et al., 2003]. All soils
in that region are composed of thick accumulations of
soluble salts including sulfates, chlorides, and nitrates
[Ericksen, 1981; Ewing et al., 2006; Buck et al., 2006a,
2006b]. Sulfates (gypsum and anhydrite) are most abundant
at the top of soils. The Atacama sample was collected from
a deflated surface crust of soil gypsum located on a mature
alluvial fan in Llano de la Paciencia (22!49.045 0S,
68!20.4960W), just north of the Salar de Atacama at an
altitude of 2850 m. Colonized green layers were observable
just below the surface of the gypsum in a limited area where
the soil gypsum was exposed at the surface, but not in
adjacent areas where the soil gypsum was covered by
!25 cm of overlying material. Because of limited exposure
of soil gypsum, it was not possible to survey what percent
of exposed soil gypsum was colonized. Precipitation at this
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locality is estimated to be !10 mm/yr and average temperature to be !13!C based on climate data from the Direccı́on
General de Aguas, Chile, for stations at similar elevation
along the Pacific slope of the Andes in this region of Chile.
Vegetation cover is <2% and composed of Atriplex imbricata
(alive) and Acantholippia deserticola (dead).
[8] Al-Jafr Basin is a large internally-drained basin located
in southeast Jordan. The landscape is largely devoid of
vegetation and blanketed by a desert pavement of chert clasts
with desert varnish. Sample JB-1 was collected from a
secondary vein of fibrous gypsum within the Cretaceous
Muwaqqar Chalk/Marl Formation that has been exposed by
erosion on a pediment surface in the northern al-Jafr Basin
(30!30.4790N, 36!38.3760E) at an altitude of 940 m. Veins of
fibrous gypsum and the green layers just below the surface
were only found at this one location. Many fibrous gypsum
rocks at this location are colonized, but in general, veins of
fibrous gypsum at the surface are not widespread. Thus, it is
difficult to assess heterogeneity of colonization patterns in
vein gypsum. Precipitation is estimated to be !20 mm/yr and
average temperature to be !19!C, ranging from !2! to
35!C, based on limited climate data from the Jordan
Meterological Department for the nearby city of Al-Jafr.
There is no vegetation in this area.
[9] The Mojave Desert sample DG was collected from
the soil surface at the DryGyp site (36!23 010.60 00N,
114!25043.5000W) at an altitude of 474 m, located about
75 km northeast of Las Vegas, Nevada, United States.
Colonized gypsum is commonly present in this region.
Gypsum increases dramatically with depth, ranging from
14% in the surface to 90% within <20 cm, forming shallow
petrogypsic horizons. Visual inspection reveals that the
pattern of colonized gypsum is similar to one another, thus
only one representative sample was analyzed. Soils in this
area contain nearly pure gypsum that is cemented at depth to
form petrogypsic horizons. Precipitation is !150 mm/yr and
the area has !30% vegetation cover (Psorothamnus fremontii,
Petalonyx parryi, Acacia greggii, and Eriogonum inflatum).
Average temperature is !20!C and ranges from !3 to 48!C.
2.2. X-Ray Diffraction
[10] XRD analyses of powdered samples were performed
by step scanning using a PANalytic X’Pert PRO diffraction
system. CuKa radiation (K-alpha1 = 1.54060 Å, K-alpha2 =
1.54443 Å) was used at 40 kV, 40 mA with a 0.017! 2q step
interval and a step-counting time of 0.25 s. Diffraction
patterns generated from a 6! – 75! 2q range were imported
into X’Pert High Score software where sample mineralogy
was determined by matching diffraction profile peaks via
auto-identify and user defined database queries. Additional
full mineralogical analyses using standard Soil Survey
Methods (Soil Survey Staff, 2004) were performed on the
Mojave Desert DryGyp sample at the National Soil Survey
Center Soil Survey Laboratory in Lincoln, Nebraska.
2.3. Scanning Electron Microscopy (SEM)
[11] Freshly cleaved gypsum specimens were moistened
in phosphate buffer saline (PBS) solution for 20 min, fixed
in 0.5% formaldehyde (in PBS) and then in 1% glutaraldehyde (in PBS) each for 15 min, and dehydrated in ethanol
series 15%, 30%, 50%, 75%, 95%, 100%, each for 15 min.
After two additional changes in anhydrous ethanol, the
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specimens underwent two soaks in hexamethyldisilazane
(HMDS), each for 30 min. HMDS was decanted, and the
specimens were air-dried. After gold-coating (75 s), the
specimens were viewed under a JEOL scanning electron
microscope JSM-5610 equipped with an Oxford ISIS energy
dispersive spectrometer (EDS) at the University of Nevada
Las Vegas Electron Microanalysis and Imaging Laboratory.
SEM/EDS analyses were used to identify the relationship
between gypsum crystals (with Ca and S peaks) and organic
tissues (only C peaks).
2.4. Cultivation and Light Microscopy
[12] Experiments were set up to enrich cyanobacteria
from the colonized layer of the Atacama and the Jordan
sample using a general medium for cyanobacteria (i.e.,
BG11) according to a published procedure [Rippka et al.,
1979]. Enrichment cultures were examined under light
microscope. DNA extraction was also performed on the
enriched Jordan sample to confirm the identity of the
enriched cyanobacteria.
2.5. Molecular Microbiology - Clone Library
Construction
[13] Genomic DNA was extracted from the colonized
zones of each sample and from an enrichment culture from
the colonized layer of the Atacama sample. Extraction was
performed with an Ultra Clean Soil DNA Isolation Kit
(MoBio Laboratories, Inc., Solana Beach, CA). The
uncolonized zone of the Atacama sample was also analyzed
as a background control. The samples were designated as
follows: Atacama-col and Atacama-cont stand for colonized
(green layer) and control (nongreen layer) Atacama gypsum, respectively, Jordan for the Jordan sample, and
Mojave for the Mojave sample. Purified DNA was PCRamplified according to the procedure of Failsafe Kit (Epicentre Biotechnologies, Madison, WI). Primer sequences
for bacteria were Bac27F and Univ1492 [Jiang et al., 2006].
PCR conditions were the same as previously described
[Jiang et al., 2006].
[14] The PCR product was ligated into pGEM-T vector
(Promega Inc., Madison, WI) and transformed into E. Coli
DH5a competent cells. Gene clone libraries of 16S rRNA
were constructed, and a sufficient number of randomly
chosen colonies per sample were analyzed for insert 16S
rRNA gene sequences until rarefaction curves were fully
saturated. However, only twelve clones were sequenced for
the enrichment culture from the Jordan sample and rarefaction curve was not saturated. Plasmid DNA containing
inserts of 16S rRNA gene was prepared using QIAprep
Spin Miniprep Kit (Qiagen, Valencia, CA). Sequencing
reactions were carried out with primer Bac27F for bacteria
with a BigDye Terminator version 3.1 Cycle Sequencing
Kit (Applied Biosystems, CA, United States). The 16S
rRNA gene sequence was determined with an ABI 3730
automated sequencer. Sequences were typically !700 –
800 bp long. The sequences were aligned with ClustalW.
Phylogenetic analyses of partial 16S rRNA gene sequences
were conducted using molecular evolutionary genetics analysis (MEGA) version 2.1. Neighbor-joining phylogenies
were constructed from dissimilatory distances and pair-wise
comparisons with the Jukes-Cantor distance model. The
sequences determined in this study have been deposited in
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the GenBank database under accession numbers EF071489 –
EF071546.
3. Results
3.1. Texture and Mineralogy of the Gypsum Samples
[15] The Atacama and Mojave samples are composed of
massive, micritic to spar-sized gypsum. The colonized zone
is located at 1 – 3 mm below the surface (Figures 1a and 1b).
The Jordan sample is made of vertical bundles of clear,
fibrous gypsum (selenite) (Figure 1c). In this sample the
colonized zone is located deeper into gypsum, !4 – 10 mm
below the surface. It has a width of 3 – 14 mm and displays a
more transitional (less contrast) appearance from the
uncolonized to the colonized zone. The colonized zone also
displays a blackish (dark-green) coloration (Figure 1c). In
the Atacama and Mojave samples the colonized zones are
concentrated around microtopographic lows or depressions
in the soil gypsum crust.
[16] X-ray diffraction patterns revealed that the Jordan
sample is pure gypsum with no detrital soil materials. The
Atacama and Mojave samples are mostly gypsum (>95%),
but also contain trace amounts of insoluble dust materials
(quartz, feldspar, kaolinite, montmorillonite, and mica).
3.2. Light Microscopy and Scanning Electron
Microscopy
[17] Light microscope observations revealed that cyanobacterium Chroococcidiopsis is a dominant organism in the
enrichment culture from the colonized zone of the Atacama
sample (Figure 1d). Similar observations were made for the
Jordan enrichment culture. This identification was based on
the characteristic morphology and texture of this organism.
[18] SEM observations of the colonized layers of all three
gypsum samples revealed that all studied gypsum specimens contain abundant unicellular cyanobacteria, which
range in diameter from 2.5 to 4.5 mm (Figures 2a –2e).
The Mojave specimen contains, in addition to the unicellular forms, a small number of filamentous cyanobacteria
(Figure 2d). In the Mojave specimen both the unicellular
and filamentous cyanobacteria are covered by exopolymer
polysaccharide (EPS), which obscure their morphology. In
contrast, organisms in the other specimens appear to have
no or little EPS and have a smooth appearance (Figures 2a,
2c, and 2e). In these specimens, evidence of binary cell
divisions was observed. Small cocci and rod-shaped bacteria are present in all the communities, but are especially
abundant in the Jordan specimen (Figures 2a and 2b). In all
specimens, the organisms appear to occupy preexisting
crevices and pore spaces, and exhibit no signs of boring.
However, dissolution of gypsum crystals, possibly by
organisms, was occasionally observed (Figure 2e).
3.3. Bacterial Diversity
3.3.1. Autotrophic Cyanobacteria
[19] Cyanobacteria are the most abundant organisms in
the Jordan enrichment culture (3 out of 12 sequences)
(Figure 3). In the three gypsum samples, cyanobacterial
sequences constitute the most abundant group in the colonized zones of the Atacama and the Jordan sample (25 and
18 out of total 73 and 23 clone sequences, respectively)
(Figures 3 and 4), but are a small component (9 out of 51) in
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Figure 1. Samples of soil gypsum with cyanobacteria: (a) Soil gypsic crust sample AT326b from the
Atacama Desert; (b) soil gypsic crust sample DG from the Mojave Desert; (c) fibrous gypsum sample
JB1 from a secondary vein exposed by erosion at the surface from Al-Jafr Basin, Jordan; (d) light
micrograph of cyanobacterium Chroococcidiopsis in an enrichment culture from sample AT326b from
the Atacama Desert.
the colonized zone of the Jordan sample. The majority of
clone sequences in this group (13, 13, and 9 out of those 25,
18 and 9 cyanobacterial sequences) are closely (96 – 99%
similarity) related to hypolithic cyanobacterial clone
sequences (AY644697) recovered from translucent quartz
stones in the arid and hyperarid regions of the Atacama
desert [Warren-Rhodes et al., 2006]. The second most
abundant group of sequences forms a cluster with Chroococcidiopsis sp. BB96.1 (AJ344555) (Figure 3), a photobiont of the lichen Peltula euploca in South Africa [Fewer
et al., 2002]. Seven sequences from the colonized zone of
the Atacama sample form a cluster with uncultured Antarctic cyanobacteria (AY151733, DQ181678) [Taton et al.,
2006, 2003].
3.3.2. Heterotrophic Bacteria
[20] Each group of the heterotrophic community is described below.
[21] Alphaproteobacteria: Members of the Alphaproteobacteria group are present in all samples, except in the Jordan
sample (Figures 3 and 4). However, four sequences in the
enrichment culture from the Jordan sample belong to this
group. Most clone sequences from the colonized zone of the
Atacama sample (Atacama-col) are related to the Rhizobiales
group (such as Mycoplana dimorpha or Rhizobium taeanense), bacterium of the rhizosphere (AJ252588), and Sphingomonas sp. from Lake Vostok accretion ice [Christner et al.,
2001] (Figure 3). All sequences from the uncolonized regions
of the Atacama sample (nongreen layer) are related to an
uncultured alpha proteobacterium (X97079) from peat in
Germany [Rheims et al., 1996]. The majority of clone
sequences from the Mojave sample (along with 3 sequences
from the Jordan enrichment culture) are nearly identical to
Caulobacter sp. (AJ227770), a common bacterium in aquatic
environments [Abraham et al., 1999]. Some sequences
from the Mojave sample are related to Methylobacterium fujisawaense (AB175634) or iron-oxidizing acidophile Y005 (AY140237) (Figure 3). Members of the genus
Methylobacterium are ubiquitous in nature [Green, 2001],
including soil, dust, freshwater, and lake sediments. Strain
Y005 was isolated from sites in Yellowstone National Park
[Johnson et al., 2003].
[22] Gammaproteobacteria: The Gammaproteobacteria
group is most abundant in the uncolonized region of the
Atacama sample, a significant group in the Jordan sample, a
minor group in the Mojave sample, and absent in the
colonized layers of the Atacama sample (green layers)
(Figures 3 and 4). The most dominant group of clone
sequences (8 from the Atacama-cont and 1 from the Mojave
sample) are >99% similar to gamma proteobacterium
HTB082 isolated from deep-sea mud samples (2759 m)
[Takami et al., 1999]. Another group of 3 sequences from
the Atacama-cont sample are nearly identical to Stenotrophomonas maltophilia. A group of 4 sequences from the
Jordan sample are 95% similar to Pseudomonas plecoglossicida isolated from a rice field (GenBank description).
[23] Betaproteobacteria: One sequence from the Jordan
enrichment culture is nearly identical to Ralstonia
metallidurans.
[ 24 ] Deltaproteobacteria: Two sequences from the
uncolonized zone of the Atacama sample are closely
(>98% similarity) related to an uncultured hydrocarbon seep
bacterium GCA017 (AF154102) (GenBank description).
[25] Verrucomicrobia: Three sequences from the colonized zone of the Atacama sample are related to (95%
similarity) an uncultured Xiphinematobacteriaceae bacterium
from a pasture soil (GenBank description).
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Figure 2. SEM micrographs of fractured soil gypsum specimens from (a) Jordan, revealing unicellular
cyanobacteria and coccoid bacteria; (b) Jordan, showing rod-shaped bacteria; (c) Atacama site (AT326b),
unicellular cyanobacteria and cell divisions (arrows); (d) Mojave, unicellular and filamentous
cyanobacteria covered by exopolymer polysaccharide (arrows); (e) Jordan, unicellular cyanobacteria
with crosscutting relationship between the cyanobacteria displaying cell division (arrow, lower right) and
a cluster of tabular pseudohexagonal gypsum crystals indicating dissolution of gypsum crystals during
the growth of the cyanobacteria cells. Scale bar is 5 mm.
[ 26 ] Firmicutes: This group is insignificant in the
uncolonized region of the Atacama sample and in the
Mojave sample, a minor component in the colonized zone
of the Atacama sample, and absent in the Jordan sample
(Figure 4). Three sequences from the Atacama-cont sample
are related to unidentified Hailaer soda lake bacterium F27.
The other three, along with two from the Mojave sample,
are grouped with Bacillus sp. Z-0521 (DQ675454), an
anaerobic alkaliphilic bacterium isolated from a soda lake
(GenBank description) (Figure 3). Other Mojave sequences
are related to either Desulfosporosinus sp. A10 (AJ582756)
or Alkaliphilus transvaalensis (AB037677). A common
nature of the Firmicutes sequences is that they are related
to alkaliphilic bacteria (with the exception of Desulfosporosinus sp.) isolated from aquatic environments.
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Figure 3
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Figure 4. Pie charts showing frequencies of all phylotypes affiliated with the major phylogenetic
groups in the bacterial clone libraries for all the samples.
[27] Actinobacteria: The Actinobacteria group is minor
or absent in all samples (Figures 3 and 4). The sequences in
this group are related to uncultured bacteria from various
soil environments [Lueders et al., 2006, 2004; Nemergut et
al., 2004].
[28] Gemmatimonadetes: Four sequences from the Atacama-col sample are remotely related to (!90% similarity) uncultured Gemmatimonadetes bacteria from soils
[Mummey and Stahl, 2003].
[29] Planctomycetes: Two sequences from the Atacamacol sample are remotely related to (85% similarity) uncultured Planctomycetes in river biofilms [Brummer et al.,
2004].
[30] Bacteroidetes: Three sequences from the Atacamacol sample are related to (97% similarity) uncultured
Bacteroidetes bacterium in soils of Marble Point and Wright
Valley, Victoria Land, Antarctica (GenBank description).
[31] Unclassified bacteria: A small number of sequences in
each clone library could not be classified. They were related
to uncultured bacteria in the air of Texas (DQ129347)
(GenBank description) and an agricultural soil (AY037635)
[Furlong et al., 2002; Lu et al., 2006].
4. Discussion
4.1. Presence of Cyanobacteria in Gypsum Rocks
[32] Several studies have documented endolithic cyanobacteria in gypsum from wet environments. Parnell et al.
[2004] presented photographic evidence for the presence of
cyanobacterial layers (possibly Gloeocapsa and Nostoc) in
impact-generated hydrothermal gypsum deposits in Devon
Island, Canada. Hughes and Lawley [2003] reported a
microbial endolithic community within gypsum crusts
found on the surface of sandstone boulders at Two Step
Cliffs, Alexander Island, Antarctic Peninsula. The endolithic
community was localized and only a few isolates were
studied. Occasional snowmelt was the major source of water
for these organisms. Boison et al. [2004] studied N2 fixation
activities of Chroococcidiopsis-dominated cyanobacteria in
gypsum rock shards in the southern part of the Harz
Mountains in Germany, but they did not characterize the
Figure 3. Neighbor-joining tree (partial sequences, !700 bp) showing the phylogenetic relationships of bacterial 16S
rRNA gene sequences cloned from three desert samples and one enrichment culture (Jordan) to closely related sequences
from GenBank. One representative clone type within each phylotype is shown and the number of clones within each
phylotype is shown at the end (after the GenBank accession number). If there is only one clone with a given phylotype, the
number ‘‘1’’ is omitted. Clone sequences from this study are coded as follows, with Atacama-colB3 as an example:
Atacama-col: colonized gypsum (green bands) from Atacama; B, bacteria; 3, clone number. Thus, it reads bacterial clone
3 from the colonized gypsum (green bands) of the Atacama sample. Scale bars indicate Jukes-Cantor distances. Bootstrap
values of >50% (for 500 iterations) are shown. Aquifex pyrophilus is used as an outer group, and a single tree showing all
bacterial sequences is created.
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cyanobacterial community and habitat. Warren-Rhodes et
al. [2006] noted microbial colonization in soil gypsum in
the Atacama Desert, but they did not analyze the community. Cyanobacterial colonization is commonly observed in
gypsum crusts associated with evaporite deposits [Douglas
and Yang, 2002; Douglas, 2004; Sanz-Montero et al., 2006]
and salt evaporation ponds [Oren et al., 1995; Kedar et al.,
2002; Ionescu et al., 2007], but environmental conditions at
these locations are different from dry desert soils.
[33] In this study, we have demonstrated that soil gypsic
crusts are an important substrate for cyanobacterial colonization in the dry deserts of Mojave, Jordan and Atacama. At
the Atacama sampling site, occasional summer precipitation
(!10 mm/yr) is an important source of moisture. Coastal
fog does not penetrate into this region of the Atacama. To
sustain a microbial community, gypsum crusts would have
to retain sufficient moisture for a long period of time after a
rainfall [Buck and Van Hoesen, 2002]. High humidity levels
occur only during occasional precipitation events.
[34] Endolithic cyanobacteria typically grow a few millimeters below the exposed rock surface [Warren-Rhodes et
al., 2006; Wierzchos et al., 2006]. The depth at which
endolithic cyanobacteria colonize rocks appears to be determined by a physiological balance of several important
factors. Whereas greater depth helps retain moisture and
increases the level of protection from intolerable irradiation,
high temperature, and arid surface condition, at the same
time these microorganisms have to acquire a minimum
amount of light and air (CO2 and N2) required for photosynthesis and N2 fixation [Boison et al., 2004; Rothschild et
al., 1994]. Cockell et al. [2002] specifically investigated the
shielding effect of rocks. A 5-min exposure of Chroococcidiopsis sp., a desiccation-tolerant, endolithic cyanobacterium, to martian-surface UV and visible light flux led to a 99%
loss of cell viability. Under 1 mm of sandstone, however, the
same organism could survive (and potentially grow) if water
and nutrient requirements for growth were met.
[35] This physiological balance is apparently seen in our
gypsum samples. Cyanobacteria colonize deeper into the
clear form of gypsum (selenite) from the Jordan Desert than
the massive microcrystalline form of gypsum from the
Atacama and Mojave Deserts. The clear selenite form of
gypsum is believed to facilitate the penetration of photosynthetically active radiation and UV radiation to the cyanobacterial colonies [Parnell et al., 2004]. Thus, in order to
find their optimal niche (reduced light intensity and O2
tension in addition to water), the organisms would have to
reside deeper into the crystal. In order to cope with increased
level of UV penetration into the clear selenite crystal, a black
coloration (Figure 1c) may be developed by the synthesis of
ultraviolet screening compounds [Cockell et al., 2002;
Parnell et al., 2004]. In contrast, the massive and micritic
form of gypsum from the Atacama and Mojave Desert do not
exhibit any black coloration in the colonized zones and the
colonization depth is shallow, only within a few mm from
the surface, probably because of the poor light penetration
through the massive gypsum. Although the observed colonization pattern (depth and coloration) appears to be correlated with the gypsum texture, it is cautioned that this
observation is based on a limited number of samples. A
better understanding of colonization and rock texture
requires a systematic study with a larger sampling size.
G02030
4.2. Bacterial Diversity in Soil Gypsum Crusts from
Desert Environments
[36] The clone library approach provides information on
bacterial diversity, but the estimate of the relative proportion
of each group (Figure 4) is qualitative. We note some degree
of inconsistency in biomass estimation of cyanobacteria
between visual observations (both optical and electron
microscope observations) and molecular identification. Under optical and SEM, more than 95% of biomass appeared
to be cyanobacteria, but 16S rRNA gene analysis revealed
that cyanobacteria constitute a much lower percentage in the
overall population. There are several possibilities that may
be responsible for this inconsistency. Firstly, some amount
of contamination by heterotrophic community from the
uncolonized regions of gypsum (uncolonized by cyanobacteria) may be possible, thus lowering the percentage of
cyanobacterial biomass in the colonized zone. Secondly, it
may be difficult to release DNA from certain cyanobacterial
cells, thus resulting in an underestimation of the cyanobacterial population by the molecular method. Thirdly, PCR
may introduce some bias.
[37] Although the clone-library approach is qualitative in
estimating the relative proportion of different microbial
groups, it should be accurate to reveal diversity, especially
when rarefaction curves are saturated. It is striking to note
the difference in the microbial community structure among
the studied gypsum samples (Figure 4). The community
structure in the Atacama and the Mojave sample consists of
8 and 6 phylogenetic groups, respectively. However, only
3 groups are present in the Jordan sample. One primary
difference between the Jordan sample and the other two is
the gypsum texture. The amount of precipitation between
the Jordan and the Atacama sampling sites is similar, at
20 and 10 mm/yr, respectively, both of which are significantly lower than the Mojave Desert at 150 mm/yr. In both
the Atacama and Mojave sample, gypsum occurs as finegrained, massive assemblages, but in the Jordan sample, it
occurs as clear crystal (selenite). It is possible that the clear
form of gypsum allows more sunlight to penetrate so that
photosynthetic cyanobacteria may be more competitive in
this environment. Again, it is cautioned that this observed
relationship between the microbial diversity and the gypsum
texture is based on a limited number of samples.
[38] A secondary factor in controlling cyanobacterial
abundance may be the amount of precipitation. Cyanobacteria are a significant group in the colonized zones of all
three samples, but in different abundance (Figure 4). Qualitatively, the cyanobacteria group is more abundant in drier
deserts (Atacama and Jordan), suggesting that a dry desert
environment may favor cyanobacteria. In wetter climates
where organic matter may be readily available, heterotrophic bacteria may be more dominant. In addition to the
effect on the cyanobacterial abundance, the amount of
precipitation apparently exerts an effect on the amount of
EPS production. Our data indicate that in the samples from
the drier sites (Atacama and Jordan), the amount of EPS is
less than that in the wetter site (Mojave). EPS production
may be related to the metabolic state of cells. When
bacterial cells are near the limit of survival, they simply
have no energy reserves to produce EPS. Stress level in the
dry sites (especially at Atacama) may be near the limit
because (1) cyanobacteria are dominated by Chroococci-
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diopsis and there are no filamentous forms; (2) growth is
binary instead of simultaneous divisions. Under such a
stress condition, EPS production may be minimal. Under
relatively wet conditions, such as the Mojave site of this
study and Antarctic [de los Rios et al., 2004, 2007; Omelon
et al., 2006], EPS are typically abundant in biofilms of
endolithic microbial communities.
[39] The composition of the heterotrophic bacteria in the
three desert environments is generally consistent with
previously identified groups. Except in the Jordan sample,
the Alphaproteobacteria group constitutes an important
component in the overall community (Figure 4). WarrenRhodes et al. [2006] identified clone sequences recovered
from quartz stones in the Atacama Desert that belong to
Alphaproteobacteria. The Alphaproteobacteria group
occurs between Copiapo and Altamira with a precipitation
of 21 and 4.7 mm/yr, respectively. Our gypsum sample was
collected in an area that receives !10 mm/yr precipitation
and thus it is not surprising to observe this group in our
gypsum sample. Abundant Alphaproteobacteria have also
been detected in Beacon sandstone samples from the
McMurdo Dry Valleys of Antarctic [de la Torre et al.,
2003]. The authors report that some members of this group
may potentially be capable of aerobic anoxygenic photosynthesis. However, caution must be exercised to infer any
physiological functions based on relatedness of clone
sequences to known cultures. Future work is needed to
determine the functions of this important group in desert
environments. Clone sequences that belong to Gammaproteobacteria have also been recovered from quartz stones in
the core arid region of the Atacama Desert [Warren-Rhodes
et al., 2006]. Our data show that this group may be
significant in the normal Atacama soil gypsum (without
cyanobacterial colonization).
[40] The other important groups, i.e., Gram positive
Actinobacteria and Firmicutes, Gemmatimonadetes and
Planctomycetes, have been detected in the Atacama Desert
[Drees et al., 2006; Navarro-Gonzalez et al., 2003]. NavarroGonzalez et al. [2003] found that surface soil samples from
the Atacama Desert, except for the driest Yungay region,
contain 6 to 26 distinct taxa, most of which belong to the
Gram positive Actinobacteria and Firmicutes. These two
groups are detected in our normal gypsum sample without
cyanobacterial colonization. Drees et al. [2006] detected
Gemmatimonadetes and Planctomycetes phyla in the Atacama soil at a depth of 25– 35 cm.
4.3. Endolithic Microbial Communities: The Last
Stage of Life on Mars
[41] Life on Mars, assuming it ever arose there, probably
originated about 3.5 –4.0 Ga years ago, when the planet was
warm and temperate [Carr, 1996; McKay, 1997; McKay and
Davis, 1991]. As it dried and cooled, however, life would
withdraw into protected refuges [Friedmann and Koriem,
1989; McKay et al., 1992]. The earliest such refuges were
likely in ice-covered lakes, similar to those found in
Antarctic Dry Valleys [Friedmann et al., 1987; McKay,
1997; Priscu and Christner, 2004]. The next stage of
existence, after liquid water disappeared from the planet
surface, would probably be endolithic microbial communities [McKay et al., 1992].
G02030
[42] The concept of endolithic life on Mars was initially
based on the discovery of the cryptoendolithic communities
in the Antarctic desert (high altitude regions of the Dry
Valleys) [Friedmann et al., 1987]. These communities live
inside sandstone, the most common endolithic substratum
available in the Dry Valleys. The protective role of the
substratum is well established. During the austral summer,
the rocks are warmed by solar insolation and can melt snow.
At the same time, sufficient sunlight penetrates the sandstone to support photosynthesis. It was suggested, therefore,
that similar communities might have existed on Mars.
[43] In the original concept, the endolithic model was a
general ecological model of survival on Mars [Friedmann et
al., 1987; Friedmann and Ocampo, 1976]. However, it has
been recently pointed out that quartz and sandstone are
unlikely to occur on Mars [Christensen et al., 2000]. Quartz
is a late stage mineral that requires a long geological period
of plate tectonic activity, which is lacking on Mars [Head
and Solomon, 1981; Solomon, 1978]. In light of these recent
findings, the endolithic model is implied not to be directly
applicable to study the biological history of Mars.
[44] Sulfate deposits have been detected as the predominant salts on Martian surface [Cooper and Mustard, 2002;
Gendrin et al., 2005; Langevin et al., 2005; Squyres et al.,
2004] and the presence of endolithic life in gypsum crystals
thus revives the endolithic model. Understanding where life
can and can not occur on Earth helps narrow the search of
life on Mars. Sulfate soil crusts in the hyperarid Atacama
Desert may serve as a potential Mars analog [NavarroGonzalez et al., 2003]. In addition to sulfate deposits and
aridity, the hyperarid core region of the Atacama Desert has
three other ‘‘Mars-like’’ characteristics, i.e., low levels of
refractory organic material, low number of detectable soil
bacteria, and the presence of one or more chemical oxidants
[Navarro-Gonzalez et al., 2003; Wierzchos et al., 2006].
[45] Cockell and Raven (2004) used a radiative transfer
model to study four micro-habitats in which damaging UV
radiation could be reduced to levels tolerable to life, but
where light in the photosynthetically active region would be
above the minimum required for photosynthesis. These
habitats include sediments containing ferric iron impurities,
halite crystals, snow-ice covers, and impact-shocked crystalline rocks. Interestingly, massive halite was identified as
one favorable habitat. Massive halite (sub-millimeter crystals) acts as an effective screen for UV radiation because
halite crystals scatter radiation, not because NaCl is an
effective UV absorber. Gypsum is not an effective UV
absorber either, and the authors speculate that life protection
under gypsum crusts would depend on its scattering property
and/or presence of UV absorbing contaminants in gypsum
such as iron. Despite the fact that gypsum as a potential
habitat has not been demonstrated with such a model prediction, its role in life protection certainly can not be ruled out.
Additionally, chemical data indicate that sulfate salts are
more common than halite on Mars, so gypsum may be more
likely to provide suitable widespread habitats on Mars.
[46] In addition to serving as a Mars analog, existence of
life in salt deposit offers additional significance for exobiology research. On Earth, ancient microbial life, including
some phototrophic organisms, can be preserved in sedimentary salt deposits [Bell, 1989; Coolen and Overmann, 1998;
Kunte et al., 2002]. If inside fluid inclusions of salt crystals,
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such microbial life may survive in salt for millions of years
[Vreeland et al., 2000]. Thus, it may be possible to not only
search for modern life on the planet, but also to study extinct
Martian life and its evolution. Such investigations likely
require a combination of multiple approaches, such as direct
detection of microbial life, as well as biomolecules, geochemical, and mineralogical biosignatures left behind from
past biological activity. Ancient soil sulfate crusts preserved
in Miocene paleosols in the hyperarid Atacama Desert may
provide valuable materials for studying ancient life on Mars.
[47] Regardless of modern or ancient microbial life,
microbial colonization under translucent rocks, such as
gypsum and halite, offers advantage for detection by remote
instrumentation. Depending on gypsum texture (massive vs.
selenite), cyanobacterial community may occur only a few
mm below the surface. If so, this community may be
detectable by remote, nondestructive spectroscopy methods.
Edwards et al. (2005) demonstrated that important biomolecular signatures from a cyanobacterial community a few
millimeters below the surface can be detected by Raman
spectroscopy. Before any Mars samples can be successfully
returned to Earth, such remote-sensing based techniques
continue to be an important source of information.
5. Conclusion
[48] In this study, we have presented evidence that
endolithic cyanobacteria colonize soil sulfate crusts in
several major deserts around the world. Although only a
limited number of samples were studied, our results show
that the colonization pattern depends on the texture of the
gypsum. The endolithic cyanobacteria preferentially colonize below microtopographic depressions where water can
pond and infiltrate into the gypsum. The texture of the
gypsum also appears to have a strong influence on the
optical properties of the gypsum and the preferred habitat
for endolithic cyanobacteria. In the micritic and massive
gypsum from the Atacama and Mojave Desert, colonization
occurs at a depth of only a few mm below the surface. In the
fibrous gypsum from the Jordan Desert, the colonization
depth is greater, up to 14 mm. The optimal colonization
depth appears to be achieved by balancing acquisition of
adequate light, O2, and N2 for photosynthesis with water
retention and protection from adverse environmental conditions. In addition to cyanobacteria, heterotrophic bacteria
are also an important component in the community. Both
precipitation and gypsum texture are important in affecting
bacterial diversity and the community structure. These
results are important in defining future targets to look for
modern and ancient life on Mars.
[49] Acknowledgments. The authors are grateful to Judy Costa,
Doug Merkler, Rebecca Burt, and Joe Chiaretti for field and laboratory
data collection. The authors are grateful to two anonymous reviewers for
their constructive comments, and Chris Mckay for helpful discussions
during the development of this project.
References
Abraham, W. R., et al. (1999), Phylogeny and polyphasic taxonomy of
Caulobacter species. Proposal of Maricaulis gen. nov. with Maricaulis
maris (Poindexter) comb. nov. as the type species, and emended description of the genera Brevundimonas and Caulobacter, Int. J. Syst. Evol.
Microbiol., 49, 1053 – 1073.
G02030
Bell, C. M. (1989), Saline lake carbonates within an Upper Jurassic-Lower
Cretaceous continental red bed sequence in the Atacama region of northern Chile, Sedimentology, 36, 651 – 664.
Boison, G., A. Mergel, H. Jolkver, and H. Bothe (2004), Bacterial life and
dinitrogen fixation at a gypsum rock, Appl. Environ. Microbiol., 70,
7070 – 7077.
Brummer, I. H., A. D. Felske, and I. Wagner-Dobler (2004), Diversity and
seasonal changes of uncultured planctomycetales in river biofilms, Appl.
Environ. Microbiol., 70, 5094 – 5101.
Buck, B. J., and J. G. Van Hoesen (2002), Snowball morphology and SEM
analysis of pedogenic gypsum, southern New Mexico, USA, J. Arid
Environ., 51, 469 – 487.
Buck, B. J., K. Wolff, D. Merkler, and N. McMillan (2006a), Salt mineralogy of Las Vegas Wash, Nevada: Morphology and subsurface evaporation, Soil Sci. Soc. Am. J., 70, 1639 – 1651.
Buck, B. J., J. Rech, M. Howell, J. Prellwitz, and A. Brock (2006b), A new
formation process for patterned ground, Atacama Desert, Chile, paper
presented at Geological Society of America Annual Meeting, Philadelphia, Pa., 22 – 25 Oct.
Carr, M. H. (1996), Water on Mars, Oxford Univ. Press, Oxford.
Carter, B. J., and W. P. Inskeep (1988), Accumulation of pedogenic gypsum
in western Oklahoma soils, Soil Sci. Soc. Am. J., 52, 1107 – 1113.
Christensen, P. R., J. L. Bandfield, M. D. Smith, V. E. Hamilton, and R. N.
Clark (2000), Identification of a basaltic component on the Martian surface from Thermal Emission Spectrometer data, J. Geophys. Res., 105,
9609 – 9621.
Christner, B. C., E. Mosley-Thompson, L. G. Thompson, and J. N. Reeve
(2001), Isolation of bacteria and 16S rDNA from Lake Vostok accretion
ice, Environ. Microbiol., 3, 570 – 577.
Clark, B. C., and D. C. Van Hart (1981), The salts of Mars, ICARUS, 45,
370 – 378.
Clark, B. C., A. K. Baird, R. J. Weldon, D. M. Tsusaki, L. Schrabel, and
M. P. Candelaria (1982), Chemical composition of Martian fines, J. Geophys. Res, 87, 10,059 – 10,068.
Cockell, C. S., P. Lee, G. Osinski, G. Horneck, and O. Broady (2002),
Impact-induced mcirobial endolithic habitats, Meteorit. Planet. Sci., 37,
1287 – 1298.
Coolen, M. J. L., and J. Overmann (1998), Analysis of subfossil molecular
remains of purple sulfur bacteria in a lake sediment., Appl. Environ.
Microbiol., 64, 4513 – 4521.
Cooper, C. D., and J. F. Mustard (2002), Spectroscopy of loose and cemented sulphate-bearing soils: implications for duricrust on Mars, ICARUS,
158, 42 – 55.
de la Torre, J. R., B. M. Goebel, E. I. Friedmann, and N. R. Pace (2003),
Microbial diversity of cryptoendolithic communities from the McMurdo
Dry Valleys, Antarctica, Appl. Environ. Microbiol., 69, 3858 – 3867.
de los Rios, A., J. Wierzchos, L. G. Sancho, and C. Ascaso (2004), Exploring the physiological state of continental Antarctic endolithic microorganisms by microscopy, FEMS Microbiol. Ecol., 50, 143 – 152.
de los Rios, A., M. Grube, L. G. Sancho, and C. Ascaso (2007), Ultrastructural and genetic characteristics of endolithic cyanobacterial biofilms
colonizing Antarctic granite rocks, FEMS Microbiol. Ecol., 59, 386 – 395.
Douglas, S. (2004), Microbial biosignatures in evaporite deposits: evidence
from Death Valley, California, Planet. Space Sci., 52, 223 – 227.
Douglas, S., and H. X. Yang (2002), Mineral biosignatures in evaporites:
presence of rosickyite in an endoevaporitic microbial community from
Death Valley, California, Geology, 30, 1075 – 1078.
Drees, K. P., J. W. Neilson, J. L. Betancourt, J. Quade, D. A. Henderson, B. M.
Pryor, and R. M. Maier (2006), Bacterial diversity in the hyper-arid core of
the Atacama desert, Chile, Appl. Environ. Microbiol., 72, 7902 – 7908.
Ericksen, G. E. (1981), Geology and the Origin of the Chilean Nitrate
Deposits, 37 pp.
Ewing, S. A., B. Sutter, J. Owen, K. Nishiizumi, W. Sharp, S. S. Cliff,
K. Perry, W. Dietrich, C. P. McKay, and R. Amundson (2006), A threshold
in soil formation at Earth’s arid-hyperarid transition, Geochim. Cosmochim. Acta, 70, 5293 – 5322.
Fewer, D., T. Friedl, and B. Budel (2002), Chroococcidiopsis and heterocystdifferentiating cyanobacteria are each other’s closest living relatives, Mol.
Phylo. Evol., 23, 82 – 90.
Friedmann, E. I. (1980), Endolithic microbial life in hot and cold deserts,
Origins of Life, 10, 233 – 245.
Friedmann, E. I., and A. M. Koriem (1989), Life on Mars: how it disappeared (if it was ever there), Adv. Space Res., 9, 167 – 172.
Friedmann, E. I., and R. Ocampo (1976), Endolithic blue-green algae in the
dry valleys: primary producers and the Antarctic desert ecosystem,
Science, 193, 1247 – 1249.
Friedmann, E. I., and R. Ocampo-Friedmann (1994), A primitive cyanobacterium as pioneer microorganism for terraforming Mars, Adv. Space
Res., 15, 243 – 246.
10 of 11
G02030
DONG ET AL.: ENDOLITHIC CYANOBACTERIA IN SOIL GYPSUM
Friedmann, E. I., Y. Lipkin, and R. Ocampo-Paus (1967), Desert algae of
the Negev (Israel), Phycologia, 6, 185 – 196.
Friedmann, E. I., C. P. McKay, and J. A. Nienow (1987), The cryptoendolithic microbial environment in the Ross Desert of Antarctic; satellite
transmitted continuous nanoclimate data, Polar Biol., 7, 273 – 287.
Furlong, M. A., D. R. Singleton, D. C. Coleman, and W. B. Whitman
(2002), Molecular and culture-based analyses of prokaryotic communities
from an agricultural soil and the burrows and casts of the earthworm
Lumbricus rubellus, Appl. Environ. Microbiol., 68, 1265 – 1279.
Gendrin, A., et al. (2005), Suffates in martian layered terrains: the OMEGA/
Mars Express view, Science, 307, 1587 – 1591.
Green, P. N. (2001), Methylobacterium, in The Prokaryotes: An Evolving
Electronic Resource for the Microbiological Community, edited by
M. Dworkin, Springer, New York.
Haldeman, D. L. (1997), The storage-related phenomenon: implications for
handling and analysis of subsurface samples, in The Microbiology of the
Terrestrial Deep Subsurface, edited by P. S. Amy and D. L. Haldeman,
CRC Press, Boca Raton, Fla.
Head, J. W., and S. C. Solomon (1981), Tectonic evolution of the terrestrial
planets, Science, 213, 62 – 76.
Herrero, J., and J. Porta (2000), The terminology and concepts of gypsumrich soils, Geoderma, 96, 47 – 61.
Houston, J., and A. J. Hartley (2003), The Central Andean west-slope
rainshadow and its potential contribution to the origin of hyperaridity
in the Atacama Desert, Int. J. Climatol., 23, 1453 – 1464.
Hughes, K. A., and B. Lawley (2003), A novel Antarctic microbial endolithic
community within gypsum crusts, Environ. Microbiol., 5, 555 – 565.
Ionescu, D., A. Lipski, K. Altendorf, and A. Oren (2007), Characterization
of the endoevaporitic microbial communities in a hypersaline gypsum
crust by fatty acid analysis, Hydrobiologia, 576, 15 – 26.
Jiang, H., H. Dong, G. Zhang, B. Yu, L. R. Chapman, and M. W. Fields
(2006), Microbial diversity in water and sediment of Lake Chaka: An
athalassohaline hypersaline lake in Northwestern China, Appl. Environ.
Microbiol., 72, 3832 – 3845.
Johnson, D. B., N. Okibe, and F. F. Roberto (2003), Novel thermo-acidophilic
bacteria isolated from geothermal sites in Yellowstone National Park:
physiological and phylogenetic characteristics, Arch. Microbiol., 180,
60 – 68.
Kedar, L., Y. Kashman, and A. Oren (2002), Mycosporine-2-glycine is the
major mycosporine-like amino acid in a unicellular cyanobacterium
(Euhalothece sp.) isolated from a gypsum crust in a hypersaline saltern
pond, FEMS Microbiol. Lett., 208, 233 – 237.
Klingelhofer, G., et al. (2004), Jarosite and hematite at Meridiani Planum
from Opportunity’s Mossbauer spectrometer, Science, 306, 1740 – 1745.
Kunte, H. J., H. G. Truper, and H. Stan-Lotter (2002), Halophilic microorganisms, in Astrobiology, the Quest for the Conditions of Life, edited by
G. Horneck and C. Baumstark-Khan, Springer, Koln, Germany.
Langevin, Y., F. Poulet, J. P. Bibring, and B. Gondet (2005), Sulfates in the
north polar region of Mars detected by OMEGA/Mars express, Science,
307, 1584 – 1586.
Lu, Y., D. Rosencrantz, W. Liesack, and R. Conrad (2006), Structure and
activity of bacterial community inhabiting rice roots and the rhizosphere,
Environ. Microbiol., 8, 1351 – 1360.
Lueders, T., B. Wagner, P. Claus, and M. W. Friedrich (2004), Stable isotope probing of rRNA and DNA reveals a dynamic methylotroph community and trophic interactions with fungi and protozoa in oxic rice field
soil, Environ. Microbiol., 6, 60 – 72.
Lueders, T., R. Kindler, A. Miltner, M. W. Friedrich, and M. Kaestner
(2006), Identification of bacterial micropredators distinctively active in
a soil microbial food web, Appl. Environ. Microbiol., 72, 5342 – 5348.
McKay, C. P. (1997), The search for life on Mars, Origins of Life and
Evolution of the Biosphere, 27, 263 – 289.
McKay, C. P., and W. L. Davis (1991), Duration of liquid water habitats on
early Mars, ICARUS, 90, 214 – 221.
McKay, C. P., E. I. Friedmann, R. A. Wharton, and W. L. Davis (1992),
History of water on Mars: a biological perspective, Adv. Space Res., 12,
231 – 238.
McLennan, S. M., et al. (2005), Provenance and diagenesis of the evaporitebearing Burns formation, Meridiani Planum, Mars, Earth Planet. Sci. Lett.,
240, 95 – 121.
Mermut, A. R., and M. A. Arshad (1987), Significance of sulfide oxidation
in soil salinization of southeastern Saskatchewan, Canada, Soil Sci. Soc.
Am. J., 51, 247 – 251.
Mrozek, S. J., B. J. Buck, P. J. Drohan, and A. L. Brock (2006), Decorative
landscaping rock as a source for heavy metal contamination, Las Vegas
NV, Soil Sed. Contam., 15, 471 – 480.
Mummey, D. L., and P. D. Stahl (2003), Candidate division BD: phylogeny,
distribution and abundance in soil ecosystems, Syst. Appl. Microbiol., 26,
228 – 235.
G02030
Navarro-Gonzalez, R., et al. (2003), Mars-like soils in the Atacama Desert,
Chile, and the dry limit of microbial life, Science, 302, 1018 – 1021.
Nemergut, D. R., A. P. Martin, and S. K. Schmidt (2004), Integron diversity
in heavy-metal-contaminated mine tailings and inferences about integron
evolution, Appl. Environ. Microbiol., 70, 1160 – 1168.
Nettleton, W. D. (1991), Occurrence, characteristics, and genesis of carbonate, gypsum, and silica accumulation in soils, 149 pp., Soil Sci. Soc. of
Am., Madison, Wis.
Omelon, C. R., W. H. Pollard, and F. G. Ferris (2006), Chemical and
ultrastructural characterization of high arctic cryptoendolithic habitats,
Geomicrobiol. J., 23, 189 – 200.
Oren, A., M. Kuhl, and U. Karsten (1995), An endoevaporitic microbial
mat within a gypsum crust: zonation of phototrophs, photopigments, and
light penetration, Mar. Ecol. Prog. Ser., 128, 151 – 159.
Parnell, J., P. Lee, C. S. Cockell, and G. R. Osinski (2004), Microbial colonization in impact-generated hydrothermal sulphate deposits, Haughton
impact structure, and implications for sulphates on Mars, Int. J. Astrobiol.,
3, 247 – 256.
Podwojewski, P., and M. Arnold (1994), The origin of gypsum in Vertisols in
New Caledonia determined by isotopic composition of sulfur, Geoderma,
63, 179 – 195.
Priscu, J. C., and B. C. Christner (2004), Earth’s icy biosphere, in Microbial
Diversity and Bioprospecting, edited by A. T. Bull, pp. 130 – 145, ASM
Press, Washington, D. C.
Rech, J. A., J. Quade, and W. J. Hart (2003), Isotopic evidence for the
source of Ca and S in soil gypsum, anhydrite, and calcite in the Atacama
Desert, Chile, Geochim. Cosmochim. Acta, 67, 575 – 586.
Rheims, H., F. A. Rainey, and E. Stackebrandt (1996), A molecular approach to search for diversity amomg bacteria in the environment, J. Ind.
Microbiol., 17, 159 – 169.
Rippka, R., J. Deruelles, J. B. Waterbury, M. Herdman, and R. Y. Stainer
(1979), Generic assignments strain histories and properties of pure cultures of cyanobacteria, J. Gen. Microbiol., 111, 1 – 61.
Rothschild, L. J., L. J. Giver, M. R. White, and R. L. Mancinelli (1994),
Metabolic-activity of microorganisms in evaporites, J. Phycol., 30, 431 –
438.
Sanz-Montero, M. E., J. P. Rodriguez-Aranda, and J. P. Calvo (2006),
Mediation of endoevaporitic microbial communities in early replacement
of gypsum by dolomite: a case study from Miocene lake deposits of the
Madrid Basin, Spain, J. Sed. Res., 76, 1257 – 1266.
Solomon, S. C. (1978), Volcanism and thermal tectonics on one-plate planets, Geophys. Res. Lett., 5, 461 – 464.
Squyres, S. W., et al. (2004), In situ evidence for an ancient aqueous
environment at Meridiani Planum, Mars, Science, 306, 1709 – 1714.
Taimeh, A. Y. (1992), Formation of gypsic horizons in some arid regions of
Jordan, Soil Sci., 153, 486 – 498.
Takami, H., K. Kobata, T. Nagahama, H. Kobayashi, A. Inoue, and
K. Horikoshi (1999), Biodiversity in deep-sea sites located near the south
part of Japan, Extremephiles, 3, 97 – 102.
Taton, A., S. Grubisic, E. Brambilla, R. De Wit, and A. Wilmotte (2003),
Cyanobacterial Diversity in Natural and Artificial Microbial Mats of Lake
Fryxell (McMurdo Dry Valleys, Antarctica): a Morphological and Molecular Approach, Appl. Environ. Microbiol., 69, 5157 – 5169.
Taton, A., S. Grubisic, P. Balthasart, D. A. Hodgson, J. Laybourn-Parry, and
A. Wilmotte (2006), Biogeographical distribution and ecological ranges
of benthic cyanobacteria in East Antarctic lakes, FEMS Microbiol. Ecol.,
57, 272 – 289.
Toulkeridis, T., P. Podwojewski, and N. Clauer (1998), Tracing the source
of gypsum in New Caledonian soils by REE contents and S-Sr isotopic
compositions, Chem. Geol., 145, 61 – 71.
Vreeland, R. H., W. D. Rosenzweig, and D. W. Powers (2000), Isolation of
a 250 million-year-old halotolerant bacterium from a primary salt crystal,
Nature, 407, 897 – 900.
Warren-Rhodes, K. A., K. L. Rhodes, S. B. Pointing, S. A. Ewing, D. C.
Lacap, B. Gomez-Silva, R. Amundson, E. I. Friedmann, and C. P. McKay
(2006), Hypolithic cyanobacteria, dry limit of photosynthetic and microbial community ecology in the hyperarid Atacama Desert, Microb. Ecol.,
52, 389 – 398.
Wierzchos, J., C. Ascaso, and C. P. McKay (2006), Endolithic cyanobacteria in halite rocks from the hyperarid core of the Atacama desert,
Astrobiology, 6, 415 – 422.
""""""""""""""""""""""
B. J. Buck, Department of Geosciences, University of Nevada, Las
Vegas, NV 89154, USA.
H. Dong, H. Jiang, and J. A. Rech, Department of Geology, Miami
University, Oxford, OH 45056, USA. ([email protected])
H. Sun, Division of Earth and Ecosystem Sciences, Desert Research
Institute, Las Vegas, NV 89119, USA.
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