Control of Lunar and Martian dust--experimental insights from artificial and natural cyanobacterial and algal crusts in the desert of Inner Mongolia, China.
ABSTRACT Studies on the colonization of environmentally extreme ground surfaces were conducted in a Mars-like desert area of Inner Mongolia, People's Republic of China, with microalgae and cyanobacteria. We collected and mass-cultured cyanobacterial strains from these regions and investigated their ability to form desert crusts artificially. These crusts had the capacity to resist sand wind erosion after just 15 days of growth. Similar to the surface of some Chinese deserts, the surface of Mars is characterized by a layer of fine dust, which will challenge future human exploration activities, particularly in confined spaces that will include greenhouses and habitats. We discuss the use of such crusts for the local control of desert sands in enclosed spaces on Mars. These experiments suggest innovative new directions in the applied use of microbe-mineral interactions to advance the human exploration and settlement of space.
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ABSTRACT: The supportive and negative evidence for the stress gradient hypothesis (SGH) led to an ongoing debate among ecologists and called for new empirical and theoretical work. In this study, we took various biological soil crust (BSCs) samples along a spatial gradient with four environmental stress levels to examine the fitness of SGH in microbial interactions and evaluate its influence on biodiversity-function relationships in BSCs. A new assessment method of species interactions within hard-cultured invisible soil community was employed, directly based on denaturing gradient gel electrophoresis fingerprint images. The results showed that biotic interactions in soil phototroph community dramatically shifted from facilitation to dominant competition with the improvement of microhabitats. It offered new evidence, which presented a different perspective on the hypothesis that the relative importance of facilitation and competition varies inversely along the gradient of abiotic stress. The path analysis indicated that influence of biotic interactions (r = 0.19, p < 0.05) on ecosystem functions is lower than other community properties (r = 0.62, p < 0.001), including soil moisture, crust coverage, and biodiversity. Furthermore, the correlation between species interactions and community properties was non-significant with low negative influence (r = -0.27, p > 0.05). We demonstrate that the inversion of biotic interaction as a response to the gradient of abiotic stresses existed not only in the visible plant community but also in the soil microbial community.Microbial Ecology 04/2013; 65:700-708. · 3.28 Impact Factor
Article: Shifting Species InteractionMicrobial Ecology 01/2013; · 3.28 Impact Factor
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ABSTRACT: As the dominant cyanobacterial species in biological soil crusts (BSCs), Microcoleus vaginatus often suffer from many stress conditions, such as desiccation and high temperature. In this study, the activities of light harvesting complexes (LHCs) and reaction centers of photosystem (PS) II in crust cyanobacteria M. vaginatus were monitored under high temperature and desiccation conditions using chlorophyll fluorescence technology. The results showed that all the fluorescence signals were significantly inhibited by high temperature or desiccation treatments. Under high temperature conditions, it was further demonstrated PS II reaction centers were first destructed within the first hour, then the LHCs gradually dissociated and free phycocyanin formed within 1-5 hours, and the activities of all the light harvesting and reaction center pigment proteins were fully suppressed after 24 hours of high temperature treatment. Furthermore, the high temperature treated M. vaginatus lost its ability to recover photosynthetic activity. On the contrary, although desiccation also led to the loss of photosynthetic activity in M. vaginatus, after rehydration in the light the fluorescence parameters including Fo, Fv and Fv/Fm could be well recovered within 12 hours. It was concluded desiccation could provide crust cyanobacteria M. vaginatus some protection from other stresses, such as high temperature demonstrated in this experiment. The combine of temperature change and precipitation pattern in the field provide a guarantee for the alternate metabolism and inactivity in crust cyanobacteria. That may be a very important strategy for the survival of crust cyanobacteria in high temperature regions.Physiologia Plantarum 02/2014; · 3.66 Impact Factor
Volume 8, Number 1, 2008
© Mary Ann Liebert, Inc.
Control of Lunar and Martian Dust—Experimental
Insights from Artificial and Natural Cyanobacterial and
Algal Crusts in the Desert of Inner Mongolia, China
YONGDING LIU,1CHARLES S. COCKELL,2GAOHONG WANG,1CHUNXIANG HU,1
LANZHOU CHEN,3and ROBERTO DE PHILIPPIS4
Studies on the colonization of environmentally extreme ground surfaces were conducted in
a Mars-like desert area of Inner Mongolia, People’s Republic of China, with microalgae and
cyanobacteria. We collected and mass-cultured cyanobacterial strains from these regions and
investigated their ability to form desert crusts artificially. These crusts had the capacity to re-
sist sand wind erosion after just 15 days of growth. Similar to the surface of some Chinese
deserts, the surface of Mars is characterized by a layer of fine dust, which will challenge fu-
ture human exploration activities, particularly in confined spaces that will include green-
houses and habitats. We discuss the use of such crusts for the local control of desert sands in
enclosed spaces on Mars. These experiments suggest innovative new directions in the applied
use of microbe-mineral interactions to advance the human exploration and settlement of space.
Key Words: Desert algae—Cyanobacteria—Colonization—Soil—Mars—Dust. Astrobiology 8,
et al., 2006; Laurent et al., 2006). During the de-
velopment of a human presence on Mars, it will
be necessary to control the dust in enclosed
spaces, particularly in greenhouses and habitats.
A similar challenge exists on the surface of the
Moon (Taylor, 2005). Organisms that naturally
grow on the surface of desert soils on Earth could
INE, UBIQUITOUSLY DISTRIBUTED DUST is a feature
of both martian and terrestrial deserts (Kahre
provide insights into how to employ applied ge-
omicrobiology to control dust on the surfaces of
other celestial bodies in enclosed environments.
Certain desert regions on Earth approximate
the surface of Mars in terms of a number of en-
vironmental characteristics (e.g., Navarro-Gonza-
lez et al., 2003; Bridges et al., 2004; Wentworth et
al., 2005). Particularly, terrestrial deserts provide
a model for the extreme aridity of the martian sur-
face. Although even the most extreme terrestrial
deserts receive more water from precipitation
1State Key Laboratory of Freshwater Ecology and Biotechnology, Institute of Hydrobiology, The Chinese Academy
of Sciences, Wuhan, China.
2Planetary and Space Sciences Research Institute, Open University, Milton Keynes, UK.
3School of Resource and Environmental Sciences, Wuhan University, Wuhan, China.
4Department of Agricultural Biotechnology, University of Florence, Florence, Italy.
and fog than the surface of Mars, arid terrestrial
deserts are often characterized by dry, dusty con-
ditions and extreme-tolerant biota (Eldridge and
Greene, 1994; Chen et al., 2003; Warren-Rhodes et
al., 2006; Lester et al., 2007), which could provide
a useful stock of organisms for use in various as-
pects of planetary settlement.
As there is little or no cohesion between soil
particles in many terrestrial desert environments
(which is also the case for the martian surface),
dust storms with the capacity to bury and destroy
organisms are a major consideration. Terrestrial
desert organisms are well adapted to being fre-
quently covered in dust (Hu et al., 2002a, 2002b).
In terrestrial deserts, diurnal surface tempera-
ture variations can be large and can have adverse
affects on biomembrane integrity and metabolic
activity (Potts, 1999; Chen et al., 2003). Although
temperatures in extraterrestrial greenhouses
could be controlled, terrestrial deserts provide a
source of organisms that are robust against tem-
Some of the organisms that live under extreme
conditions in terrestrial deserts are cyanobacteria.
Cyanobacteria are ubiquitous photoautotrophic
microorganisms that can survive in various en-
vironments: desert mountains, icy regions (in-
cluding Antarctica), fertile riversides, permafrost,
or even heavily polluted regions (Whitton and
Potts, 2000; Friedmann and Ocampo-Friedmann,
1995; Cockell et al., 2002; Garcia-Pichel et al., 2001).
The structure of terrestrial phototrophic commu-
nities has been characterized in the hyper-arid,
ultracold Antarctic Dry Valleys, where, with re-
spect to temperature and aridity, the climate is
similar to Mars, albeit less extreme (Friedmann,
1980; McKay and Friedmann, 1985; Wierzchos
and Ascaso, 2002).
In desert crusts, cyanobacteria commonly grow
on the surface or at a depth down to several cen-
timeters, where they aggregate soil particles and
sand grains. Thereafter, other microorganisms
take part in the formation of a desert microbial
crust. As pioneer organisms, cyanobacteria are of-
ten the first organisms to grow in harsh desert en-
vironments. They gradually affect and change the
surrounding environment. For example, they fix
nitrogen and produce photosynthate; this allows
other organisms to survive and grow at later suc-
cessional stages (Danin et al., 1998). Their ability
to fix nitrogen has previously made cyanobacte-
ria favored organisms for soil conditioning and
biofertilization (Hu and Liu, 2003; Hu et al.,
Cyanobacteria have already been suggested as
possible agents for the planetary-scale environ-
mental alteration of Mars. Chroococcidiopsis spp.
is one of the most desiccation- and nutrient-star-
vation–resistant cyanobacterial genera (Billi and
Grilli Caiola, 1996; Billi et al., 2000). It is found in
a wide range of extreme hot and cold desert envi-
ronments (Fewer et al., 2002; Rezanka et al., 2003).
It has been suggested that Chroococcidiopsis spp.,
due to its remarkable tolerance of extremes, is a
likely candidate as a pioneer photosynthetic mi-
croorganism in the terraforming of Mars (Fried-
mann and Ocampo-Friedmann, 1995). Other
phototrophs, such as Matteia sp., a lime-boring
cyanobacterium isolated from Negev desert
rocks, could be used to dissolve carbonate rocks
both for initial release of CO2and for the design
of a martian carbon cycle, which would be one of
the most serious challenges in terraforming
(Friedmann et al., 1993). Martian carbonates, how-
ever, remain elusive.
Prior to such ambitious engineering specula-
tions, however, there are local environmental
problems on the Moon and Mars that will be en-
countered during early human exploration and
settlement, particularly the control of fine dust in
enclosed greenhouse and habitat structures. In
contrast to terraforming, these problems are more
tractable short-term geomicrobiological chal-
Here we describe experiments in which we
used artificial algal crusts in the “Mars-like” ar-
eas in Inner Mongolia, China. Investigations on
the desert, sand-consolidating properties of bio-
logical crusts are described. The use of desert
phototrophs for local control of dust in enclosed
habitats on Mars or the Moon is discussed.
Algal crusts were collected from Shapotou
(37°27?N, 104°57?E), which is located in the south-
east of the Tengger Desert, Ningxia Hui Au-
tonomous Region of China, and at an altitude of
1200 m above sea level. The climate can be char-
acterized as that of a typically continental mon-
soon pattern, with windy days (?5 m s?1) for
more than 200 d yr?1, average precipitation 186
mm yr?1(mainly in summer), and evaporation
of more than 2900 mm yr?1. The average annual
soil surface temperature is 9.6°C with the highest
LIU ET AL.76
temperature, in summer, reaching 74°C. The low-
est winter temperature is ?25°C (Hu et al., 2003).
Sampling, determination of dominant species, and
analyses of soil physico-chemical properties
Desert crusts in Shapotou were collected as ap-
proximately 50 mm diameter cores with an asep-
tic ring-knife. Samples were collected at 6 differ-
ent sites (designated S1–S6) during the summer
of 1997 and 1998 (see Table 1 for details). Site 6
was a control site with no crust. The crusts were
of different ages (Table 1). The age of the crusts
was defined as the time since the area was closed
to human and animal movements, which is the
main destructive factor for desert crusts in China.
This was accomplished by their enclosure behind
iron banisters in 1956, 1964, 1981, 1990, and 1994.
A section of each sample was packed into steril-
ized aluminum boxes or petri dishes and en-
closed with parafilm or in sterilized paper bags
(Liu and Li, 1989; Hu et al., 2003). The samples
cut from different sites were collected separately
(4–6 replications for each sample). Samples from
vertical layers (0–50 mm and 50–100 mm below
the surface) were also collected from each site.
Phototrophs were identified and counted by
the methods of Liu and Li (1989). Some organ-
isms were enriched and isolated in a diversity of
media (Chu’s 10, BBM, BG11, and HB-D1 agar
media), and cultured under 70 ?mol m?2? s?1
with a sunlight lamp (Philip, TLD 30W/54 YZ
30RR25, Netherlands) in an incubator at a tem-
perature of 30 ? 2°C for 15 or 30 days. Dominant
species were determined by way of Importance
Value (I.V.), which was defined as:
I.V. ? Relative Number
? Relative Volume ? Relative Frequency
as described by Hu and Liu (2003). Volume was
the mean value of each species that could be mea-
sured (some species were too small to be mea-
sured effectively using optical microscopy). Only
those organisms with I.V. ? 1.0 at all sites were
measured as dominant species. For cyanobacte-
ria and diatoms, the mean volume of each species
was obtained from measurements of 50 individ-
uals with direct observation of field samples by
optical microscopy, while green alga and euglena
values were obtained from the observation of cul-
Soil crust samples were analyzed with stan-
dard soil analysis methods. In brief, for pH val-
ues, samples were aseptically mixed 1:5 with dis-
tilled water (w/v), and after 30 min pH was
determined. Organic matter was estimated by di-
gestion with 1 M potassium dichromate; total and
available nitrogen were analyzed with the Kjel-
dahl method (Hu et al., 2003).
The biomass of phototrophs was expressed as
the chlorophyll content of the crust. Two grams
of sample were ground in 90% acetone to 10 ml
total volume, and 2.5 ml of DMSO was added.
The samples were refrigerated in the dark at 4°C
overnight. Samples were centrifuged (7000 rpm,
10 min), the supernatants were separated, and ab-
sorbance was measured with a spectrophotome-
ter (Ultrospec 3000 UV/Visible Spectrophoto-
meter, Pharmacia Biotech). The chlorophyll
ARTIFICIAL CRUST FOR SOIL COLONIZATION 77
TABLE 1.CHARACTERISTICS OF NATURAL DESERT CRUSTS EXAMINED IN THIS STUDY
SitesS1 S2 S3S4S5S6
5.17 ? 0.16
3.37 ? 0.07
1.57 ? 0.06
3.33 ? 0.09
Site age (yr)
2.33 ? 0.14 Without
33 25 1550
concentration at 663 nm, 384 nm, and 490 nm was
estimated with the trichromatic equations of
Garcia-Pichel and Castenholz (1991), which cor-
rect the chlorophyll absorbance for absorption
due to the cyanobacterial sheath pigments and
Isolation, mass culture of organisms, and
colonization of desert soil
For colonization experiments, 4 filamentous
Phormidium tenue (Menegh.) Gom., Scytonema ja-
vanicum (Kutz.) Born. et Flah., and Nostoc sp.—
and a single-celled green alga, Desmococcus oli-
vaceus (Pers. ex Ach.) Laundon, all of which
were isolated from Shapotou crusts (37°27?N,
104°57?E), were selected because they were found
to be the dominant species and had the largest
biomass in the crusts. They were batch cultured
first in 200 ml bottles, and then in 5 L bottles in
BG11 at a temperature of 25 ? 2°C and an irra-
diance of 50 ?mol photon m?2? s?1. They were
bubbled with ambient air. After 20 days of
growth, the organisms were harvested by filtra-
tion through silk, and all of them were directly
inoculated with a sprayer as homogeneously as
possible onto the same batches of unconsolidated
sand at a density of about 0.3 mg chlorophyll
a/g.d.s (per g dry soil) of soil. Experiments were
conducted in the greenhouse and in the field.
The experiments all used aeolian sandy soil,
which was composed of 94.98% fine sand
(0.05–0.25 mm) and 4.79% coarse sand (0.25–1.00
mm) and is representative of typical desert sand
To show that the organisms can be used to col-
onize a region other than the one from which they
were isolated, similar experiments were carried
out in an Inner Mongolian desert. Because the col-
onization experiment in Shapotou indicated that
M. vaginatus and S. javanicum are the best strains
for formation of crust at Shapotou desert (Hu et
al., 2002a), they were selected to establish mass
cultivation experiments in Dalateqi, Inner Mon-
golia (40°21’N, 109°51’E). The organisms were
cultivated in a 40 ? 6 ? 0.25 m cycle culture pond
with groundwater in a greenhouse at Shapotou
desert. The cultures were harvested by gravity
deposition and directly inoculated with a pro-
portion of 10:1 (M. vaginatus: S. javanicum) onto
unconsolidated sand in 2500 m2field plots in
Dalateqi with a biomass of about 0.6 mg chloro-
phyll a/g.d.s. Different experiments were also
carried out in areas with shrub (Salix psammophila)
and grass (Aneurolepidium chinensis) cover, and
without vegetation cover, to compare the effect
of this vegetation on crust formation. The plots
were irrigated with 20 mm of groundwater per
day by automatic sprinkling micro-irrigation fa-
cilities from 9:00 to 16:30.
Analysis of Ca2?, Mg2?, and K?was run on
leachates of dried samples of artificial crusts from
Dalateqi as described by Bender et al. (1994). All
data are reported as mean values of 4–8 determi-
Wind-tunnel experiments were conducted in
the wind-tunnel laboratory of the Lanzhou Insti-
tute of Desert Research, Chinese Academy of
Sciences (Hu et al., 2002b). The tunnel provided
laminar air flow under low velocity. The experi-
mental segment was 21 m long, with a cross sec-
tion of 1.2 ? 1.2 m. Natural unconsolidated sand
from Shapotou was delivered into the air stream
at the entrance of the tunnel working section,
12 m upstream of the crust surface. The long di-
mension of the trays paralleled the length of the
tunnel. To prepare artificial crust for the wind-
tunnel experiments, rectangular trays (30 ? 40 ?
2.8 cm) were filled with unconsolidated sterilized
sand from Shapotou to 2.3–2.4 cm high, water-
soaked, and leveled. Cultured cyanobacteria
were then harvested by filtering through silk fab-
ric as described above. The organisms were
spread into a thin layer, air dried, and ground to
pass through a mesh sieve. The dried cells were
then rehydrated and sprayed onto trays as ho-
mogeneously as possible (so that the culture was
distributed evenly over the tray). In all experi-
ments, 4 replicates were used for each treatment.
Trays were kept in the greenhouse and in the field
at Shapotou, where the highest air temperature
was 43°C, with a surface sand temperature of
8–38°C. The trays were watered with a fogger at
8:30 and 17:30 (100 ml each time, each tray). At
11:30 and 14:10, the trays were sprayed with BG11
medium under the same conditions. The control
groups were the same sand without culture ad-
dition. In all cases, the final water content and
biomass of air-dried sands were determined be-
fore the wind tunnel experiments by subsampling
the plots outside the test area. After 15 days cul-
LIU ET AL. 78
tivation, the trays with artificial crusts were put
into the wind tunnel to test their strength. In one
experiment, samples of the natural crusts from
Shapotou (S1–S5, Table 1) were also tested for
their ability to withstand high wind by applying
a 25 m s?1wind for 2 hours.
Trays were level with the bottom of the tunnel
to maintain laminar, non-turbulent flow. Wind
speed was measured with a pitot tube. Wind
speeds of 5, 6, 10, 12, 15, 20, 25 m s?1were used
during the course of the studies. Five-minute ex-
posure times were used. The threshold friction
velocity—that surface velocity at which erosion
first begins to occur—was determined as a mea-
sure of the strength of the crust. Two different
types of threshold friction velocity were used
here: “net wind,” which means that the wind is
composed of gas or wind with different speeds,
and “sand-holding wind,” which means that the
wind blows the surface of soil and entrains solid
materials, similar to a sand and dust storm.
The distribution of algae in the natural desert crust
In natural crusts (S1–S5), a total of 24 taxa were
recorded from the studied area (Table 1, Fig. 1),
of which cyanobacteria (10 taxa) were the most
diverse group, followed by diatoms (7 taxa),
green algae (5 taxa), and euglena (2 taxa). There
were no organisms, however, at the control site
(S6) at Shapotou. The 5 dominant cyanobacterial
species, as determined by the largest I.V. num-
bers (data not shown) were Microcoleus vaginatus
Gom., Scytonema javanicum Born. et Flah., Lyng-
bya cryptovaginatus Schk., Phormidium tenue Gom.,
and Nostoc sp.
The vertical distribution of cyanobacteria and
microalgae in the crusts was distinctly laminated
and consisted (from top down) of an inorganic
layer (ca. 0.00–0.02 mm, with few organisms), an
organism-dense layer (ca. 0.02–1.0 mm), and an
ARTIFICIAL CRUST FOR SOIL COLONIZATION79
Bar indicates 0.3 m length.
Photographs of natural crust (A, B) in Shapotou and artificial crust (C, D) in Dalateqi formed in field.
organism-impoverished layer (ca. 1.0–5.0 mm).
In all crusts, Scytonema javanicum Born. et Flah.
(or Nostoc sp., cyanobacterium), Desmococcus oli-
vaceus (Pers. ex Ach.) Laundon (green alga), and
Microcoleus vaginatus Gom. (cyanobacterium)
dominated at a depth of 0.02–0.05, 0.05–0.1, and
0.1–1.0 mm, respectively. Phormidium tenue Gom.
(or Lyngbya cryptovaginatus Schk., cyanobac-
terium) and Navicula cryptocephala Kutz. [or
Hantzschia amphioxys (Ehr.) Grun.] dominated at
the depth of 1.0–3.0 and 3.0–4.0 mm, respectively,
of the crusts from the 42- and 34-year-old sites
(Table 2). It was apparent that, in more developed
crusts, there were more green algae, and the
niches of Nostoc sp., Chlorella vulgaris Beij., M.
vaginatus, N. cryptocephala and fungi were nearer
to the surface.
The effects of phototroph colonization on
The biomass of microalgae of natural crusts in-
creased at an early stage of colonization (Fig. 2)
but decreased at a later stage. The possible rea-
son for this is that other species were not able to
compete with the cyanobacteria due to their in-
feriority in sand stabilization, UV resistance, and
desiccation resistance. The thickness and spatial
heterogeneity of the crusts increased over time
LIU ET AL. 80
TABLE 2.VERTICAL MICRODISTRIBUTION OF SPECIES WITHIN THE NATURAL DESERT CRUSTS
Depth 0.00–0.02 mm 0.02–0.05 mm0.05–0.1 mm 0.1–1.0 mm1.0–3.0 mm3.0–4.0 mm
For the 42- and 34-year old
crusts For all crusts
222 19 137
FIG. 2. Soil analysis of crust with different ages showing key parameters. Error bars are standard deviation.
As is shown in Fig. 2, soil fertility (as measured
by available nitrogen and organic matter) of all
crusts also remained high after 1 year of colo-
nization, which indicates that the phototrophs
may be effective as soil-conditioning biofertiliz-
ers due to the fact that some of them are capable
of fixing nitrogen from the atmosphere. The pH
values of different crusts were found to vary be-
tween 7.9 and 8.1.
Experiments on artificial colonization of desert
soil with cyanobacteria
Figure 3A shows that the artificial crust formed
in Shapotou grew much faster in the greenhouse
than in the field. It may have been that conditions
in the greenhouse prevented water evaporation,
which then accelerated the growth of cyanobac-
teria. Artificial crusts of Dalateqi formed 10 days
after inoculation (Fig. 1C–D, Fig. 3B). Crusts that
grew under grasses or shrubs had a higher bio-
mass than those that grew on unconsolidated
sand (Fig. 3B). The vegetation accelerated the suc-
cession of community structure and the stabi-
lization of mobile sand dunes. Cyanobacteria
diversity had also changed 22 days after inocula-
tion. In all experiments in Dalateqi, M. vaginatus
accounted for more than 99% of biomass, and Scy-
tonema javanicum, Phormidium tenue, and Nostoc
sp. comprised less than 1%.
Soil chemical analysis showed that there were
no significant differences in terms of N, P, Ca2?,
ARTIFICIAL CRUST FOR SOIL COLONIZATION81
Shapotou (A) and in Dalateqi (B) with differ-
ent culture conditions. Greenhouse, inoculation
with organisms on unconsolidated sand in green-
house; Field, inoculation with organisms on un-
consolidated sand in the field; Shrub cover ? in-
oculation, cover with Salix psammophila and
inoculation with organisms on unconsolidated
sand; Grass cover ? inoculation, cover with
Aneurolepidium chinensis and inoculation with or-
ganisms on unconsolidated sand; No cover ? in-
oculation, no cover and inoculation with organ-
isms on unconsolidated sand; No cover ? no
inoculation, no cover and no inoculation with or-
ganisms on unconsolidated sand as the control.
Error bars are standard deviation.
The growth curves of desert algae in
and Mg2?content measured in soils from the col-
onization sites compared to those in the control
areas at Dalateqi but that colonization sites were
significantly higher (p ? 0.05, one-way analysis
of variance) in K?, biomass, and organic com-
pounds (Table 3).
Wind-tunnel experiments of artificial crust
Since our previous experiments on coloniza-
tion indicated that M. vaginatus is the best strain
for formation of crust (Hu et al., 2002a), we car-
ried out experiments using M. vaginatus to test
the relationship between biomass and crust
strength. It was found that M. vaginatus stabilized
the sand surface both with and without sand in
the air stream. The higher the biomass, the higher
the threshold friction velocity (ms?1) of the crusts
(Fig. 4), which indicated that the cyanobacteria in
LIU ET AL.82
vaginatus crusts and the threshold friction veloc-
ity (5 min) of crust under net wind (A) and sand-
holding wind (B) when measured with a wind-
Relationship between biomass of M.
ARTIFICIAL CRUSTS FORMED IN DALATEQI UNDER
DIFFERENT TREATMENTS IN FIELD
SOIL PHYSICOCHEMICAL PROPERTIES OF
Total N (mg/g)
Total P (mg/g)
Biomass (?g chl a/cm2)
Organic compounds (mg/g)
0.3 ? 0.00
0.4 ? 0.10
5.2 ? 0.70
41 ? 10 0
24 ? 0.90
0.12 ? 0.01
0.3 ? 0.10
0.5 ? 0.20
0.3 ? 0.00
7.2 ? 0.90
46 ? 6 00
28.2 ? 4.30
0.41 ? 0.10
19.3 ? 1.60
The data were averages and s.d., n ? 3.
CK is the control site, which was not inoculated and ir-
the artificial crust improved the strength of the
All initial inocula were the same for each
species and combinations, but marked differ-
ences were noted among taxa (Table 4) when they
were tested at similar biomass levels. Mix 1 was
a combination in which M. vaginatus, P. tenue, S.
javanicum, Nostoc sp., and D. olivaceus accounted
for 80%, 5%, 5%, 5%, and 5%, respectively; Mix 2
was a combination of equal percentages of the 5
cyanobacteria (20% each). The results from the
wind-tunnel experiments indicated that the sta-
bilization capacity of the organisms from highest
to lowest was M. vaginatus, P. tenue, S. javanicum,
Nostoc sp., D. olivaceus (Table 4). The effect of Mix
1 was better than Mix 2 because the threshold fric-
tion velocity of the crust with Mix 1 was higher
than that of the crust with Mix 2 (Table 4). M.
vaginatus was among the most effective stabiliz-
ers with regard to threshold friction velocity.
All natural crusts (S1–S5) in our study had
great strength and could resist sand-laden wind
at the speed of 25 ms?1for at least 2 h (data not
The surface of Mars is covered by a ubiquitous
layer of dust that is globally similar in its miner-
alogical characteristics (Hamilton et al., 2005). In
enclosed structures, such as greenhouses or habi-
tats, the control of surface dust will be a perva-
sive challenge, particularly if plants are to be
grown directly in the soil. It will be necessary to
control dust between and near the plants. Fur-
thermore, the martian soil is likely to be nutrient
poor. By “conditioning” the surface dust with
desert crust organisms, including nitrogen fixers,
it may be rendered a more suitable substrate for
plant growth systems and provide for closed-
loop life support systems (Birch, 1992; Haynes
and McKay, 1992; Cockell, 2001; Wang et al.,
2004a, 2004b, 2006).
Desert crusts could be used to landscape soils
in and around walkways in habitats—essentially
extraterrestrial “gardening.” Although this may
appear a frivolous concern, the monotonous grey
and red landscapes of the Moon and Mars, re-
spectively, make the concept of adding green and
other colored biofilms to soils in habitats attrac-
tive. Desert crusts could even be seen as a way to
mitigate the negative psychological impact of
these environments by adding to the landscape a
biotic component that would need minimum
Our experiments using wind tunnels in Mars-
like Chinese deserts show that the colonization of
soil with phototrophs stabilizes fine sands be-
cause the threshold friction velocity (ms?1) of the
soil increases after colonization with cyanobac-
terium. Our previous studies show that the ef-
fects of phototrophs on soil are likely a result of
the excretion into the surrounding soil of a vari-
ety of low-molecular, extracellular polymeric
substances that help form a microbiological crust
on the soil surface that is resistant to sandstorm
erosion (Hu et al., 2002b). Previous experiments
have also shown how the excretion into the sur-
rounding soil of a variety of low-molecular, ex-
tracellular polymeric substances helped stabilize
unconsolidated sand even after colonization for
only 1 month in natural crusts (Hu et al., 2002b).
As was revealed by their tolerance of the artifi-
cial wind tests in the experiments, the greater
strength of the natural crusts (which are several
decades old) in comparison to the artificial crusts
shows that crusts that have endured over long
periods of time can effectively bind soils.
Although the exact species used in any attempt
to alter martian desert sands would depend on
the optimum growth rates in martian soils, the
experiments we present provide a generalized
model for how microbial crusts can be used,
rapidly, to create a solid, consolidated surface.
We found that single species of cyanobacteria,
and mixes of them, could be used to bind desert
sands, and that consolidated crusts could be
formed within the order of tens of days, all of
which shows that the biota needed to create such
crusts does not require the complexity of natural
ARTIFICIAL CRUST FOR SOIL COLONIZATION 83
CRUSTS MADE FROM DIFFERENT ORGANISMS (VELOCITY AT
WHICH THE CRUST FIRST BEGINS TO BE DESTROYED)
THE THRESHOLD FRICTION VELOCITY FOR DESERT
velocity (ms?1) Wind Species
Experiment was for 5 min. Identical biomass was used
for all experiments (see text for details).
communities. The wind-tunnel experiments
showed how the crusts can consolidate the sur-
face material and enhance the erosion resistance
of the surface, which suggests that they can be
used to prevent dust from being lofted into the
air by air circulation in life support systems. Al-
though our wind-tunnel experiments on artificial
crusts were of a short duration (5 min), the pres-
ence of crusts in Shapotou that are 42 years old
confirms that, in natural environments, such
crusts can recover from, and resist, wind-induced
destruction for long periods of time.
The community analysis by microscopy
showed that species introduced at the initial
stages can persist over long periods of time and
provide the basis for a long-lived crust. With the
pioneering improvement of cyanobacteria on the
martian soil, other organisms can then be added.
For colonization, it was found that available liq-
uid water is an essential factor for the process (Hu
et al., 2003). Water would, therefore, have to be
provided for the development and continuation
of the crust.
Primary crusts could be initiated by the addi-
tion of a dried powder of organisms. The desic-
cation tolerance of the organisms would allow
them to be transported to Mars and then de-
ployed in the enclosed structures.
Soil crusts, such as those that we have de-
scribed here, are susceptible to damage by human
movements; hence, we confined our studies to
crusts that have been protected. This would ob-
viously limit their use in areas where there is con-
tinuous human activity. Specific locations in
which we could see a use for these crusts include
the following: areas around plants and vegetation
in life-support systems where soils need to be
controlled and human activity is limited; in and
around the edges of habitats where natural sands
might be exposed and need controlling; deliber-
ate landscaping of martian and lunar sands near
walkways and in habitats to create regions of aes-
We did not investigate crust formation in lu-
nar and martian analog soils. The size fraction of
Chinese desert sands used here (fine 0.05–0.25
mm and coarse 0.25–1.00 mm sand) is not dis-
similar to the sand fractions measured, for ex-
ample, at Meridiani Planum, Mars, with one pop-
ulation of grains of size ?0.125 mm and another
between 1 and 4.5 mm (Weitz et al., 2006). There
is, however, variation across the surface of Mars
(Dollfus et al., 1993). The grain sizes and behav-
ior of clays, silt, and sands found in terrestrial
desert sands have previously been recognized as
potential analogues for understanding grain size
and behavior in martian deserts (Greeley and
Williams, 1994). On the Moon and on Mars there
is a large inventory of very fine dust created by
impact gardening of the surface (Dollfus, 1998;
Lee, 1995; Kolesnikov and Yakovlev, 2003). Pro-
vided that the material is sufficiently unconsoli-
dated to allow microorganisms to move through-
out the grains, however, crust formation should
be possible. The light penetrability of martian and
lunar dust will influence the potential depth of
colonization of phototrophs [e.g., see Cockell and
Raven (2004) for some calculations on the mar-
tian case], but light will also penetrate through
the organisms themselves. Colonization of dark
basaltic materials by phototrophs is well docu-
mented on Earth (Carson and Brown, 1978).
Chemically, active strategies of alteration for hu-
man use may be necessary, and deficits in nutri-
ents may need compensation with amendments.
The presence of metals and other elements at
toxic levels in some materials may require the use
of resistant organisms or pre-treatment of surface
A concern regarding our proposals is planetary
protection. Despite the similarities in the physi-
cal properties of fine dusts on Mars and Chinese
deserts, and the possibilities we elaborate for
their control by microbial crusts, many of the or-
ganisms used in a surface crust have little chance
of survival or growth on the martian surface in
unshielded conditions. The temperature on the
surface of Mars is between about –123°C and
?25°C, depending on season and geographic lo-
cation. The atmospheric pressure is also low, on
average about 560 Pa, and the atmosphere con-
sists mainly of CO2. The chemical composition
and low pressure of the martian atmosphere re-
sult in a UV radiation–intense climate because
oxygen, as a trace element in the atmosphere, can-
not form UV-absorbing ozone in any useful quan-
tity. The UV radiation dose that reaches the sur-
face of Mars is far greater than that reaching the
surface of Earth and will kill terrestrial organisms
quickly (Cockell et al., 2000; Ronto et al., 2003).
In 2000, however, the Mars Global Surveyor re-
turned images that indicated signs of water seep-
ing into what appear to be young, freshly cut gul-
lies and gaps in the martian surface, which offers
some support to the theory that liquid water may
exist in the subsurface of Mars (Heldmann et al.,
2005). One hypothesis is that the gullies were
formed by streams of snowpack melt water, some
LIU ET AL.84
of which have been estimated to provide about
10 m3of liquid water per day per gully (Chris-
tensen, 2003). Thus, it may still be required that
desert crust soil alteration methods in enclosed
structures be strictly controlled, particularly near
putative “special regions” considered high-prior-
ity sites for scientific study, where growth of ter-
restrial microorganisms cannot be discounted
with certainty (MEPAG, 2006). However, on the
Moon such concerns would be irrelevant.
More ambitiously, these experiments also sug-
gest an approach to altering for human use large
areas of martian desert in future “terraforming”
schemes, in which atmospheric composition itself
is proposed to be altered. Although terraforming
is both practically and ethically controversial
(McKay and Marinova, 2001), the experiments
suggest a way to control fine regolith material
over large areas that are ubiquitously spread over
The work was supported by the Chinese Acad-
emy of Sciences (KSCX-SW-322) and The Project
of Chinese Manned Spaceflight.
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LIU ET AL. 86
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