5375_06_p450-459 11/29/04 8:56 AM Page 450

ASTROBIOLOGY
Volume 4, Number 4, 2004
© Mary Ann Liebert, Inc.

Evaporites, Water, and Life—Part 2

Hypersaline Microbial Systems of Sabkhas:

Examples of Life’s Survival in “Extreme” Conditions

WOLFGANG ELISABETH KRUMBEIN, ANNA A. GORBUSHINA,

and ELISABETH HOLTKAMP-TACKEN

ABSTRACT

Life and living systems need several important factors to establish themselves and to have a
continued tradition. In this article the nature of the borderline situation for microbial life un-
der heavy salt stress is analyzed and discussed using the example of biofilms and microbial
mats of sabkha systems of the Red Sea. Important factors ruling such environments are de-
scribed, and include the following: (1) Microbial life is better suited for survival in extremely
changing and only sporadically water-supplied environments than are larger organisms (in-
cluding humans). (2) Microbial life shows extremely poikilophilic adaptation patterns to con-
ditions that deviate significantly from conditions normal for life processes on Earth today. (3)
Microbial life adapts itself to such extremely changing and only ephemerally supportive con-
ditions by the capacity of extreme changes (a) in morphology (pleomorphy), (b) in metabolic
patterns (poikilotrophy), (c) in survival strategies (poikilophily), and (d) by trapping and en-
closing all necessary sources of energy matter in an inwardly oriented diffusive cycle. All this
is achieved without any serious attempt at escaping from the extreme and extremely chang-
ing conditions. Furthermore, these salt swamp systems are geophysiological generators of en-
ergy and material reservoirs recycled over a geological time scale. Neither energy nor mater-
ial is wasted for propagation by spore formation. This capacity is summarized as poikilophilic
and poikilotroph behavior of biofilm or microbial mat communities in salt and irradiation-
stressed environmental conditions of the sabkha or salt desert type. We use mainly cyanobac-
teria as an example, although other bacteria and even eukaryotic fungi may exhibit the same
potential of living and surviving under conditions usually not suitable for life on Earth. It
may, however, be postulated that such poikilophilic organisms are the true candidates for life
support and survival under conditions never recorded on Planet Earth. Mars and some plan-
ets of other suns may be good candidates to search for life under conditions normally not
thought to be favorable for the maintenance of life. Key Words: Biofilm—Cyanobacteria—
Hypersaline—Microbial mat—Planetary biology—Poikilophily—Poikilotrophy. Astrobiology
4, 450–459.

Geomicrobiology, Institute for Chemistry and Biology of the Marine Environment, Carl von Ossietzky Universi-
taet, Oldenburg, Germany.

450
5375_06_p450-459 11/29/04 8:56 AM Page 451
HYPERSALINE MICROBIAL SYSTEMS OF SABKHAS
INTRODUCTION
W ITHOUT EXCEPTION, every terrestrial envi-
ronment that supports life has, at least
briefly, water present in liquid form. Exobiology
search strategies for life on other planets such as
Mars must therefore be based upon the search for
environments where liquid water was (or is) pre-
sent for at least short intervals of time. Whether
water is frozen or tightly bound in evaporated
brines and salt minerals (such as halite inclusions
and hydrated gypsum) is of little consequence;
both states of water are more accessible to meta-
bolic needs than highly diluted water vapor. Fur-
thermore, water can be immobilized and kept
from evaporation by incorporation into highly
concentrated and polymeric substances such as
the extracellular polymeric substances or slimes
of biofilms (Wiggins, 1990). Thus even under con-
ditions quite far from those at the surface of the
Earth, water could be made available for metab-
olism under certain conditions. Hypersaline sys-
tems are only one of the potential candidates.
Of all the planets explored by spacecraft in the
last 4 decades, Mars is the only one with surface
conditions remotely related to those of the Earth.
Given that a major objective for the exploration
of Mars is to determine whether life ever existed
on the planet, Brack et al. (1999) assessed the po-
tential for terrestrial environments and organ-
isms to serve as models for fossil or extant life on
Mars and other planets. They concluded from a
comparison between early Earth and early Mars
that life likely established itself on both planets.
Water naturally plays an important role (Malin
and Edgett, 2000). Work on potential “Mars”-type
or martian microorganisms has centered very of-
ten on hypersaline systems (Litchfield, 1998; Lan-
dis, 2001a,b). Fossil traces of water with elevated
salinities are known from the geological record
(Anbar and Knoll, 2002). Zalar et al. (1999) have
recently studied fungi that survive extremely
high salt concentrations. Gorbushina et al. (1999)
pointed to the similarities of poikilophilic behav-
ior between cyanobacteria and certain genera of
fungi.
In this article, we stress the high level of life
adaptation, as well as the global geophysiologi-
cal potential, of hypersaline systems along the
shores of the Red Sea and Persian Gulf. Coastal
systems with high sun levels, high rates of evap-
oration, and ephemeral rainwater flooding are lo-
cated adjacent to large continental deserts. Ex-
451
amples of such deserts are the Negev, the Arava,
the Sinai Desert, the Western Desert (Sahara), and
the main deserts of the Arabian Peninsula, in-
cluding the shores of Iran. Salt swamps, pans, and
related phenomena are called sabkhas. Sabkha is
an old semitic-arabic term familiar to the Jewish
and Arabic tribes around the Red Sea since the
onset of human history. Ironically it has also been
spelled sabath. The biblical story of Moses guid-
ing the Hebrew people may exactly describe the
difficulties of passing salt swamps of the North-
ern Gulf of Suez, including the difficulties of
gaining fresh water for maintenance of life. The
meaning in the scientific annotation is best de-
scribed as places where water is only ephemer-
ally present, and usually not useful for drinking
purposes or any purpose to maintain life. Fur-
thermore, it describes places where salt infiltra-
tion makes life (and traffic) almost impossible.
Though humans regard such places as uninhab-
itable, microorganisms can thrive, and when the
water activity is insufficient for metabolic activ-
ity, they can survive in a resting stage for many
years. These microbes evolved the capacity not
only to live at the lowest possible water activity
but also to produce extracellular reservoirs of wa-
ter and means of protection from irradiation as
well as from total desiccation. Biogenic evaporate
(carbonates, gypsum) and iron minerals (mag-
netite, pyrite and others), recognized by their dis-
tinct morphologies, can protect such microbes
from cell death by environmental stress (Krum-
bein, 1986; Nealson and Conrad, 1999; Friedmann
et al., 2001; Gorbushina et al., 2001, 2002). Natu-
rally, cell death or survival in microorganisms
may have other explanations (Parkes, 2000).
In the following we focus on sabkhas of the
Gulf of Aqaba—their microbiota and adaptation
potential—as well as some global aspects of the
metabolic processes going on in these extremely
stressed, and therefore exobiologically interest-
ing, environments.
SETTING AND MORPHOLOGY
The geology and sedimentology of coastal
deserts and salt pan areas of the Red Sea and the
Persian Gulf were described by Friedman (1985)
and Purser (1973, 1985), and a review of prior sci-
entific exploration was provided by Krumbein
(1985a,b). The entire fault system of the Red Sea
and Gulf of Aqaba has been poised for burial and
5375_06_p450-459 11/29/04 8:56 AM Page 452
452
subduction since the early Tertiary, and hot
brines in the central parts of the Red Sea are al-
ready recycling some of the materials entrapped
in earlier sabkha systems.
Figure 1 shows some of the geographically im-
portant features related to major structural con-
trols of such ecosystems. Figure 2 gives a typical
example of the evaporative pumping systems
that occur along the shores of the three gulfs (the
Persian Gulf, Gulf of Aqaba, and Gulf of Suez).
Other important examples are represented by the
back barrier systems of the Pacific Islands, the
Australian Coast, and the whole area of Baja
California (Mexico). Evaporative pumping, solar
lakes (energy accumulators), and biogeochemical
transformations, however, act similarly in impor-
tant ephemeral inland water reservoirs, the most
important being the Dead Sea, the Great Salt
Lake, the Tschad, Australian inland pans, and the
huge athalasso-haline continental brine systems
FIG. 1. Satellite view of the Sinai with the adjacent graben and strike-slip fault zones depicting the coastal
sabkhas of this area.
KRUMBEIN ET AL.
of the southeastern parts of the Russian and
Asian inland deserts (Zhilina and Zavarzin, 1991;
Zavarzin et al., 1999; Zavarzin and Zhilina, 2000;
Zavarzin, 2002, 2003). In this context, hypersaline
systems can be subdivided into truly halophilic
ones located near the borders of modern oceans
and the continental inland lakes and pans. In both
types, biofilms are important for the precipitation
of minerals and organic materials (oil, gas, kero-
gen). In the marine (thalasso-haline) environ-
ments bordering oceans the major energy and
material storage is, however, organized via the
calcium cycle (Fig. 3).
In the modern continental or desert depression
salt and sun pumping systems (athalasso-haline)
where large rivers vanish in salt pans of huge di-
mensions, alkaline conditions form something
like a “Soda Continent” (Zavarzin, 2003). Krum-
bein et al. (2003b), however, suggested that these
inland systems may have been representative
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HYPERSALINE MICROBIAL SYSTEMS OF SABKHAS 453

FIG. 2. Map of the Sabkha Gavish with a transect depicting the flow of water and zones of different biofilm
communities at different salinity levels reaching from Red Sea salinity (near 6 g L
1) to total saturation with halite,
other chlorides, and sulfates. Zones 7, 8, and 9 represent the minerals and biofilms accumulating through evapora-
tive pumping. Zones 5, 6, and 7 are regions of intensive stromatolite-like microbial mats.

over considerably long geological periods in the
Proterozoic and parts of the late Paleozoic with-
out bordering deep “Soda Oceans.” An alterna-
tive scenario depicts an Earth crust with less ver-
tical deviation of geomorphology leading to large
and extended continental platforms. This would
bias biogeochemical cycles via mainly alkali ele-
ment transformations rather than earth–alkali
transformations typical for coastal margins bor-
dered by deep Ca- and Mg-regulated oceanic
basins, where high mountains lead to rapid bio-
geomorphogenesis. Under these conditions not
enough time is left for clay mineral and chert (sil-
ica) formation as represented in greenschist belts
and the Gunflint Chert. Continental hypersaline
systems may therefore be generators of clays and
cherts, and also silicified bacteria (Toporski et al.,
2002; Zavarzin, 2003). Similar though not identi-
cal conditions prevail today in parts of the Gobi
Desert and in Australia. The huge energy and ma-
terial transfer systems along modern coastal mar-
gins and their biofilm communities may serve as
accumulators for energy in the form of organic
material (petroleum, kerogen, iron sulfides) and
of huge amounts of calcium carbonates and gyp-
sum important for global tectonics and crust dy-
namics (Anderson, 1984). Colder coastal mar-
gins, in contrast, may be characterized by huge
amounts of solidified methane and iron oxide/
calcium phosphate coupling, a thought already
expressed by Gerdes and Krumbein (1987) and
Krumbein et al. (1994). Arp et al. (2001) argued
5375_06_p450-459 11/29/04 8:57 AM Page 454
454
FIG. 3. Model of a sun-powered evaporative pumping
system. Seawater moves by evaporative pumping
through coastal bars. Photons are pumped into cyanobac-
teria, creating organic matter. The latter is partially oxi-
dized using oxygen and sulfate as electron acceptors,
thereby creating large amounts of energy-rich organic
matter and metal sulfides, as well as calcium and mag-
nesium carbonates. These are stored in the burial zones;
the organics are later liberated as petroleum, gas, and
heat.
that variation in the ratio of dissolved inorganic
carbon and calcium concentrations from the Pre-
cambrian to the Phanerozoic may explain dif-
ferences in calcification in cyanobacterial mats.
Krumbein (1979) and Gerdes et al. (1985), how-
ever, argued that internal cycling of carbon and
calcium in hypersaline organic-rich sediments
initiates bacterial decay mechanisms that account
for photosynthesis-independent carbonate depo-
sition rates under aerobic and anaerobic decay
situations. In semiclosed systems highly enriched
in extracellular polymeric substances, in which
diffusivities are significantly lower than those in
water, such processes may yield large amounts
of fossil organic carbon and carbonates with very
heavy isotopic signatures (Schidlowski et al.,
1985). A broad survey of fossil and recent biofilms
in hypersaline wet and dry environments is given
by Krumbein et al. (2003a).
ORGANISMS AND SURVIVAL
Organisms capable of coping with conditions
significantly different from those considered
“normal” for life are usually called extremophiles.
However, as pointed out elegantly by Hausmann
and Kremer (1994), such a term is extremely an-
thropocentric and should not be used in a scien-
KRUMBEIN ET AL.
tific context when discussing physical and chem-
ical conditions far different from those suitable,
or even comfortable, for some eukaryotes such as
Homo sapiens sapiens. In this context a distinction
needs to be made between (1) organisms that
have narrow limits of minimal, optimal, and max-
imal demands for any of the important physical
and chemical parameters ruling survival and (2)
those organisms that have somewhat, even ex-
tremely, wide limits of survival conditions. Un-
der situation (1) we may imagine an extreme ther-
mophile just surviving at 105°C, thriving well at
110°C, but then dying at 118°C. Another example
is H. sapiens sapiens. This species contains water
with a 9 g L
1 salt content (known as physiolog-
ical salt solution), which represents about triple
the halite concentration of ocean water. This same
species requires a water supply of no more than
9 g L
1 of the same salts to replenish its liquid
water resources. Cyanobacteria in biofilms asso-
ciated with hypersaline environments, however,
are capable of changing their internal solute con-
centrations from almost pure water to nearly 350
g L
1 compatible solute concentrations by several
different and ingenious tricks. Depending on the
water supply and aqueous environment, these
microorganisms may thrive in distilled water as
well as in water containing more than 300 g L
1
salt content. Thus, extreme can mean narrow
bands of variable compounds far from human
standards, and extreme can also mean life and
survival under extremely variable, but still ac-
ceptable, conditions with ranges from 0 to 80°C
and more for temperature, 0.9 to 350 g L
1 for
solutes, and electromagnetic radiation ranging
from almost none to space-like.
Extreme conditions described by external (en-
vironmental) factors are defined by us as poik-
ilophilic and the internal (physiological) aspects
of such organisms as poikilotrophs (Gorbushina
and Krumbein, 2000a). Krumbein and Stal (1991)
described the potential of the major microbial
mat-forming microorganisms, namely cyanobac-
teria, as exceeding almost any environmental and
internal adaptation potential by adapting them-
selves to extreme changes of salt concentration,
water availability, nutrient supply, electromag-
netic radiation exposure, and other factors. These
relatively simple organisms (often called primi-
tive) are able to accomplish almost all imaginable
metabolic pathways, including oxygenic and
anoxic photosynthesis, carrying out respiration
using oxygen, sulfur, sulfate, and other relatively
5375_06_p450-459 11/29/04 8:57 AM Page 455
HYPERSALINE MICROBIAL SYSTEMS OF SABKHAS
oxidized compounds, and living anaerobically by
disproportioning sugars into alcohol or acid, like
other anaerobic fermentative microorganisms.
They can survive temperature changes from

4°C to more than 104°C. They can maintain
their metabolic capacity even after more than 100
years of total lack of water. They live in distilled
water as well as at 35% salt concentrations (wa-
ter activity practically zero). Furthermore, these
incredibly poikilotrophic and poikilophilic bacte-
ria have developed means to survive and thrive
at light intensities far below the limits of dim
moonlight in the depths of the ocean and at those
of permanent exposure to strong ultraviolet light
on the highest peaks of the Earth’s mountains.
Cyanobacteria (together with some non-photo-
synthetic bacteria like Geodermatophilus and fungi
like Coniosporium, a black yeast) are the most ver-
satile inhabitants of the Earth. These three or-
ganism types are probably better suited for space
travel and survival on other planets than humans
or even Deinococcus radiodurans, which is usually
considered to be the most radiation-tolerant or-
ganism known (Makarova et al., 2001). D. radio-
durans, an organism about which it is presently
speculated that its peculiar genetic characteristics
can only be explained by evolutionary adaptation
through several space trips from Mars to Earth,
and vice versa, in addition has some special genes
in common with early cyanobacteria. Within the
framework of this article, it is impossible to sketch
the entire natural history of cyanobacteria. Here
it suffices to say that these highly poikilophilic
microorganisms have been, and still are, deeply
involved in the parahistology, geophysiology,
and biogeochemistry of the Earth’s crust. The
new theory of a ring of life circulating and ex-
changing information between Archaea and Eu-
bacteria also hints to the potential of the first
stages of evolution of mixed gene sets and eu-
karyotic micromycetes taking place (at least in
part) under space conditions (Rivera and Lake,
2004). These poikilophilic types of microbes
thrive and survive under radically changing con-
ditions, thereby contributing to the storage of ma-
terial and information into the deeper layers of
the crust for future buffering of living conditions
on this planet. They are so versatile and stress re-
sistant that the idea of higher rates of exchange
of material (and organisms) within the inner
planetary ring of the Solar System throughout the
Archean sounds very reasonable also in terms of
the evolution of special stress response mecha-
455
nisms. Figures 4–10 give an impression of the
high variability of morphology and physiology of
this peculiar and ancient organism group. The
cyanobacteria depicted in the photomicrographs
in Figs. 4–10 could be labeled as at least three dif-
ferent genera and four different species. The cells,
however, are all derived from a single cultured
clone reacting to environmental challenges by ex-
pressing different genes and producing more or
less of many different proteins. These bacteria are
at least as astonishing as the higher eukaryotes
(the chimpanzee and H. sapiens sapiens), which
also seem to differ only in the type and amount
of different proteins produced from one and the
same set of genetic information under different
internal and external conditioning circumstances.
GLOBAL PHYSIOLOGY OR
GEOPHYSIOLOGY AND
PARAHISTOLOGY OF HYPERSALINE
BIOSPHERE REGULATOR SYSTEMS
Subaquatic biofilms are sometimes character-
ized as 99% (wt/vol) biologically solidified wa-
ter. This is achieved through large amounts of ex-
tracellular polymeric organic substances excreted
by the biofilm community for many purposes. A
major part of metabolic activity is transformed
into these slimes. They are so stable and charac-
teristic that they even change the petrography of
sedimentary rocks. Sand grains float and move
upwards within these mats instead of falling from
suspension to the bottom and create grain-to-
grain contacts. In contrast, subaerial biofilms and
rock-inhabiting networks (biodyction) are usu-
ally characterized by 99% (wt/vol) living organic
matter surviving with a minimum of supply of
water (Gorbushina and Krumbein, 2000b). These
layers of microorganisms cover nearly all sur-
faces on Earth, including the hair of the polar bear
and human skin.
Wachendörfer (1991) was the first to suggest
an interesting terminology by analogy to plant
or animal tissue studies. He introduced the term
of parahistology for the study of these incred-
ibly poikilophilic communities (Krumbein, 1994;
Wachendörfer et al., 1994). Geophysiology and
parahistology describe Earth’s global biofilm sys-
tem, which runs the major biogeochemical cycles
(Krumbein, 1983; Krumbein and Dyer, 1985;
Krumbein and Schellnhuber, 1992; Krumbein and
Lapo, 1996). In brief, the living skin of the planet
5375_06_p450-459 11/29/04 8:57 AM Page 456

456 KRUMBEIN ET AL.

FIG. 5. Individual cell clusters of strain 112 at 1.5 M

NaCl. Scale bar  10
m.

ferent approaches, have postulated that these

FIG. 4. Ensheathed (and thus protected) cells of strain
112 from the Gavish sabkha at 1 M NaCl. Scale bar  10

m.
parahistologically defined mega- or metatissues
regulate even plate tectonics and the cycling of
nutritive elements through the crust (from down-
under to up into the active metabolic cycles).
Krumbein (1996) reviewed some of the historic
aspects mentioned above in an article on non-
Darwinian aspects of the establishment and
maintenance of microbial life on Earth.

Earth is highly productive, highly versatile, and CONCLUSIONS

highly poikilotrophic and poikilophilic, and it
acts like the tissue of any organism (superorgan- What can be concluded from this sketch of hy-
ism). The tissue-like system––and preferentially persaline sabkha-type biogeochemical activities?
the hypersaline tissue––transforms and accumu- Assuming that the data collected in handbooks of
lates huge amounts of energy (heat) and reduced
and oxidized compounds over geological periods
of time. The sum of both (i.e., solar energy stored
in organic matter and kerogen as well as in metal
sulfides) reaches annually the same order of mag-
nitude of the annual heat flow as that from the
crust to the surface layers of Earth (Krumbein and
Schellnhuber, 1992).
The terms geophysiology, parahistology, and
global biogeochemistry seem to be very appro-
priate in these cases. Intertidal coastal margin and
continental hypersaline microbial biofilms, as
well as subaerial biofilms often associated with
the latter, reach geological dimensions in their
metabolic activity, and store gigagrams of organic
carbon and biogenic minerals in deeper layers of
the crust. Krumbein and Schellnhuber (1992) and FIG. 6. Elongated, nearly filamentous, cells of strain
the geophysicist Anderson (1984), using two dif- 112 at 2.5 M NaCl. Scale bar  10
m.
5375_06_p450-459 11/29/04 8:57 AM Page 457

HYPERSALINE MICROBIAL SYSTEMS OF SABKHAS 457

FIG. 9. Transmission electron photomicrograph of

FIG. 7. Strain 112 at 3 M NaCl. Scale bar  10
m. strain 112 at 3.2 M NaCl showing adaptation patterns in
new and mature cells. Original magnification 5,100.

physics and chemistry and geochemistry are cor-

rect, one must come to the following conclusions,
especially for the highly productive hypersaline and hydrogen at global levels and masses and
biofilm systems: geological time scales.
3. The products of these geophysiological cycles
1. Solar energy is caught in flight and trans- of the parahistological system, such as volatile
formed into useful chemical potential (or en- (methane) and refractory (kerogen) organic
ergy) in annual amounts exceeding geother- carbon compounds, carbonates, sulfides, and
mal heat flow. This energy is stored in even cherts, generate new potential for meta-
sedimentary rocks and liberated only after ge- bolic processes upon liberation at the surface
ological-scale time periods. Most of this en- of the Earth.
ergy storage is carried on in hypersaline,
highly fluctuating, systems where the chances
of long-term storage are highest.
2. The elements and materials involved embrace
alkali elements (continental soda lake and
playa systems) and alkali earth elements
(oceanic brine and evaporative systems), along
with carbon, oxygen, sulfur, iron, phosphorus,

FIG. 10. Cells of strain 112, 3 days after transfer from

1 M NaCl to 3 M NaCl. One of the visible effects illus-
trated in Figs. 4–10 is the high degree of pleomorphy de-
rived, in part, from individual production of compatible
solutes. Solute production may damage the membrane
and lead to distorted planes of division and accelerated
and/or highly reduced replication rates. The oval “nor-
FIG. 8. Strain 112 at 3.2 M NaCl. Scale bar  10
m. mal” cells measure 3  6
m.
5375_06_p450-459 11/29/04 8:57 AM Page 458
458
4. The processes of capture, entrapment, burial,
and feedback into living parahistological
biofilm tissue are regulated through plate tec-
tonics, global climate, and oceanic currents.
5. The latter seem to be under the control of geo-
physiology or global biogeochemical and bio-
geomorphogenetic processes inherent to liv-
ing systems covering Earth like a tissue, thus
justifying the term parahistology.
ACKNOWLEDGMENTS
We acknowledge support by INTAS grant 97-
30776 and by DFG Schwerpunkt Programme
“Mars and the Terrestrial Planets” via grant DFG
Go 897/2-1 and DFG grant Kr 333/30-1. Late
stages of the work on biofilm formation were sup-
ported by EU project BIODAM (EVK4-CT-2002-
00098). Mario Latoschinski was helpful in prepar-
ing some of the graphs.
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Address reprint requests to:
Dr. Wolfgang Elisabeth Krumbein
Geomicrobiology
Institute for Chemistry and Biology
of the Marine Environment
Carl von Ossietzky Universitaet
P.O. Box 2503
D-26111 Oldenburg, Germany
E-mail: wek@uni-oldenburg.de