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Microalgae and cyanobacteria of the Dead Sea and its surrounding springs

Article in Israel Journal of Plant Sciences · December 2008

DOI: 10.1560/IJPS.56.1-2.1

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 Israel Journal of Plant Sciences Vol. 56 2008 pp. 1–13
10.1560/IJPS.56.1–2.1

Microalgae and cyanobacteria of the Dead Sea and its surrounding springs

Aharon Oren,a,* Danny Ionescu,a,b Muna Hindiyeh,c and Hanan Malkawid

The Institute of Life Sciences, and the Moshe Shilo Minerva Center for Marine Biogeochemistry,
a

The Hebrew University of Jerusalem, Jerusalem 91904, Israel

b
The School for Marine Sciences, The Ruppin Academic Center, Emek-Hefer 40250, Israel
c
Department of Environmental Science, Jordan University of Science and Technology, Irbid 22110-3030, Jordan
d
Department of Biological Sciences, Yarmouk University, Irbid 21163, Jordan

(Received 19 December 2007; accepted in revised form 24 February 2008)

Abstract
Scientific exploration of the algal and cyanobacterial flora of the Dead Sea and its
surroundings started in the 1930s. The unicellular green alga Dunaliella parva is the
sole primary producer in the water column of the Dead Sea. The dynamics of the
Dunaliella population and the interrelationships between the alga and the physical
and chemical parameters in the lake are now well understood. Although cyanobacte-
ria have occasionally been encountered in the Dead Sea as well, they are not known
to contribute significantly to the microbial activities in the lake. Dense growth of
cyanobacteria is found in various freshwater and saline, cold and warm springs in
the Dead Sea area. Abundant cyanobacterial communities develop in the hot (up
to 63 ºC) freshwater springs of Zerka Ma’in and Zara near the eastern shore of the
lake. We here report data on the diversity of these communities, based both on mi-
croscopic observations and on molecular phylogeny techniques, and on their content
of UV-absorbing pigments (mycosporine-like amino acids, scytonemin), which is of
interest in view of the lowered levels of UV light reaching the Dead Sea shores.
Keywords: Dunaliella, cyanobacteria, Dead Sea, Israel, Jordan, hot springs

Where Sodom and Gomorrah reared their domes and towers, that solemn sea now floods the plain, in whose
bitter waters no living thing exists—over whose waveless surface the blistering air hangs motionless and
dead—about whose borders nothing grows but weeds ….
(Mark Twain, The Innocents Abroad or The New Pilgrims Progress, 1869)
A barren land, bare waste. Vulcanic lake, the dead sea: no fish, weedless, sunk deep in the earth.
(James Joyce, Ulysses, 1922)

Introduction
The two quotations above give a depressing picture of
the plant life in the Dead Sea and its surroundings, the
lake itself being “weedless” with nothing but “weeds”
around its borders. However, examination of the world
of microalgae and cyanobacteria inhabiting the lake and
its surrounding area shows many interesting aspects that
deserve in-depth study.
The year 1936 was an important landmark in the ex-
ploration of the Dead Sea area for the presence of algal
and cyanobacterial life. In that year, Benjamin Elazari-
Volcani (Wilkansky) (1915–1999), then a Ph.D. student
at the Hebrew University of Jerusalem, published a
short paper entitled “Life in the Dead Sea”, in which he
first mentioned the occurrence of Dunaliella in the wa-
ter column of the lake. In samples collected 3-4 km from
*Author to whom correspondence should be addressed.
E-mail: orena@cc.huji.ac.il

© 2008 Science From Israel / LPPltd., Jerusalem



the mouth of the Jordan River, “microscopic examina-
tion of a hanging drop of the water revealed the presence
of a living phytoflagellate, 13µ long, believed to be
either a Chlamydomonas or a Dunaliella” (Wilkansky,
1936) (Fig. 1, upper panels). In the spring of the same
year, Tcharna Rayss (1890–1965), a professor of botany
at the Hebrew University, joined by the famous French
phycologist Abbé Pierre Frémy (1880–1944) and a
group of students from Jerusalem, made a sampling trip
to the warm springs of Zara—the ancient Kallirrhoe. A

Fig. 1. Benjamin Elazari-Volcani as a student (1938), and a drawing of a Dunaliella cell from the Dead Sea, derived from his
Ph.D. thesis (Elazari-Volcani, 1940a) (upper panels), and a portrait of Tscharna Rayss and her drawings of different types of
filamentous cyanobacteria found in the springs of Ein Zara, the ancient Kallirrhoe (Frémy and Rayss, 1938) (lower panels).

Israel Journal of Plant Sciences 56 2008


detailed report on the cyanobacterial communities found
during the survey of the springs was published in 1938 in
Volume 1, issue 1 of the Palestine Journal of Botany—Je-
rusalem Series, now the Israel Journal of Plant Sciences
(Frémy and Rayss, 1938) (Fig. 1, lower panels).
We here present a short review of the earlier pub-
lished work on the algal and cyanobacterial communi-
ties of the Dead Sea and its surrounding springs, and
include novel information from our recent surveys in
the area to provide an updated overview of our current
understanding of the microalgal and cyanobacterial di-
versity in and around the Dead Sea.
Dynamics of Dunaliella and other
phototrophic microorganisms in the
Dead Sea water column
The unicellular green alga Dunaliella is a common
inhabitant of the Dead Sea. Since it was first reported
there by Volcani in the 1930s (Elazari-Volcani, 1940b;
Volcani, 1944; Wilkansky, 1936), its presence was con-
firmed in the early 1960s (Kaplan and Friedmann, 1970)
and during blooms in 1980–1982 (Oren and Shilo, 1982)
and 1992-1993 (Oren et al., 1995). Volcani identified the
species as Dunaliella viridis. Nevo and Wasser (2000)
named it Dunaliella parva Lerche, stating Dunaliella
viridis Teod. sensu Butcher 1959 as synonym.
The first attempts to count Dunaliella cells in the
Dead Sea water column were made in 1964. Very high
population densities of up to 40,000 cells/ml were en-
countered in surface waters (sampling date not stated).
At 50 m depth, algal numbers were lower by two orders
of magnitude, and no Dunaliella cells were detected
in a sample collected from 100 m depth (Kaplan and
Friedmann, 1970). A systematic monitoring program
to follow the population densities of Dunaliella in the
lake was initiated in 1980, and from that year onwards
we have a good understanding of the occurrence of the
alga in the lake (Oren and Shilo, 1982; Oren et al., 1995,
2005; Oren and Ben-Yosef, 1997; Oren, 2000). During
the period of study, massive algal blooms developed
twice in the surface waters of the Dead Sea: in 1980 (up
to 8,800 cells/ml) and in 1992 (up to 15,000 cells/ml and
possibly even higher). These two bloom events occurred
following exceptionally rainy winters in which unusu-
ally large amounts of fresh water caused a dilution of the
upper 5–10 m of the water column, initiating meromic-
tic conditions in the lake (1980–1982 and 1992–1995).
In both cases the algae were found all over the lake,
with little spatial heterogeneity during the height of the
blooms. No algae were observed the water column dur-
ing the monomictic periods (1983–1991 and from 1996
until 2007), when this manuscript was finalized.

The field observations can be understood on the basis
of laboratory and outdoor mesocosm simulations that
have shown that for a Dunaliella bloom to develop in
the lake two factors must be fulfilled: (1) A significant
(10% at least) dilution of the upper water layers is a
prerequisite for an algal bloom in the lake, as undiluted
Dead Sea water is too saline to support growth of Du-
naliella. (2) Phosphate, which is the limiting nutrient,
must be available (Oren and Shilo, 1985; Oren et al.,
2004, 2005). Such simulation experiments are highly
relevant in view of the planning of a Red Sea—Dead
Sea water carrier (Oren et al., 2004). During the pro-
longed periods in which no algae can be observed in the
water column, Dunaliella probably survives in the sedi-
ments as thick-walled resting stages (zygotes), which
were actually observed to be formed during the decline
of the 1992 bloom (Oren et al., 1995). This theory is
consistent with the observation that the 1992 bloom
started in the shallow areas all around the lake where
the resting cells became exposed to the lowered salinity
and spread afterwards over the entire lake surface (Oren
and Ben-Yosef, 1997).
Dunaliella is the only phototroph shown to grow
and be active in the hypersaline waters of the Dead Sea.
There are a number of reports of sightings of other algae
and of cyanobacteria in the lake (Vinogradova et al.,
1996b; Dor, 1998; Nevo and Wasser, 2000), but most of
the species mentioned are not known to be halophilic or
highly halotolerant. To what extent they had developed
in the Dead Sea should therefore be doubted. Bernard
(1957) reported abundance of the coccolithophorid ma-
rine alga Coccolithus and the marine dinoflagellate Exu-
viella in Dead Sea water collected at the western shore,
with densities up to 788 and 5,510 cells/ml, respectively.
The true source of these algae can no longer be ascer-
tained. Elazari-Volcani (1940b) published a short paper
on “algae in the bed of the Dead Sea”, based on exami-
nation of a sediment sample allegedly collected from a
depth of 350 m (a value in error, being 15 m more than
the maximum depth of the lake at the time) from a sta-
tion 8 km west of the east coast and “23 km west-south-
west of the mouth of the Jordan” (apparently another
error, as such a station would be located 10 km inland
and 23 km from the eastern shore). In this and other
Dead Sea sediment samples, Volcani found many algal
species, including members of the Chlorophyceae (spe-
cies of Scenedesmus, Pediastrum, Ulothrix); pennate
and centric diatoms (genera Melosira, Navicula, Gom-
phonema, Cymbella, Pinnularia, Eunotia, Synedra);
and unicellular and filamentous cyanobacteria (genera
Aphanocapsa, Aphanothece, Oscillatoria, Phormidium,
Plectonema) (Elazari-Volcani, 1940a,b). Volcani suc-
ceeded in culturing several cyanobacteria from these
Oren et al. / Microalgae and cyanobacteria of the Dead Sea

samples: Aphanocapsa, Microcystis (?), Phormidium
(in 18% salt medium), and Nostoc sp. (in 0–12% salt).
A 0.5% salt medium yielded Chlorella sp., and two cul-
tures with 12 and 15% salt yielded an unidentified small
green flagellate (2–3 ´ 4–6 µm) with a single flagellum.
The organism could grow over the whole range of salt
concentrations between 1 and 27% (Elazari-Volcani,
1940a,b; Volcani, 1944).
The finding of unicellular cyanobacteria such as
Aphanothece and Aphanocapsa in the older Dead Sea
studies is of special interest. They have also been found
in hypersaline environments near the Dead Sea: the
Hamei Mazor warm hypersaline sulfur springs (now
largely dried up) on the western shore of the lake (Oren,
1989) and experimental solar ponds (no longer opera-
tive) at the northern end of the lake near Bet Ha’Arava
(Dor and Ehrlich, 1987). The too-high salinity and the
special ionic composition of Dead Sea water prevents
their active growth in the Dead Sea, but dense masses
of Cyanothece/Aphanothece-like cells embedded in
polysaccharide slime were observed to develop in ex-
perimental mesocosms in which Dead Sea water was
mixed with an equal volume of water from the Red Sea
(Oren et al., 2005).
Algae and cyanobacteria in warm and
cold springs around the Dead Sea
The surroundings of the Dead Sea are of special interest
as a habitat for cyanobacteria and eukaryotic microal-
gae. The area is hot and arid, and therefore develop-
ment of cyanobacterial desert crusts can be expected.
Moreover, there is a great variety of springs with highly
diverse chemical and physical properties: from cold to
hot, and from freshwater to hypersaline, some having a
high content of sulfide as well.
As a result the area has attracted the attention of
algal taxonomists who have performed surveys and pre-
pared inventories of species found at the different sites.
Information about the cyanobacterial species detected
around the Dead Sea is especially abundant thanks to
extensive studies by a number of experts over the past
70 years (Frémy and Rayss, 1938; Rayss, 1944; Dor and
Ehrlich, 1987; Dor and Danin, 1996; Vinogradova et
al., 1996a,b; Dor, 1998; Nevo and Wasser, 2000;). The
monumental study by Ehrlich (1995) provides an excel-
lent survey of the distribution of diatoms in the springs
and other sites on the Israeli side of the Dead Sea shore.
She listed at least 45 genera with at least 149 species of
Bacillariophyta sighted in the area. A further discussion
of the diatom communities in the Dead Sea springs is
outside the scope of the present article, which will fur-
ther center on cyanobacterial diversity. The very small
Israel Journal of Plant Sciences 56 2008
numbers of species listed by Nevo and Wasser (2000)
suggest that no extensive surveys for Chlorophyta and
other classes of algae appear to have been made in the
Dead Sea area.
Based on the literature sources cited above, we
can compile a long list of genera of cyanobacteria
found around the Dead Sea. Species of Entophysalis,
Schizothrix, Microcoleus, and Nostoc have been re-
ported from the terrestrial areas. The freshwater springs
and brackish water pools of Ein Fesha (Enot Zuqim)
yielded no less than 29 species belonging to the genera
Merismopedia, Chroococcus, Gloeocapsa, Gloeothece,
Gomphosphaeria, Johannesbaptista, Oscillatoria,
Schizothrix, Phormidium, and Nodularia. From the Ein
Gedi area, Scytonema and Homoeothrix species were
reported. Two species of Phormidium were identified in
the Ein Boqeq spring, and the warm springs of Hamei
Zohar contained species of Gloeothece, Merismopedia,
Chroococcus, Oscillatoria, Spirulina, Phormidium,
Cylindrospermum, Scytonema, and Mastigocladus.
Another rich source of cyanobacterial diversity was the
area of the experimental solar ponds for the generation
of electricity established at Bet Ha’Arava in the 1980s.
These shallow ponds contained a bottom layer of Dead
Sea water and an upper layer of brackish water, caus-
ing heliothermal heating of the lower water layers. At
the time, rich communities of cyanobacteria developed
along the salinity and temperature gradients in the ponds
and in their vicinity, and these included species of Apha-
nothece, Aphanocapsa, Gomphosphaeria, Gloeocapsa,
Chroococcus, Chlorogloea, Chroococcidiopsis, Phor-
midium, Spirulina, and Oscillatoria (Dor and Ehrlich,
1987 and other sources cited above). The operation of
the system has since been discontinued.
Beyond the taxonomic characterization of species
there have been few ecophysiological studies on the
cyanobacterial communities in the springs at the western
side of the Dead Sea. In the 1980s, when there still were
warm (39 ºC), hypersaline (around 170 g/l total dis-
solved salts) sulfur springs exposed near the shore south
of En Gedi (Hamei Mazor), dominated by dense benthic
growth of Oscillatoria or Phormidium-type filaments, it
was established that these cyanobacteria were capable
of anoxygenic photosynthesis with sulfide as electron
donor, driven by photosystem I, with the production of
elemental sulfur, this in addition to oxygenic photosyn-
thesis with water as electron donor, driven jointly by
photosystems II and I (Oren, 1989). This cyanobacterial
community contained a high concentration of glycine be-
taine that served as the cells’ osmotic solute to withstand
the high salinity of the environment (Oren et al., 1994).
The exposed sulfur springs have since dried out, and the
characteristic cyanobacterial growth has disappeared.

The eastern shore of the Dead Sea presents us with
two extremely interesting environments for the study of
cyanobacteria: the freshwater thermal springs of Zara
near the lake’s shore and the even warmer (up to 63 ºC)
springs in Wadi Zerka Ma’in, 4–5 km inland (Fig. 2).
The cyanobacterial communities of these Jordanian hot
spring areas have been the subject of our recent stud-
ies.
Fig. 2. The location of the springs of Ein Gedi, Ein Feshcha, Zara, and Zerka Ma’in and phase-contrast micrographs of repre-
sentative cyanobacteria collected from the sites.

The cyanobacterial communities of the thermal
springs of Zara and Zerka Ma’in
As mentioned at the beginning of this paper, the Zara
hot springs (the ancient Kallirrhoe) (Donner, 1963) had
been sampled and examined for algal life in 1936. The
temperature of the water at the sampling sites varied
between 35 and 40 ºC. Seventeen species of cyanobac-
Oren et al. / Microalgae and cyanobacteria of the Dead Sea

teria were identified, belonging to the unicellular genera
Aphanocapsa, Merismopedia, Chroococcus, and Gloeo-
thece and the filamentous genera Phormidium, Oscil-
latoria, Spirulina, Cylindrospermum, Hapalosiphon,
and Scytonema (Frémy and Rayss, 1938; Fig. 1). A list
published later by Rayss (1944) also mentions Aulosira
thermalis. A few diatoms were present as well, but no
attempt was made to further identify them.
The presence of green-colored cyanobacterial mats
in the freshwater hot springs in Wadi Zerka Ma’in was
already mentioned by the first explorer who reached
the area, Ulrich Jasper Seetzen, who visited the site in
1807. He noted that “In dem Wasser wuchs eine grüne
schleimige Conferve” [In the water grew a green slimy
microscopic alga] (Seetzen, 1854). More observations
of the biological phenomena in the hot spring water
were made by the German geologist Max Blancken-
horn, who surveyed the area in 1908. Blanckenhorn
noted that where the water was particularly hot, blue-
green Cyanophyceae dominated. He found the bottom
of the stream and the submerged rocks covered by green
algal mats. Not being a specialist on algae, he rightly
commented that “an algologist can find here, as well as
in the other hot sulfur springs of Palestine, a wonderful
area for observations and collection” (Blanckenhorn,
1912; translation A.O.).
Our joint Jordanian–Israeli studies of the cyanobac-
terial communities of the Zerka Ma’in springs were ini-
tiated in 2005 by the Bridging the Rift Foundation, and
the first results have recently been published (Ionescu
et al., 2007, submitted). Conspicuous types include
unicellular Thermosynechococcus and Gloeocapsa, and
Spirulina-like filaments. Spirulina labyrinthiformis was
earlier reported as the dominant organism in material
collected by A. Aaronson from a 52 ºC spring of the
Zerka Ma’in (Rayss, 1944; Vinogradova et al., 1996b).
Several representative types of Thermosynechococcus,
Gloeocapsa, and Mastigocladus/Fischerella have been
isolated and cultured. Amplification of cyanobacterial
16S rRNA genes from DNA extracted from the mats
showed a high diversity of Thermosynechococcus
(Ionescu et al., submitted). Low concentrations of am-
monium and nitrate in the water and the presence of
heterocystous cyanobacteria indicated that biological
nitrogen fixation may be important in the spring ecosys-
tem. Genes related to nifH of Fischerella, Phormidium,
and Lyngbya spp. were amplified from the community
DNA. Laboratory experiments with heterocystous iso-
lates showed occurrence of nitrogen fixation (acetylene
reduction) at 52 ºC but not at 63 ºC. However, reverse
transcription PCR with mRNA isolated from a 63 ºC
site amplified a gene identical to a nifH gene found in
a filamentous cyanobacterial culture obtained from the
Israel Journal of Plant Sciences 56 2008
site. Moreover, low but significant rates of acetylene
reduction were measured during in situ incubations
up to the highest temperatures in the springs. It is thus
suggested that nitrogen fixation may occur in the cya-
nobacterial community of the Zerka Ma’in hot springs
at temperatures significantly higher than the thus far
recognized upper temperature boundary for filamentous
cyanobacterial nitrogen fixation of about 55 ºC (Ionescu
et al., submitted).
Microscopical and molecular characterization of the
cyanobacterial communities of the thermal springs
of Zerka Ma’in and Zara
We have extended our evaluation of the morphological
and molecular diversity of the Zerka Ma’in hot spring
cyanobacteria. The spring sites around the Dead Sea
explored during our surveys yielded a wide variety of
morphological types, unicellular as well as filamentous.
Figure 2 shows the most abundant types.
Tightly wound Spirulina filaments were particularly
abundant at the Zara site in outflow channels with wa-
ter up to 44 ºC. At the hottest sites of the Zerka Ma’in
springs, unicellular Thermosynechococcus-type cya-
nobacteria dominated. As the water cools down down-
stream towards the outflow channels, additional types
of cyanobacteria start to appear, as pictured in Fig. 2.
Cultures of Gloeocapsa and Mastigocladus/Fischerella
were obtained from samples collected at diffent places
in the Zerka Ma’in area. Near some of the outflow chan-
nels of the hot springs of the Zerka Ma’in, large colonies
of the branching heterocystous cyanobacterium Scyto-
nema were found (Fig. 2, lower panels). These colonies
consist of dark-green to black material growing on the
rocks, not in direct contact with the warm waters, but
continuously sprayed by small droplets of water from
the stream. Occurrence of Scytonema sp. was earlier
reported from the Zara hot springs area (Frémy and
Rayss, 1938).
16S rRNA gene sequences obtained from the envi-
ronmental samples and from the cultures derived from
them were aligned and plotted as a tree (Fig. 3). We
have amplified 46 distinct sequences related to Ther-
mosynechococcus/Synechococcus from Zerka Ma’in
(Fig. 3A). Unfortunately, no cultures of this type were
yet recovered from the springs. Filamentous non-het-
erocystous cyanobacteria are represented in the tree
(Fig. 3B) by 5 cultured strains and 17 environmental
clones. In addition, we have isolated two cultures of
heterocystous cyanobacteria affiliated with the gen-
era Fischerella and Mastigocladus from the springs
(Fig. 3C). No related sequences were yet detected
among the environmental 16S rRNA gene fragments
cloned from the DNA isolated from the site. None of the
 Fig. 3A.

Fig. 3. Phylogenetic tree of 16S rRNA gene sequences of unicellular types of cyanobacteria (A), non-heterocystous filamentous cyanobacteria (B), and heterocystous types of cyanobacte-
ria (C) from cultures and environmental samples obtained from the Zerka Ma’in hot springs. Samples were collected between December 2005 and June 2007 and stored refrigerated until
processed within 40 h. For DNA extraction, samples were incubated for 30 min at 100 ºC in lysis buffer (100 mM Tris-HCl, 50 mM EDTA, 10 mM NaCl, 1% SDS, pH 8), followed by
extraction with phenol–chloroform–isoamyl alcohol (25:24:1). The extracts were washed with chloroform–isoamyl alcohol (24:1). DNA was precipitated with 1 volume of isopropanol and
0.01 volume of 3 M Na acetate, pH 5.5, washed with ice-cold 70% ethanol, and resuspended in nuclease-free water. Fragments of the 16S rRNA gene were amplified by PCR, using cyano-
bacteria-specific primers 106f and 781R (Nübel et al., 1997). For environmental samples a GC-clamp modified 781R primer was used. Amplicons were separated by denaturating gradient
gel electrophoresis and cloned using the InsTAclone kit (K1214, Fermentas). The 16S rRNA gene sequences obtained from isolates (marked rBTRCCn followed by a serial number) and
environmental samples (marked Clone followed by letters and numbers), all indicated in boldface type in the trees) (Accesion numbers DQ471441-9; and EU326950-437026 respectively)
were aligned with 1760 additional cyanobacterial sequences from the Greengenes database (http://greengenes.lbl.gov; DeSantis et al., 2006) using the ClustalW algorithm, and plotted as a


Oren et al. / Microalgae and cyanobacteria of the Dead Sea

Minimal Evolution tree using the MEGA 4.0 software (Tamura et al., 2007).
 
Fig. 3B.

Israel Journal of Plant Sciences 56 2008

 

Fig. 3C.

Oren et al. / Microalgae and cyanobacteria of the Dead Sea

10
70 sequences was identical to any of the other cyanobac-
terial rRNA gene sequences found in the GenBank.
Survey of UV-absorbing substances
in cyanobacterial communities in
springs around the Dead Sea
The amount of ultraviolet solar radiation that reaches
the surface of the earth is a function of the optical path
length of the light. It is attenuated by atmospheric scat-
tering by air molecules, water vapor, and aerosols, as
well as by absorption by ozone, water, and carbon di-
oxide. The Dead Sea, being the lowest terrestrial place
on earth, its current surface level being at 420 m below
sea level, is therefore the place with the longest atmo-
spheric optical path length. The amount of UV radiation
penetrating to the area is therefore reduced. The levels
of UV-B radiation at wavelengths above 310 nm at
the Dead Sea (measured at 375 m below sea level) are
about 12% lower than at an elevation of 315 m above
sea level in a nearby area, and UV light of wavelengths
shorter than 300 nm is much more efficiently attenuated
(Kudish et al., 1997, 2003). The selective decrease in
short-wavelength UV is considered one of the reasons
Fig. 4. Absorption spectra of pigment extracts of cyanobacterial material collected from the Zerka Ma’in thermal springs area.
(A): a sample collected on November 16, 2006 from an outflow channel, GPS coordinates 8092506-4165670, water temperature
52 ºC), extracted in methanol–acetone 1:1 (v/v); (B): the same sample extracted in 20% methanol; (C): material from a nearby
colony of Scytonema, extracted in acetone.
Israel Journal of Plant Sciences 56 2008
for the success of the treatment of psoriasis and other
skin diseases in health spas around the Dead Sea.
Organisms exposed to full sunlight have to protect
themselves against the harmful action of UV radiation.
One strategy used by cyanobacteria is the accumulation
of “sunscreen compounds” that absorb the harmful radi-
ation. Two classes of such compounds have been identi-
fied: the mycosporine-like amino acids and scytonemin.
Mycosporines and mycosporine-like amino acids
(MAAs) are small (generally <400 Da) water-soluble
molecules with maximum absorbance between 310
and 365 nm. They are accumulated by a wide range of
microorganisms, prokaryotic (cyanobacteria) as well as
eukaryotic (microalgae, yeasts and fungi). MAAs are
composed of either an aminocyclohexenone or an ami-
nocyclohexeneimine ring, carrying nitrogen or imino
alcohol substituents (Bandaranayake, 1998; Sinha et al.,
1998; Schick and Dunlap, 2002). Their biosynthesis is
probably based on the shikimate pathway for the synthe-
sis of aromatic amino acids. Thus far, the chemical struc-
tures of over 30 different MAAs have been elucidated.
In recent years evidence has accumulated that MAAs
have additional functions: they may serve as antioxidant
molecules scavenging toxic oxygen radicals, they can be

accumulated as compatible solutes following salt stress,
their formation is induced by desiccation or by thermal
stress in certain organisms, they have been suggested
to function as an accessory light-harvesting pigment in
photosynthesis or as an intracellular nitrogen reservoir,
and they are involved in fungal reproduction. Thus, they
may be considered as multipurpose secondary metabo-
lites (Oren and Gunde-Cimerman, 2007). MAAs are
found in a variety of cyanobacteria, unicellular as well
as filamentous (Castenholz and Garcia-Pichel, 2000;
Garcia-Pichel and Castenholz, 1993). They sometimes
occur in high concentrations inside the cells: MAAs
can accumulate to up to 0.8% of the cell dry weight in a
Gloeocapsa (Garcia-Pichel and Castenholz, 1993), and
in hypersaline environments even higher values have
been reported in the literature (Oren, 1997).
We have tested the presence of MAAs in material
from the cyanobacterial communities collected on No-
vember 16–17, 2006 and on June 3, 2007 from the hot
springs of Zerka Ma’in (elevation approximately 250 m
below sea level) and Zara (400 m below sea level), and
the cold springs of Ein Fesha and the outflow channel
of the warm hypersaline sulfur springs of Ein Gedi
(400 m below sea level). The types of cyanobacteria
encountered at the different sites are illustrated in Fig. 2.
Samples were extracted overnight at 4 ºC in the dark
with methanol–acetone 1:1 (v/v) (to extract UV-absorb-
ing pigments as well as chlorophyll a, carotenoids,
and scytonemin) or with 20% methanol to selectively
extract MAAs without releasing the other pigments.
Extracts were cleared by centrifugation, and their ab-
sorption spectra were recorded against the respective
solvents in a Hewlett-Packard model 8452A diode array
spectrophotometer. MAAs were absent or nearly absent
from all samples collected at the highest temperatures
(59–63 ºC). In most samples collected at 52 ºC and be-
low, an absorption peak was found at 334 nm, which can
be attributed to MAAs (Fig. 4A,B). This peak was in-
variably very small in comparison to the absorbance in
the visible range of the spectrum due to cyanobacterial
chlorophyll a and carotenoid pigments. Whether one or
more types of MAAs were present in the samples, and
whether all samples contained the same MAA or MAAs,
could not be ascertained by the methods used. We did
not find signs of the presence of MAA compounds that
absorb at longer wavelengths such as palythene (maxi-
mum absorbance at 360 nm) and related compounds.
The summer samples did not contain higher MAA levels
than those collected in the winter season. MAAs thus do
not contribute much to the protection of the cells against
UV radiation. The highest MAA concentrations, still
very low compared to MAA-containing cyanobacte-
rial communities found elsewhere, were encountered in
11
the benthic community of the outlet of the hypersaline
springs of Ein Gedi in November 2006, the MAA ab-
sorbance at 334 nm being about half the absorbance of
chlorophyll a at 665 nm. In June 2007 this site had dried
up, so no sample was collected then.
To test whether exposure to full sunlight at a higher
elevation may induce the formation of MAAs, samples
immersed in water from the respective sampling sites
were incubated in open Petri dishes on the roof of the
Institute of Life Sciences, the Hebrew University of
Jerusalem (elevation about 780 m above sea level) for
10 hours (7 a.m.–5 p.m.) under a clear sky, at a mid-day
temperature of 18 ºC (November 2006) or 35 ºC (June
2007). Cells were then harvested, extracted with metha-
nol–acetone, and the absorption spectra were recorded.
No significant increase in MAA content relative to the
chlorophyll a peak at 665 nm was observed in any of
the samples.
The results of our survey of the occurrence of MAAs
in the springs around the Dead Sea can be summarized
as follows:
1. MAAs are absent or nearly absent in the springs of
the highest temperatures.
2. In the lower temperature waters (52 ºC and below)
MAAs were encountered (absorption maximum
around 334 nm), but always in low concentrations
compared to other environments in which occurrence
of MAA sunscreen pigments has been documented.
3. Somewhat higher MAA concentrations were found
in the halophilic cyanobacterial community at Ein
Gedi at the lowest elevation.
4. A 10-hour exposure of samples to full sunlight at
an elevation of +780 m (albeit at suboptimal tem-
peratures) did not induce synthesis of more MAA to
compensate for the increased solar UV radiation.
The filaments of Scytonema, found in dense black-
gray colonies near the outflow channels of some of
the Zerka Ma’in hot springs, are surrounded by a thick
sheath (Fig. 2, lower panels) with the characteristic
brown color of scytonemin. Scytonemin is a dimeric in-
dole alkaloid. It is probably synthesized from aromatic
amino acid residues. It has an absorption maximum
at 384 nm (Castenholz and Garcia-Pichel, 2000). Ab-
sorption spectra of extracts of this material in acetone
or in methanol–acetone 1:1 showed the characteristic
absorption peak of scytonemin, greatly exceeding the
height of the chlorophyll a absorption peak (Fig. 4C).
Scytonemin has a broad absorption band, so that protec-
tion is provided against UV light of wavelengths shorter
than the 384 absorption maximum as well, and the very
high concentrations at which this pigment is present in
the sheaths surrounding the cells can therefore provide
Oren et al. / Microalgae and cyanobacteria of the Dead Sea
12
efficient protection against UV-induced cell damage.
However, literature data suggest that the scytonemin
content of those cyanobacteria that produce the pigment
is poorly correlated with their actual exposure to UV
light, and may be rather correlated with the occurrence
of periods of restricted metabolism: the large invest-
ments required for effective use of scytonemin may only
pay off when exposure is linked to periods of metabolic
inactivity (Castenholz and Garcia-Pichel, 2000; Pente-
cost, 1993). Scytonemin has never been reported to oc-
cur in truly thermophilic cyanobacteria. A survey of the
hot springs in Yellowstone National Park, USA (eleva-
tion above 2000 m above sea level, so that ambient UV
irradiance is high) showed UV screening pigments such
as scytonemin to be absent above 55 ºC, the upper limit
for growth of sheathed species such as Pleurocapsa and
Calothrix (Wickstrom and Castenholz, 1978).
Concluding remarks
The first survey of cyanobacterial diversity in the Dead
Sea area (Frémy and Rayss, 1938) was published in
the first issue of the Palestine Journal of Botany—Je-
rusalem Series, later renamed the Israel Journal of
Botany, now the Israel Journal of Plant Sciences. The
current article, 70 years after the description of the
cyanobacterial diversity in the Zara springs, published
in the same journal, shows that our understanding of
the algal and cyanobacterial diversity in the Dead Sea
and its surroundings has increased considerably. We
now have sufficient information about the occurrence of
Dunaliella in the lake to be able to forecast under which
conditions massive blooms of the alga can be expected
to develop in the future. This is not only an exercise of
academic interest, but the in-depth understanding of the
biology of Dunaliella is highly important when trying
to predict the implications of a Red Sea–Dead Sea or a
Mediterranean–Dead Sea water carrier on the Dead Sea
ecosystem (Oren et al., 2004, 2005).
The opening of the border between Israel and Jordan
since the peace treaty between the counties was signed
in 1994 made both shores of the Dead Sea accessible to
scientists from both countries. The joint Jordanian–Is-
raeli surveys of the hot springs of Wadi Zerka Ma’in and
of Zara, initiated in 2005 under the aegis of the Bridging
the Rift Foundation, enabled the renewed exploration of
these sites using modern scientific methods, and have
shown that the Jordanian hot springs are among the most
interesting sites for the study of the diversity and physi-
ology of cyanobacteria in thermal environments. It may
be expected that the ongoing research at the sites will
add new insights into our understanding of cyanobacte-
rial life at high temperatures.
Israel Journal of Plant Sciences 56 2008
Acknowledgments
We thank the Bridging the Rift Foundation for enabling
the survey of the Jordanian hot springs and for financial
support. We further thank Dr. Reuven Ortal of the Israel
Nature and National Parks Authority for permission to
collect samples at the Ein Fesha nature reserve, and Mr.
Boaz Ron for allowing access to the Ein Gedi spa site.
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