Phykos 42 (2): 1-13 (2012)

Phycological Society, India

Effects of UV-B on cyanobacteria

Ultraviolet-B radiation effects on cyanobacteria and the role of sunscreen pigments in its
protection
Piyoosh K. Babele 1, Garvita Singh1, Madhu B. Tyagi2, Rajeshwar P. Sinha3 and Ashok Kumar1*
1

School of Biotechnology, 2Mahila Maha Vidyalaya and 3Centre of Advanced Study in Botany, Banaras Hindu University, Varanasi-221005,
India

*Corresponding author: Tel: + 91 542 2368331/6701593; Fax: + 91 542 2368693/2368174; E-mail : kasokbt@rediffmail.com

Abstract
Depletion of the stratospheric ozone layer due to anthropogenically released chemicals such as chlorofluorocarbons (CFCs) has resulted in an
increase in ultraviolet-B (UV-B; 280-315 nm) radiation on the Earths surface. A number of physiological and biochemical processes such as
growth, survival, cell differentiation, motility, pigmentation, photosynthesis, nitrogen metabolism, proteins and DNA have been reported to be
affected by UV-B radiation. However, response of cyanobacteria towards UV-B radiation differs in various species. Most probably differential
effects are mainly due to protective mechanisms which various species of cyanobacteria adopt under natural condition upon sensing the stress of
UV-B radiation. Various protective mechanism (s) such as morphological, avoidance, synthesis of sunscreen pigments, DNA repair by
phototreactivation etc. have been reported in diverse species of cyanobacteria to counteract the damaging effects of UV-B radiation. This chapter
deals with the general effects of UV-B radiation on cyanobacteria and the role of sunscreen pigments as protective mechanism against UV-B mediated damages.

Introduction
Cyanobacteria are the first photosynthetic
oxygen-evolving gram-negative prokaryotes which
appeared during the Precambrian era (between 2.8 and
3.5109 years ago) when the ozone shield was absent. They
presumably faced high fluxes of ultraviolet radiations
(UVR), which must have acted as an evolutionary pressure
leading to the selection for effective protecting
mechanisms. Cyanobacteria are the most important
biomass producers and play globally significant role in
biogeochemical cycle of nitrogen, carbon and oxygen
(Hder et al., 2007). These prokaryotes are excellent source
of a wide range of biologically active compounds of
significant values that has fascinated researchers for their
pharmaceutical
and
biotechnological
exploitation
(Gademann and Portmann, 2008; Rastogi and Sinha, 2009).
During past few decades rapid industrialization
has resulted in an increase in anthropogenically released
atmospheric pollutants such as chlorofluorocarbons,
chlorocarbons and organobromides that cause depletion of
stratospheric ozone layer (Weatherhead and Anderson,
2006). The rapid depletion of ozone layer causes increase
in the highly energetic UV radiation on the Earths surface
which is absorbed by biomolecules such as nucleic acids
and proteins and ultimately shows lethal effects on the
biological systems (Hder et al., 2007).
On the basis of the mechanisms of interaction
with living matter and its overall severity, the solar UV
spectrum can be divided into ultraviolet-A (315400 nm),
ultraviolet-B (280315 nm), and UV-C (100-280 nm). UVA effects occur through sensitizing molecules, which on
absorption can interact with oxygen to create reactive
oxygen species (ROS) these in return can oxidize a number
of cellular biomolecules. UV-B damage, by contrast, results
from direct absorption by the target molecules (mainly

DNA and proteins) and does not depend on the presence of

oxygen (Rastogi et al., 2010). Highest energetic ultravioletC radiation does not reach the Earths surface at present,
owing to absorption by ozone and losses through
atmospheric scattering.
General effects of UV-B radiation on cyanobacteria
Several studies conducted under laboratory and
natural conditions have revealed the harmful effects of UVB radiation on growth, survival, motility, development,
pigmentation, nutrient uptake, and various other metabolic
processes of cyanobacteria (Hder et al., 2007). These
effects are in part due to the direct effect on membrane
proteins, photosystem II, DNA, enzymes, growth regulators
or due to indirect effect through the formation of reactive
oxygen species. Of several targets of UV-B damage that
have been reported, DNA and photosynthesis are
recognized as the most predominant action sites (Singh et
al., 2010a). It has been elegantly demonstrated that when
Anabaena aequalis cultures are exposed to UV-B radiation
there is delayed differentiation of vegetative cells to
heterocyst and further into akinetes (Blakefield and Harris,
1994). Growth and survival of several cyanobacteria are
severely affected by UV-B exposure although degree of
growth inhibition and survival vary significantly in
different genera (Sinha et al., 1995). Virtually, most of the
experiments on UV-B radiation have been conducted under
controlled laboratory conditions, a few workers reported
that growth is inhibited up to 40 % under solar UVR in
Anabaena sp. PCC 7120 and certain other nitrogen-fixing
cyanobacteria (Gao et al., 2007).
One of the crucial detrimental effects of UV-B
radiation in cyanobacteria include photobleaching of
photosynthetic pigments, decrease in phycobiliprotein
content and disassembly of phycobilisome complex (Sinha

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et al., 2005). SDS-PAGE analysis of phycocyanin and its

linker polypeptides in Anabaena sp. revealed loss of
monomers of phycocyanin after 1 h of UV- B exposure
(Sinha et al., 2003). Additionally, several studies have
demonstrated that UV-B radiation affects spectral
properties of pigments specifically chlorophyll a and
phycobiliproteins of cyanobacteria (Gao et al., 2007).
Together with this, various other photosynthetic parameters
such as 14CO2 uptake, O2 evolution and ribuolose-1, 5
bisphosphate carboxylase/oxygenase (RUBISCO) activity
are also down regulated (Sinha et al., 2008). The D1 and
D2 proteins that are major constituent of PSII reaction
centers are degraded by exposure of UV-B. Equally
important effects of UV-B radiation include inhibition of
nitrogen fixation in almost all the species so far tested.
Kumar et al.,(2003) reported complete loss of nitrogenase
activity within 25-40 min of UV-B exposure in several rice
field cyanobacteria. It was demonstrated that the activity of
UV-B inhibited nitrogenase did not appear upon transfer of
cultures to fluorescent light, suggesting that the inhibition
may be due to specific inhibition of the enzyme (Kumar et
al., 2003). Using inhibitors of protein synthesis and PS-II
activity, they demonstrated that restoration of nitrogenase
activity in UV-B exposed cultures occurred by fresh
synthesis of nitrogenase polypeptide. Interestingly, other
enzymes of nitrogen metabolism such as nitrate reductase,
glutamine synthetase and glutamate synthase are less
sensitive to elevated level of UV-B intensity (Kumar et al.,
1996).
Total protein profile of cyanobacteria showed
significant alterations following exposure of cultures to
UV-B radiation (Sinha et al., 2005). Several protein bands
disappeared and a few new protein bands appeared in the
gel. Total proteome analysis of Synechocystis sp. PCC 6803
by 2-dimensional (2-D) gel electrophoresis showed
different expression level of proteins in the cytoplasm
under short and long-term UV-B stress (Gao et al., 2009).
One hundred and twelve differentially expressed protein
spots were identified by mass spectrometry to match 75
diverse protein species. The above study focused on amino
acid biosynthesis, photosynthesis and respiration, energy
metabolism, protein biosynthesis, cell defense, and other
functional groups (Gao et al., 2009).
Several types of DNA damages have been
identified which probably develop mainly due to direct
absorption of UV-B radiation by the native DNA molecule
and indirectly by oxidative stress. The main DNA damages
include formation of dimeric photoproducts such as cis-syn
cyclobutane pyrimidine dimers (CPDs) and pyrimidine (64) pyrimidone photoproducts (6-4PPs) and their Dewar
isomers (Sinha and Hder, 2002). Damage to DNA was
also evident in the study conducted by Kumar et al., (2004)
who found loss of template activity of genomic DNA in
Anabaena BT2 after UV-B exposure. They employed

Effects of UV-B on cyanobacteria

simple and rapid technique of PCR assay such as RAPD

(random
amplified
polymorphic
DNA),
rDNA
amplification and ARDRA (amplified ribosomal DNA
restriction analysis) to reveal damage caused to DNA by
UV-B treatment. Recently a modified version of the
fluorometric analysis of DNA unwinding (FADU) assay
has been described by Rastogi et al., (2010) that enabled
the measurement of DNA strand breaks and DNA repair in
a reliable and convenient manner. Huang et al., (2002) have
made critical analysis of global gene expression profile of
the cyanobacterium Synechocystis sp. strain PCC 6803 in
response to irradiation with UV-B and white light. The
study showed that several families of transcripts were
altered by UV-B treatment, including mRNAs specifying
proteins involved in light harvesting, photoprotection and
heat shock response. There are several other processes in
cyanobacteria which are affected by UV-B radiation, herein
we have highlighted only general effects.
Defense mechanisms developed by cyanobacteria
against UV-B radiation
As described above cyanobacteria have many
cellular targets that are severely affected by harmful UV
radiations however these microorganisms developed
various defense mechanisms to overcome harmful effects
of these UV radiations. In this section various defense
mechanisms adopted by cyanobacteria against UV
radiations are described.
Cyanobacteria in their natural habitat adopted
avoidance as a first line of defense which includes
migration from high level to low level of UV intensity in
water column, formation of mats, changes in morphology
to provide self shading and synthesis of extracellular
polysaccharides. The avoidance of damaging UVR
provides protection upto some extent as this mechanism
includes motility and mat forming capability of
cyanobacteria as well as on the turbidity and depth of the
water column.
However, once UVR reaches inside the cell it
interacts with oxygen and other organic compounds to
generate toxic ROS such as superoxide (O2-), hydroxyl
radical (OH-) or hydrogen peroxide (H2O2) which causes
oxidative stress. To overcome these oxidative stresses a
second line of defense comes into play which comprise
both non-enzymatic and enzymatic antioxidants. Nonenzymatic antioxidants in the cells are ascorbate (vitamin
C), tocopherol (vitamin E), carotenoids and reduced
glutathione. The enzymatic antioxidants are superoxide
dismutase (SOD), catalase, glutathione peroxidase (GSHPx) and the enzymes involved in the ascorbate-glutathione
cycle to detoxify the ROS such as ascorbate peroxidase
(APX), monodehydroascorbate reductase (MDHAR),
deghdroascorbate reductase (DHAR) and glutathione
reductase (GR) (He and Hder, 2002).

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A third line of defense operates through the

synthesis of UV-absorbing compounds by several
cyanobacteria (Sinha and Hder, 2008). Mycosporine-like
amino acids (MAAs) and scytonemin are well known UVabsorbing/
screening
compounds
that
provide
photoprotection against UV-B and/or UV-A radiation
(Sinha and Hder, 2008). This line of defense mechanism is
described in forthcoming section.
When repair of harmful UVR-induced damages
(damages of biomolecules such as DNA and proteins)
escape from first, second and third line of defense
mechanisms, a fourth line of defense mechanism i.e., DNA
repair by photoreactivation plays vital role. Although the
presence of multiple copies of genomic DNA in the
cyanobacteria may nullify the effect of single mutations by
UVR, the existence of several DNA repair mechanisms
strengthen them even more to cope with this radiation
(Sinha and Hder, 2002). These mechanisms include
photoreactivation by photolyase which converts UV
induced dimers into monomers, the dark or excision repair
and the recombinational repair. The presence of a UVinducible photoreactivation system has been reported in
strains of Anabaena sp. such as Anabaena sp. PCC 7120,
A. variabilis PCC 7937, Anabaena sp. M-131 and A.
variabilis sp. PCC 7118 (Levine and Thiel, 1987). The
genes for photolyase homologs have been identified in
Synechocystis sp. PCC 6803 and were functionally
characterized for their roles in photoreactivation (Ng and
Pakrasi, 2001). Han et al., (2001) have also reported
photoreactivation of UV-B induced inhibition of
photosynthesis in Anabaena sp. An increase in the
transcript level of recA and the concomitant increase in the
abundance of the corresponding 3738-kDa polypeptide
were reported in A. variabilis after UV exposure (Owttrim
and Coleman, 1989). The gene for the DNA repair enzyme
Fpg (formamydopyrimidine-DNA glycosylase) has been
reported from Synechococcus elongatus and was suggested
to be involved in photoprotection against oxidative damage
(Mhlenhoff, 2000). Repair of cyclopyrimidine dimers
(CPDs) is light and temperature dependent since these
lesions were removed more efficiently in visible light than
in darkness and the optimum temperature for the repair was
found at 20 0C (Rastogi et al., 2011).
In addition, recent studies showed that
cyanobacteria may also undergo apoptosis or programmed
cell death (PCD) when a cell is damaged beyond repair. An
autocatalytic PCD has been shown to operate in the
nitrogen-fixing cyanobacterium Trichodesmium sp. and
was found to be induced by high irradiance, iron starvation
and oxidative stress (Berman-Frank et al., 2004). Similarly,
recent data on Microcystis aeruginosa showed that H2O2
treatment induces PCD in this organism, and catalase was
capable of inhibiting PCD, implicating the role of PCD
under oxidative stress (Ross et al., 2006). Several genes

Effects of UV-B on cyanobacteria

encoding for caspases, enzymes involved in PCD in

eukaryotes, have also been recently reported in the
sequenced genome of M. aeruginosa (Frangeul et al.,
2008). The caspase activity as well as proteins reacting to
human caspase-3 antibodies
was reported in
Trichodesmium sp. (Berman-Frank et al., 2004). The
freshwater cyanobacterium Anabaena has also been found
to activate PCD and increases general protease activity
after exposure to univalent-cation salts (Ning et al., 2002).
Thus, it is clear that the process of PCD plays an important
role under oxidative stress in cyanobacteria, however
further study is needed to find out its advantageous role
under UV stress or UV-mediated oxidative stress.
Sun-screening compounds in cyanobacteria
One of the most important defense mechanisms
towards UV-B radiation effects in cyanobacteria is the
production of secondary metabolites which act as
sunscreen. UV sunscreen compounds have two main
properties; (a) it must absorb in the UV range with a high
absorption coefficient, and (b) its concentration in the
organism must be sufficient to cause a substantial reduction
in the UV dose received by the organism. In addition to
above properties, the compound should not sensitize
photodamage, and should be present in a conformation that
is optimal for screening and is produced specifically and/or
in response to UV light exposure. Brief description of
sunscreen compounds is given below under separate
heading.
A. Scytonemin: a sunscreen pigment
Although several workers reported sheath
pigments from a number of cyanobacterial species but the
nature, physiological role and universality of scytonemin
remained unexplored till 1993. Garcia-Pichel and
Castenholz (1991) for the first time characterized in detail
the structure and function of scytonemin from a few
cyanobacteria. Scytonemin is a yellow to brown, lipidsoluble, non-fluorescent, very stable pigment that is
excreted and deposited in the extracellular polysaccharide
sheaths of some cyanobacteria (Garcia-Pichel and
Castenholz, 1991). Microspectrophotometric measurements
of the transmittance of pigmented sheaths and the screening
of excitation of phycocyanin fluorescence under UV light
demonstrated that the pigment is effective in shielding the
cells from incoming near-UV and blue radiation, but not
from green or red light, which is needed for photosynthesis.
The screening effect of scytonemin among many cyanobacteria is substantial, particularly among colony-forming
species (Garcia-Pichel and Castenholz, 1993). In the model
organism Chlorogloeopsis sp., its presence is associated
with amelioration of photo-inhibition of photosynthesis,
reduced photobleaching of chlorophyll a and faster growth
rates under UV-A radiation. The beneficial effects also

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remain under conditions of physiological inactivity.

Structurally scytonemin is a symmetrical indole-alkaloid
consisting of fused heterocyclic units, connected through a
carboncarbon bond, with a molecular mass of 544 g mol 1.
Scytonemin is redox sensitive, changing between a
greenish brown oxidized form and a red reduced form,
although the physiologically relevant form is in the
oxidized state. The complex ring structures with conjugated
double-bond distribution allow strong absorption in the
UV-A range, with a maximum around 370 nm in vivo
(Proteau et al., 1993).
Distribution and physiological ecology
Scytonemin can be readily detected by
microscopic observation, and it has been reported from
more than 300 cyanobacterial species, including all major
taxonomic groups (Garcia-Pichel and Castenholz, 1991). It
is common in natural populations that are exposed to high
irradiance, population from extreme environment, such as
recurrent desiccation or low temperatures. Scytonemin has
yet to be found in planktonic populations, either marine or
freshwater. Its content can reach up to 5 % of the cellular
dry weight in cultivated isolates; much larger
accumulations are encountered in field populations (Sinha
et al., 2001). Typical habitats for scytonemin-bearing
cyanobacteria are intertidal mats, epilithic biofilms and
biological soil crusts, but many others exist. Scytonemin is
produced in response to UV-A exposure in all cases
examined (Ehling-Schulz et al., 1997). Certain
environmental stresses can modulate scytonemin synthesis
in apparently complex regulatory interactions. Temperature
or photo-oxidative stresses alone do not induce scytonemin
synthesis, but can increase the levels attained during UV-A
induction (Dillon et al., 2002). Osmotic stress results in a
moderate induction of scytonemin production in one strain,
but not in many others (Garcia-Pichel and Castenholz,
1991). Periodic desiccation or lack of fixed nitrogen can
also enhance the level of scytonemin attained during UV-A
induction in some strains (Fleming and Castenholz, 2007;
2008).
Biosynthesis
Preliminary studies based on structural, genetic,
radiotracer techniques and evidences from the pregenomics era revealed that the biosynthesis of scytonemin
is related to that of the aromatic amino acids (Mandalka,
1999). Proposition of biosynthetic pathway became
possible after isolation of a scytonemin-less mutant strain

Effects of UV-B on cyanobacteria

of Nostoc punctiforme ATCC 29133 (PCC 73102) by

transposon mutagenesis. The mutation was formally traced
to open reading frame (ORF) NpR1273 (now known as
scyD). Subsequently, it was demonstrated that scyD was the
part of a gene cluster of unknown function, involving 18
contiguous ORFs (NpR1276 to NpR1259, including scyAscyF) (Fig.1). Possible involvement of aromatic amino
biosynthetic pathway is also evident from gene cluster
denoted in Fig. 1 where the homologues of genes in the
shikimate pathway and aromatic amino acid pathway are
located downstream of the scytonemin biosynthetic genes
(scyA-scyF). It is presumed that the synthesis of
scytonemin starts in the cytoplasm from supply of
tryptophan and p-hydroxyphenylpyruvate. During the first
step of biosynthesis ScyB, a homologue of amino acid
dehydrogenase, (an NADH-dependent oxidoreductase)
catalyses the oxidative deamination of Trp (tryptophan) to
provide indole-3-pyruvic acid (I3P). The second required
precursor p-hydroxyphenylpyruvic acid (HPP), is most
probably made available through NpR1269, a putative
prephenate dehydrogenase which catalyses oxidation of
prephenate to form HPP. It is also felt that as ScyA
(NpR1276) exhibits strong amino acid sequence similarity
to a thiamine pyrophosphate (TPP)-requiring enzyme
known as acetolactate synthase, most probably it is
involved in the formation of -acetolactate from two
molecules of pyruvate (Chipman et al., 1998). In the next
step of reaction, ScyC (NpR1274) mediates the
transformation of -acetolactate (-keto acid adduct) to the
monomer of scytonemin skeleton involving a series of
reaction such as decarboxylation, cyclization and oxidation
(Balskus and Walsh, 2009). Finally, the enzymes encoded
by scyD, scyE and scyF transform the resulting skeleton to
the final product in the form of scytonemin.
After the elucidation of hypothetical pathway,
certain important findings have emerged pertaining to
scytonemin biosynthesis. Studies based on comparative
genomics and direct sequencing of several strains have
revealed that the scytonemin cluster of Nostoc ATCC
29133 is well conserved among cyanobacteria (Sorrels et
al., 2009; Soule et al., 2009). Additionally, five additional
genes were found located in the cluster of several strains
(Soule et al., 2009), homologues of which are also
conserved in Nostoc ATCC 29133. Much work is still
needed to decipher the exact biosynthetic pathway and role
of individual gene in sctonemin synthesis. Equally
important is the localization of this compound, how does it
accumulate in sheath of many cyanobacteria.

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Effects of UV-B on cyanobacteria

Fig. 1. Biosynthetic pathway for scytonemin.

B. Mycosporine-like amino acids: a diverse family of

sunscreens
Mycosporine-like amino acids (MAAs) constitute
a diverse family of water soluble, colorless natural products
that share a 5-hydroxy-5-hydroxymethyl-cyclohex-1, 2-ene
ring and have a methoxy-substituent in C2 (Table 1). They
are always substituted in C3 with an amino compound and
in C1 with either an oxo or an imino moiety. Sometimes the
term mycosporine refers to those with a ketone at C1

(also known as oxo-mycosporines or mono-substituted

mycosporines), whereas MAA is reserved for those with an
imino-group (such as imino-mycosporines and bisubstituted mycosporines) (Gao and Garcia-Pichel, 2011).
MAAs can sometimes be glycosylated or covalently bound
to oligosaccharides. They present unique absorption spectra
with a single, narrow and strong absorption band that has a
maximum absorbance between 309 and 362 nm.

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Effects of UV-B on cyanobacteria

Table 1. Absorption maxima and molecular structure of MAAs

Name of MAAs
MAA-glycine

Absorption
(nm)
310

Mycosporine-taurine

309

Mycosporine-2 glycine

332

Mycosporine-alanine

310

Mycosporine-glutamine

310

Mycosporine serinol

310

maxima

Molecular Structure

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Effects of UV-B on cyanobacteria

Palythene

360

Palythine

320

Palythine-threonine

320

Palythenic acid

337

Palythinol

332

Porphyra-334

334

Shinorine

334

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Effects of UV-B on cyanobacteria

Usujirene

357

Euhalothece-362

362

Asterina-330

330

MAAs dissipates energy as heat without

generating ROS (Conde et al., 2004). Most MAAs are
stable, but mycosporine-Gly and mycosporine-Gln can
undergo photosensitized hydrolysis (Bernillon et al., 1990).
MAAs are most typically accumulated as solutes in the
cytoplasm, but derivatives covalently bound to
oligosaccharides can be excreted into the sheath
(glycocalyx), as in Nostoc commune (Bhm et al., 1995).
Mycosporine content often reaches several per cent of the
cellular dry mass of the producing organism (Favre-Bonvin
et al., 1987). Various aspects of MAA biology have
recently been comprehensively reviewed (Shick and Dunlp,
2002; Carreto and Carignan, 2011; Gao and Garcia-Pichel,
2011).
Phylogenetic and ecological distribution
For the first time mycosporines were reported in
the mycelia of fungi basidiomycetes that had been induced
to sporulate by exposure to UV-B radiation (Favre-Bonvin
et al., 1987). Since then, mycosporine-like natural products
from red algae, sea-stars, corals, phytoplankton,
dinoflagellates, lichens, sponges and cyanobacteria have
been reported and now there is a vast array of
microorganisms that have mycosporine-like secondary
metabolites (Shick and Dunlap, 2002). However, no reports
are available of the presence of MAA in bacteria, plants
and archaea. Animals do not synthesize MAAs directly as
they lack shikimate pathway but they receive them from
their diet or from symbiotic microorganisms. Bi-substituted
mycosporines are prevalent in algae and cyanobacteria, but
they are absent from fungi, in which a considerable

diversity of mono-substituted mycosporines exists (GarciaPichel, 1998). Recently a database has been developed on
the distribution of mycosporine and MAAs in marine and
freshwater organisms (Sinha et al., 2007).
Ecology and physiology of MAAs
Screening can be enhanced substantially in N.
commune (Ehling-Schulz and Scherer, 1999), in which the
MAAs are laid down extracellularly, and in most other
species owing to growth as a biofilm or colony. In
cyanobacteria, MAA content correlates with a moderate
physiological amelioration of photodamage, which remains
even under conditions of physiological inactivity, as would
be expected for a sunscreen (Garcia-Pichel and Castenholz
1993). In most MAA-synthesizing organisms, the
accumulation of MAA is induced or enhanced by exposure
to intense solar radiation, although the exact action
spectrum for the response varies (Shick and Dunlap, 2002).
The role of MAAs as sunscreens has been elegantly shown
in invertebrate eggs (Adams and Shick, 1996) and
dinoflagellates (Neale et al., 1998). Mycosporines
synthesized by primary producers in nature can be passed
along the food chain: after being taken up by a range of
grazers (from copepod crustaceans to fish; Sommaruga and
Garcia-Pichel, 1999), they are selectively preserved and
then accumulate in UV-light-sensitive tissues (such as the
epidermis of holothurians or the eye lenses of fish). MAAs
produced by symbiotic protists (zooxanthellae) are the
source of the large mycosporine pools found in
scleractinian corals.

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Alternative roles of MAAs

Mycosporine-glycine and phorphyra-334 are
efficient antioxidant. Tao et al. (2009) reported that
porphyra-334 efficiently suppressed the lipid peroxidation
induced by singlet oxygen although the antioxidative effect
observed was relatively moderate at the initial stage of
oxidation and can scavenge ROS produced during UV
exposure (or otherwise), but other MAAs, such as
shinorine, does not share this antioxidant property (Dunlap
and Yamamoto, 1995). Because in some strains MAA
biosynthesis can be induced by osmotic shock, and because
certain halophilic cyanobacteria and fungi accumulate
unusually large concentrations of MAA, a role as
compatible solutes has been proposed for these compounds
(Oren, 1997; Kogej et al., 2006). However, quantitative
assessments reveal that the contribution of MAA to the
overall intracellular osmotic pressure is negligible when
compared to that of co-occurring, bonafide compatible
solutes accumulated by the same cells (Portwich and
Garcia-Pichel, 1999). In fungi, some mycosporines seem to
be effective in eliciting morphogenetic changes: conidia
germination at high conidial density is inhibited by the
presence of extracellular mycosporine-Ala (Leite and
Nicholson, 1993). Some study shows that MAAs act as
nitrogen reservoir but experimental proofs are needed in
this context. It is found that MAAs effectively block
thymine dimer formation by UVR in vitro, however, in vivo
experiments are needed to prove the role of MAAs in
protecting DNA of organisms (Rastogi et al., 2010). MAAs
also have a role in sunscreens for skin protection as these
protects skin from premature skin-aging (Schmid et al.,
2003).
Biosynthesis
Preliminary genomic studies in fungi and cyanobacteria (Favre-Bonvin et al., 1987; Portwich and GarciaPichel, 2003) suggested that the biosynthesis of MAAs
originates from the first part of the shikimate pathway,
possibly at the level of 3-dehydroquinate synthase (DHQ
synthase, encoded by aroB) (Portwich and Garcia-Pichel,
2003) (Fig. 2). Tracer experiments in Chlorogloeopsis sp.
revealed that the amino acid condensed directly on the
cyclohexenone ring and resulted in the origin of the
variable substituents. Most probably mycosporine-gly was

Effects of UV-B on cyanobacteria

the first MAA synthesized and acted as a precursor for

other bi-substituted imino-mycosporines, such as shinorine
(Portwich and Garcia-Pichel, 2003). Recently, comparative
genomics of cyanobacteria has helped to identify a region
of potential interest as the locus for MAA biosynthesis
(Singh et al., 2010a). This was based on the presence of a
DHQ synthase homologue (ORF Ava_3858) flanked by a
putative O-methyltransferase (O-MT), which might
potentially lead to the cyclohexenone core. The gene
products of N. punctiforme also formed 4-deoxygadusol
(4-DG) when expressed in tandem in vitro if supplied with
sedoheptulose -6-phosphate (SHP) as substrate, but not
when supplied with 3-DHQ. Details of biosynthetic
pathway of MAA and tentative organization of genes
involved in its synthesis are well described in the review of
Gao and Garcia-Pichel (2011). However, much work is
needed to decipher the biosynthetic pathway especially the
role of various genes in synthesis of MAA in different
species of cyanobacteria (Balskus and Walsh, 2010).
Regulation
MAA synthesis in cyanobacteria and fungi is
typically induced or enhanced by exposure to UV-B
radiation (Portwich and Garcia-Pichel, 1999; Rozema et al.,
2002; Sinha et al., 2003; Portwich and Garcia-Pichel,
2000). The process of UV photoreception has been studied
in Chlorogloeopsis sp. (Portwich and Garcia-Pichel, 2000),
in which the UV-dependency of synthesis could be traced
to a true photosensory process mediated by a UV-B photoreceptor. The action spectrum for MAA induction and the
sensitivity of the photosensory process to specific
biosynthesis inhibitors and antagonists suggest that an asyet-unidentified pterin acts as the chromophore in the
photoreceptor. Nothing is known about signal transduction
or how this links to gene expression. Most probably a range
of sensory inputs is likely to contribute to MAA regulation
in an organism-specific manner. For example, in A.
variabilis, as in algae, visible light can induce MAA
synthesis (Singh et al., 2008), and osmotic stress
differentially regulates mono- and bi-substituted MAAs in
Chlorogloeopsis spp. (Portwich and Garcia-Pichel, 1999).
Nitrogen and sulphur availability may also influence the
allocation of resources for synthesizing MAAs (Singh et
al., 2010b).

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Phycological Society, India

Effects of UV-B on cyanobacteria

Fig. 2. Putative biosynthetic pathways for mycosporine-like amino acids.

Future prospects
Many key aspects of the scytonemin and MAAs
biology are yet to revealed. The predicted localization for
the route of biosynthesis of scytonemin remains the most
exciting open question because of its uniqueness in
cyanobacterial bacterial biology. A combination of highresolution bioimaging techniques and molecular tagging of
the enzymes involved will be needed to test it. Exact role of
a large number of genes that are associated with the
scytonemin operon is still unknown, there is a need resolve

this issue. Lastly, the molecular mechanism governing the

regulation of scytonemin synthesis is still a black box and
one has to study this process from cyanobacteria growing
in diverse habitat but favorable for bulk synthesis of
scytonemin.
Considering the large number of MAA
variations, perhaps one of the most daunting future tasks
will be to establish the molecular basis for this diversity.
Equally important is the aspects of MAAs regulation, how
it relates to environmental sensory processes, signal

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Phycological Society, India

transduction, gene expression and post-transcriptional

regulation clearly represent the next frontier in MAAs
research. During the last two decades a vast array of data
related to UV-B effects on cyanobacteria have emerged but
there is a need to expedite research in this emerging area
with renewed interest involving researchers from diverse
field of modern biology. Studies conducted may surely lead
to the discovery of many exciting facts which are otherwise
hidden till date.
Acknowledgement: Works related to UV-B radiation
effects are partly supported by the project grant sanctioned
by Department of Science and Technology, Govt. of India,
New Delhi (SR/SO/PS-49/09).
REFERENCES
Adams, N. L. and J. M. Shick, 1996. Mycosporine-like
amino acids provide protection against ultraviolet
radiation in eggs of the green sea urchin
Strongylocentrotus
droebachiensis.
Photochem.
Photobiol. 64: 149-158
Balskus, E. P. and C. T. Walsh, 2009. An enzymatic
cyclopentyl[b]indole
formation
involved
in
scytonemin biosynthesis. J. Am. Chem. Soc. 131:
14648-14649
Balskus, E. P. and C. T. Walsh, 2010. The genetic and
molecular basis for sunscreen biosynthesis in
cyanobacteria. Science 329: 1653-1656
Berman-Frank, I., Bidle, K.D., Haramaty, L. and P. G.
Falkowski, 2004. The demise of the marine
cyanobacterium, Trichodesmium spp., via an
autocatalyzed cell death pathway. Limnol. Oceanogr.
49: 997-1005
Bernillon, J., Parussini, E., Letoublon, R., Favre-Bonvin, J.
and N. Arpin, 1990. Flavin-mediated photolysis of
mycosporines. Phytochemistry 29: 81-84
Blakefield, M. K. and D. O. Harris, 1994. Delay of celldifferentiation in Anabaena aequalis caused by UV-B
radiation and the role of photoreactivation and
excision-repair. Photochem. Photobiol. 59: 204-208
Bhm, G. A., Pfleiderer, W., Bger, P. and S. Scherer,
1995. Structure of a novel oligosaccharidemycosporine-amino acid ultraviolet A/B sunscreen
pigment from the terrestrial cyanobacterium Nostoc
commune. J. Biol. Chem. 270: 8536-8539
Carreto, J. I. and M. O. Carignan, 2011. Mycosporine-like
amino acids: relevant secondary metabolites. chemical
and ecological aspects. Mar. Drugs 9: 387-446
Chipman, D., Barak, Z. A. and J. V. Schloss, 1998.
Biosynthesis of 2-aceto-2-hydroxy acids: acetolactate
synthases and acetohydroxyacid synthases. Biochim.
Biophys. Acta 1385: 401-419
Conde, F. R., Churio, M. S. and C. M. Previtali, 2004. The
deactivation pathways of the excited-states of the

Effects of UV-B on cyanobacteria

mycosporine-like amino acids shinorine and

porphyra-334 in aqueous solution. Photochem.
Photobiol. Sci. 3: 960-967
Dillon, J. G., Tatsumi, C. M., Tandingan, P. G. and R. W.
Castenholz, 2002. Effect of environmental factors on
the synthesis of scytonemin, a UV-screening pigment,
in a cyanobacterium (Chroococcidiopsis sp.). Arch.
Microbiol. 177: 322-331
Dunlap, W. C. and Y. Yamamoto, 1995. Small-molecule
antioxidants in marine organisms- antioxidant activity
of mycosporine-glycine. Comp. Biochem. Phys. B
Biochem. Mol. Biol. 112: 105-114
Ehling-Schulz, M. and S. Scherer, 1999. UV protection in
cyanobacteria. Eur. J. Phycol. 34: 329-338
Ehling-Schulz, M., Bilger, W. and S. Scherer, 1997.
UV-B-induced synthesis of photoprotective pigments
and extracellular polysaccharides in the terrestrial
cyanobacterium Nostoc commune. J. Bacteriol. 179:
1940-1945
Favre-Bonvin, J., Bernillon, J., Salin, N. and N. Arpin,
1987. Biosynthesis of mycosporines- mycosporine
glutaminol in Trichothecium roseum. Phytochemistry
26: 2509-2514
Fleming, E. D. and R. W. Castenholz, 2007. Effects of
periodic desiccation on the synthesis of the
UV-screening
compound,
scytonemin,
in
cyanobacteria. Environ. Microbiol. 9: 1448-1455
Fleming, E. D. and R. W. Castenholz, 2008. Effects of
nitrogen source on the synthesis of the UV-screening
compound, scytonemin, in the cyanobacterium Nostoc
punctiforme PCC 73102. FEMS Microbiol. Ecol. 63:
301-308
Frangeul, L., Quillardet, P., Castets, A.M., Humbert, J.F.,
Matthijs, H.C.P., Cortez, D., Tolonen, A., Zhang, C.C., Gribaldo, S., Kehr, J.C., Zilliges, Y., Ziemert, N.,
Becker, S., Talla, E., Latifi, A., Billault, A.,
Lepelletier, A., Dittmann, E., Bouchier, C., N.
Tandeau de Marsac, 2008. Highly plastic genome of
Microcystis aeruginosa PCC 7806, a ubiquitous toxic
freshwater cyanobacterium. BMC Genomics 9: 274
Gademann, K. and C. Portmann, 2008. Secondary
metabolites from cyanobacteria: complex structures
and powerful bioactivities. Curr. Org. Chem. 12: 326341
Gao, K. Yu, H. and M.T. Brown, 2007. Solar PAR and UV
radiation affect the physiology and morphology of the
cyanobacterium Anabaena sp. PCC 7120. J.
Photochem. Photobiol. B Biol. 89: 117-124
Gao, Q. and F. Garcia-Pichel, 2011 Microbial ultraviolet
sunscreens. Nature Rev. Microbiol. 9:791-802
Gao, Y. Xiong, W. Li X, Gao, C. F. Zhang, Y. L. Li, H.
and Q. Wu, 2009. Identification of the proteomic
changes in Synechocystis sp. PCC 6803 following

11

Phykos 42 (2): 1-13 (2012)

Phycological Society, India

prolonged UV-B irradiation. J. Exp. Bot. 60: 11411154

Garcia-Pichel, F. and R. W. Castenholz, 1993. Occurrence
of UV-absorbing, mycosporine-like compounds
among cyanobacterial isolates and an estimate of their
screening capacity. Appl. Environ. Microbiol. 59: 163169
Garcia-Pichel, F. 1998. Solar ultraviolet and the
evolutionary history of cyanobacteria. Orig. Life Evol.
Biosph. 28: 321-347
Garcia-Pichel, F. and R. W. Castenholz, 1991.
Characterization and biological implications of
scytonemin, a cyanobacterial sheath pigment. J.
Phycol. 27: 395-409
Hder, D.-P., Kumar, H. D., Smith, R. C. and R. C.
Worrest, 2007. Effects of solar UV radiation on
aquatic ecosystems and interactions with climate
change. Photochem. Photobiol. Sci. 6: 267-285
Han, T., Sinha, R. P. and D.-P. Hder, 2001. UV-A/blue
light-induced reactivation of photosynthesis in UV-B
irradiated cyanobacterium, Anabaena sp. J. Plant
Physiol. 158: 1403-1413
He, Y.Y. and D.-P. Hder, 2002. Reactive oxygen species
and UV-B: effect on cyanobacteria. Photochem.
Photobiol. Sci. 1: 729-736
Huang , L., McCluskey M. P., Ni, H. and LaRossa R. A.
2002. Global gene expression profiles of the
cyanobacterium Synechocystis sp. strain PCC 6803 in
response to irradiation with UV-B and white light. J.
Bacteriol. 184: 6845-6858.
Kogej, T., Gostincar, C., Volkmann, M., Gorbushina, A. A.
and N. Gunde-Cimerman, 2006. Mycosporines in
extremophilic
funginovel
complementary
osmolytes? Environ. Chem. 3: 105-110
Kumar, A., Sinha, R. P., D.-P. Hder, 1996. Effect of UVB on enzymes of nitrogen metabolism in the
cyanobacterium Nostoc calcicola. J. Plant Physiol.
148: 86-91
Kumar, A., Tyagi, M. B. and P. N. Jha, 2004. Evidences
showing ultraviolet-B radiation induced damage of
DNA in cyanobacteria and its detection by PCR assay.
Biochem. Biophys. Res. Commun. 318:1025-1030
Kumar, A., Tyagi, M. B., Jha, P. N., Srinivas, G. and A.
Singh, 2003. Inactivation of cyanobacterial
nitrogenase after exposure to ultraviolet-B radiation.
Curr. Microbiol. 46: 380-384
Leite, B. and R. L. Nicholson, 1993. Mycosporine-alanine:
a self-inhibitor of germination from the conidial
mucilage of Colletotrichum graminicola. Exp. Mycol.
16: 76-86
Levine, E. and T. Thiel, 1987. UV-inducible DNA repair in
the cyanobacteria Anabaena sp. J. Bacteriol. 169:
3988-3993

Effects of UV-B on cyanobacteria

Mandalka, A. Studies on Scytonemin Synthesis in

Cyanbacteria Univ. of Bremen, Germany, 1999
Mhlenhoff, U., 2000. The FAPY-DNA glycosylase (Fpg)
is required for survival of the cyanobacterium
Synechococcus elongatus under high light irradiance.
FEMS Microbiol. Lett. 187: 127-132
Neale, P. J., Banaszak, A. T. and C. R. Jarriel, 1998.
Ultraviolet suncreens in Gymnodinium sanguineous
(dinophyceae): mycosporine-like amino acids protect
against inhibition of photosynthesis. J. Phycol. 34:
928-938
Ng, W.-O. and H. B. Pakrasi, 2001. DNA photolyase
homologs are the major UV resistance factors in the
cyanobacterium Synechocystis sp. PCC 6803. Mol.
Gen. Genet. 264: 924-930
Ning, S. B., Guo, H. L., Wang, L., Y. C. Song, 2002. Salt
stress induces programmed cell death in prokaryotic
organism Anabaena. J. Appl. Microbiol. 93:15-28
Oren, A. 1997. Mycosporine-like amino acids as osmotic
solutes in a community of halophilic cyanobacteria.
Geomicrobiol. J. 14: 231-240
Owttrim, G.W. and J. R. Coleman, 1989. Regulation of
expression and nucleotide sequence of the Anabaena
variabilis recA gene. J. Bacteriol. 171: 5713-5719
Portwich, A. and F. Garcia-Pichel, 2003. Biosynthetic
pathway of mycosporines (mycosporine-like amino
acids) in the cyanobacterium Chlorogloeopsis sp.
strain PCC 6912. Phycologia 42: 384-392
Portwich, A. and F. Garcia-Pichel, 1999. Ultraviolet and
osmotic stresses induce and regulate the synthesis of
mycosporines in the cyanobacterium Chlorogloeopsis
PCC 6912. Arch. Microbiol. 172:187-192
Portwich, A. and F. Garcia-Pichel, 2000. A novel
prokaryotic
UVB
photoreceptor
in
the
cyanobacterium Chlorogloeopsis PCC 6912.
Photochem. Photobiol. 71: 493-498
Proteau, P. J., Gerwick, W. H., Garcia-Pichel, F. and R.
Castenholz, 1993. The structure of scytonemin, an
ultraviolet sunscreen pigment from the sheaths of
cyanobacteria. Experientia 49: 825-829
Rastogi, R. P. and R. P. Sinha, 2009. Biotechnological and
industrial significance of cyanobacterial secondary
metabolites. Biotechnol. Adv. 27: 521-539
Rastogi, R. P., Singh, S. P., Hder, D.-P. and R. P. Sinha,
2010. Detection of reactive oxygen species (ROS) by
the
oxidant-sensing
probe
2,7dichlorodihydrofluorescein
diacetate
in
the
cyanobacterium Anabaena variabilis PCC 7937.
Biochem. Biophys. Res. Commun. 397: 603-607
Rastogi, R. P., Singh, S. P., Hder, D.-P. and R. P. Sinha,
2011. Ultraviolet-B-induced DNA damage and
photorepair in the cyanobacterium Anabaena
variabilis PCC 7937. Environ. Exp. Bot.74: 280-288

12

Phykos 42 (2): 1-13 (2012)

Phycological Society, India

Ross, C., Santiago-Va zquez, L. and V. Paul, 2006. Toxin

release in response to oxidative stress and
programmed cell death in the cyanobacterium
Microcystis aeruginosa. Aquat. Toxicol. 78: 66-73
Rozema, J. et al. 2002. The role of UV-B radiation in
aquatic and terrestrial ecosystems -an experimental
and functional analysis of the evolution of
UV-absorbing compounds. J. Photochem. Photobiol.
B: Biol. 66: 2-12
Schmid, D., Schrch C., Zllif, F., Nissen H. P. and H.
Prieur, 2003. Mycosporine-like amino acids: natural
UV-screening compounds from red algae to protect
the skin against photoaging. SFW J. 129: 1-5
Shick, J. M. and W. C. Dunlap, 2002. Mycosporine-like
amino acids and related gadusols: biosynthesis,
accumulation, and UV-protective functions in aquatic
organisms. Annu. Rev. Physiol. 64: 223-262
Singh, S. P., Klisch, M., Sinha, R. P. and D.-P. Hder,
2008. Effects of abiotic stressors on synthesis of the
mycosporine-like amino acid shinorine in the
cyanobacterium Anabaena variabilis PCC 7937.
Photochem. Photobiol. 84: 1500-1505
Singh, S. P., Klisch, M., Sinha, R. P. and D.-P. Hder,
2010a. Genome mining of mycosporine-like amino
acid (MAA) synthesizing and non-synthesizing
cyanobacteria: a bioinformatics study. Genomics 95:
120-128
Singh, S. P., Klisch, M., Sinha, R. P. and D.-P. Hder,
2010b. Sulfur deficiency changes mycosporine-like
amino acid (MAA) composition of Anabaena
variabilis PCC 7937: a possible role of sulfur in MAA
bioconversion. Photochem. Photobiol. 86: 862-870
Sinha, R. P., Kumar, H. D., Kumar, A. and D.-P. Hder,
1995. Effects of UV-B irradiation on growth, survival,
pigmentation and nitrogen metabolism enzymes in
cyanobacteria. Acta Protozool. 34: 187-192
Sinha, R. P., Dautz, M. and D.-P. Hder, 2001. A simple
and efficient method for the quantitative analysis of
thymine dimers in cyanobacteria, phytoplankton and
macroalgae. Acta Protozool. 40: 187-195.
Sinha, R. P. and D.-P. Hder, 2002. UV-induced DNA
damage and repair: a review. Photochem. Photobiol.
Sci. 1: 225-236
Sinha, R. P., Ambasht, N. K., Sinha, J. P., Klisch, M. and
D.-P. Hder, 2003. UV-B-induced synthesis of
mycosporine-like amino acids in three strains of
Nodularia (cyanobacteria). J. Photochem. Photobiol.
B Biol. 71: 51-58
Sinha, R. P., Kumar, A., Tyagi, M. B. and D.-P. Hder,
2005.
Ultraviolet-B-induced
destruction
of
phycobiliproteins in cyanobacteria. Physiol.Mol. Biol.
Plants 11: 313-319
Sinha, R. P., Singh, S. P. and D.-P. Hder, 2007. Database
on mycosporines and mycosporine-like amino acids

Effects of UV-B on cyanobacteria

(MAAs) in fungi, cyanobacteria, macroalgae,

phytoplankton and animals. J. Photochem. Photobiol.
B.Biol. 89:29-35
Sinha, R. P. and D.-P.Hder, 2008. UV-protectants in
cyanobacteria. Plant Sci. 174: 278-289
Sommaruga, R. and F. Garcia-Pichel, 1999. UV-absorbing
mycosporine-like compounds in planktonic a benthic
organisms from a high-mountain lake. Arch.
Hydrobiol. 144: 255
Sorrels, C. M., Proteau, P. J. and W. H. Gerwick, 2009.
Organization, evolution, and expression analysis of the
biosynthetic gene cluster for scytonemin, a
cyanobacterial UV-absorbing pigment. Appl. Environ.
Microbiol. 75: 4861-4869
Soule, T. et al. 2009. A comparative genomics approach to
understanding the biosynthesis of the sunscreen
scytonemin in cyanobacteria. BMC Genomics 10: 1-10
Tao, C., Sugawara, T., Maeda, S., Wang, X. and T. Hirata,
2009. Antioxidative activities of a mycosporine-like
amino acid, porphyra-334. Fish. Sc.74: 1166-1172
Weatherhead, E. C. and S. B. Anderson, 2006. The search
for signs of recovery of the ozone layer. Nature 441:
39-45

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