Ind J Plant Physiol.
DOI 10.1007/s40502-014-0084-9
ORIGINAL ARTICLE
Effect of UV-B radiation on photosystem II functions in Antarctic
and mesophilic strains of a green alga Chlorella vulgaris
and a cyanobacterium Synechocystis salina
Emilia L. Apostolova • Irina Pouneva •
Georgi Rashkov • Kolyo Dankov • Irena Grigorova
Amarendra N. Misra
Received: 27 March 2014 / Accepted: 20 May 2014
Ó Indian Society for Plant Physiology 2014
Abstract The green alga Chlorella vulgaris and the
cyanobacterium Synechocystis salina cells isolated from
Antarctic and mesophilic environments, grown in batch
cultures under continuous visible light, were used to assess
the effect of the UV-B radiation on the photosystem II
(PSII). UV-induced changes in its functional activity were
estimated by Pulse Amplitude Modulated chlorophyll
fluorescence and oxygen evolution (measured with oxygen
rate electrode). The data reveal a relatively stronger UV-B-
induced inhibition of oxygen evolution in comparison to
that of the primary photochemistry of the PSII in both
green algae and cyanobacteria. The inhibition of oxygen
evolution was a result of the decrease in the number of
functionally active PSII centers. The modification of active
reaction centers was also recorded through the relatively
more effect on fast operating PSII centers than that of the
slow operating PSII centers. On the other hand, the PSII
activity of cyanobacteria was more vulnerable to UV-B
radiation than that of green algae. Likewise, the mesophilic
strain of S. salina was more susceptible to UV-B radiation
than the Antarctic isolates.
E. L. Apostolova (&)
G. Rashkov
K. Dankov
Institute of Biophysics and Biomedical Engineering, Bulgarian
Academy of Sciences, Acad. G. Bonchev Str., Bl. 21, 1113 Sofia,
Bulgaria
e-mail: emya@bio21.bas.bg
I. Pouneva
I. Grigorova
Institute of Plant Physiology and Genetics, Bulgarian Academy
of Sciences, Acad. G. Bonchev Str., Bl. 21, 1113 Sofia, Bulgaria
A. N. Misra
Centre for Life Sciences, School of Natural Sciences, Central
University of Jharkhand, Ratu-Lohardaga Road, Brambe,
Ranchi 435205, Jharkhand, India
•
Keywords Cyanobacteria
Green algae
Photosynthetic
oxygen evolution
Photochemistry of the photosystem II

UV-B radiation
Introduction
The depletion of the stratospheric ozone layer allows more
UV-B radiation to reach the Earth’s surface and to a sig-
nificant depth in the ocean (Smith et al. 1992; Häder et al.
1998, 2007; Singh et al. 2011). All aquatic organisms
appear to be susceptible to UV-B, but to a different degree
(Sinha and Häder 2002). UV radiation can cause a wide
range of genetic and cytotoxic effects in these organisms.
Lipids, proteins and DNA are the main targets of UV-B
action directly through photochemical reactions or indi-
rectly by the generation of reactive oxygen species (ROS)
(He and Häder 2002; Bhandari and Sharma 2011).
The process of photosynthesis is most sensitive to UV-B
induced damage in higher plants, algae and cyanobacteria.
The most sensitive target of UV radiation to photosynthesis
is the photosystem II (PSII) complex (Vass et al. 1999,
2005; Vass 2012). Among all the chloroplast proteins, the
light-harvesting pigment-protein (LHC) complexes are
most affected by UV-B induced damage (Lao and Glaser
1996; Vass et al. 2005; Vass 2012). The primary light
harvesting antenna of PSII is the chlorophyll a/b protein
complex in plants and green algae (Kouril et al. 2012),
while that in cyanobacteria is phycobilisomes (PBS)
(MacColl 1998; Maksimov et al. 2011). Phycobilisomes
are large pigment-protein assemblies attached to the outer
surface of thylakoid membranes, their composition is
species specific, and depends on the environmental light
quality (Bald et al. 1996). The PBS complex has significant
UV-B absorbing components and so is one of the targets
123

for UV-B damage (Sah et al. 1998). This affects the
function of the photosynthetic apparatus in cyanobacteria.
Investigations with the cyanobacterium, Synechocystis sp.
PCC 6083, revealed that UV-B radiation caused a depletion
of plastoquinone pool as well as a perturbation and deg-
radation of the D1 protein (Giacometti et al. 1996). The
potential targets of UV-induced damage in PSII are pro-
posed to be the quinone electron acceptors (QA and QB),
the catalytic Mn clusters in the oxygen evolving complex
(OEC) and tyrosine (Tz) electron donors in PSII (Vass
et al. 2005; Vass 2012). The earliest detected step of UV-
induced damage is shown to be the release of a Mn ion
from the OEC (Hakala et al. 2005).
The photosynthetic pigments can act as photosensitizers
and produce ROS under an excess UV and/or visible light
(Aro et al. 1993; Rinalducci et al. 2006; Triantaphylide and
Havaux 2007). Enhanced UV-B generally decreased the
chlorophyll content and inhibited the photosynthesis,
resulting in lower biomass production in algae and cya-
nobacteria (Xue et al. 2005; Abo-Shady et al. 2008; Sheeba
et al. 2011; Bhandari and Sharma 2011). During evolution,
algae and cyanobacteria have developed several strategies
for avoidance, protection and repair mechanisms against
the detrimental effect of UV-B (Xue et al. 2005; Lao and
Glaser 1996; Abo-Shady et al. 2008; Rastogi and Inch-
aroensakdi 2013). There are extensive reviews on the
molecular mechanism of UV radiation on various photo-
synthetic organisms (He and Häder 2002; Vass et al. 2005;
Häder et al. 2007).
Despite many studies on the effects of the UV radiation
on photosynthetic organisms, still limited knowledge is
available on the effects of UV-B radiation on the green
algae and cyanobacteria. These organisms are important in
the aquatic ecosystem, because they are major components
of the photosynthetic biomass and are valuable sources of
natural products (Xue et al. 2005; Shukla et al. 2008;
McQuaid et al. 2011). The environmental stress responses
are species specific, and so these differences could be one
of the important factors to assess the potentially damaging
effects of the increases in UV-B radiation on different
species in the ecosystem (Estevez et al. 2001; Figueroa
et al. 2003; Juneau et al. 2001). In the present study, we
investigated the sensitivity to UV-B radiation on a pro-
karyotic photosynthetic cyanobacterium and a eukaryotic
green alga. It is well known that Antarctic organisms are
subjected to high UV radiation because of the ozone hole
over Antarctica. On the other hand, these organisms are
tolerant to a wide range of temperature regimes within their
growth environment (Pandey et al. 2004). The Antarctic
organisms are characterized by higher amount of carote-
noids and phycocianin in comparison to the tropical iso-
lates (Shukla and Kashyap 2003). We studied the
cyanobacterium Synechocystis salina and the green alga
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Ind J Plant Physiol.
Chlorella vulgaris cells, collected from the Antarctic and
mesophilic waters. The effect of UV-B radiation was
studied by monitoring the changes in the photochemistry of
PSII and photosynthetic oxygen evolution of both species,
which may be used for assessing the biological impact of
UV-B radiation on evolutionarily diverse organisms orig-
inating in different ecosystems.
Materials and methods
Organisms and growth conditions
The Antarctic cyanobacterium S. salina and the green alga
C. vulgaris were isolated from moss and soil samples,
respectively, from Livingston Island, the South Shetland
Archipelago. The mesophilic S. salina and C. vulgaris were
obtained from the Culture collection of autotrophic
organisms (CCALA) at the Institute of Botany, Academy
of Sciences of the Czech Republic.
The cyanobacteria and green algal strains were culti-
vated in batch cultures for 5 days before treating with UV-
B radiation. The nutrient (1 N) medium as described by
Setlik (1967) and modified by Georgiev et al. (1978) was
used for both the Antarctic and mesophilic strains of C.
vulgaris. Twice diluted (0.5 N) medium of Pekárková et al.
(1988) supplemented with NaNO3 1.26 g l-1, NaHCO3
3.0 g l-1 and C10H14N2O8
2H2O 200 mg l-1 was used for
the Antarctic and mesophilic strains of S. salina. All strains
were cultivated aseptically in 200 ml glass vessels, under
continuous illumination of white light with intensity of
180 lmol m-2 s-1 and aerated 100 l m-3 h-1 of air enri-
ched with 2 % CO2. Growth of the culture was monitored
by the measurement of cell density determination by
spectrophotometry. Sampling was done for UV-B treat-
ment when the cells were in the mid point of the log growth
phase with an optical density (OD) 0.7 at 760 nm. In our
experiment this phase was reached on the 5th day of the
culture.
UV-B treatment
Two Phillips (TL 20 W/12 RS SLV) tubes with a peak
emission at 312 nm were used for UV-B irradiation. On the
5th day, 3 ml of cells in the mid log phase, as described
above, were placed in an open sterile Petri dishes (dia
140 mm), and were subjected to UV-B irradiation for
60 min. Sampling was done at 0, 15, 30 and 60 min after
UV-B exposure to study the photosynthetic parameters. A
magnetic stirrer gently agitated the suspension to ensure
uniform exposure to UV radiation. The intensity of the
radiation was 7.5 W m-2, as measured with a power meter
‘‘OPHIR – Nova II Display Rohs’’ (Israel). The cell density
Ind J Plant Physiol.
was kept constant to 5 lg chlorophyll per ml for cyano-
bacteria and 12 lg chlorophyll per ml for green algae.
Chlorophyll fluorescence
The chlorophyll fluorescence was recorded with a Pulse
Amplitude Modulated (PAM) fluorometer (model PAM
101-103, Heinz Walz, Effeltrich, Germany). The cells were
dark adapted for 20 min. The F0 level was measured at an
instrument frequency of 1.6 kHz and a measuring beam set
at 0.06 lmol m-2 s-1 PFD. The maximum fluorescence
level (Fm) was measured by illuminating the sample with
saturating flashes of 2000 lmol m-2 s-1 PFD of 0.8 s
provided by a Schott lamp KL 1500 (Schott Glaswerke,
Mainz, Germany). The maximum quantum yield of pri-
mary photochemistry was derived by the equation Fv/
Fm = (Fm-Fo)/Fm (Kitajima and Butler 1975). Each
experiment was replicated 5 times.
Oxygen evolution measurements
The photosynthetic oxygen evolution (flash oxygen evo-
lution and oxygen evolution under continuous illumina-
tion) was measured using a custom-built polarographic
oxygen rate electrode (Joliot-type) as described by Zeina-
lov (2002). During the measurements the cells formed a
2 mm layer on the electrode. Samples were preilluminated
with 25 flashes and then dark adapted for 5 min before
measurements. Oxygen flash yields were induced by satu-
rating (4 J) and short (t1/2 = 10 ls) periodic flash
sequences with 650 ms dark intervals between the flashes.
The initial oxygen burst was recorded after irradiation with
continuous white light (450 lmol photons m-2 s-1). The
measurements were carried out without electron acceptors.
For assessing the effect of the UV-B radiation on the
oxygen evolution we used the following parameters: A—
the amplitude of the oxygen burst under continuous illu-
mination, which correlate with the number of the func-
tionally active PSII centers; Y4—the amplitude of the
oxygen evolution after the four flash was used for evalu-
ating the effect of the UV-B on the flash oxygen evolution;
Y4/Y3, which correlates with the ratio of the PSII centers in
S0 to S1 states. These parameters are good indicators of
changes in the oxygen evolution due to structural modifi-
cations and damage to the photosynthetic apparatus under
stress (Apostolova et al. 2006; Dankov et al. 2009; Ivanova
et al. 2008; Dobrikova et al. 2013). Data are from five
independent experiments.
Statistical analysis
The statistical differences between the means were deter-
mined using a two-tailed paired Student’s t-test. Values of
P\0.05 were considered as significantly different between
the fluridone treated samples and the untreated sample.
Results
The chlorophyll-a fluorescence parameters were studied to
estimate the effect of UV-B radiation on the quantum
efficiency of primary photochemistry of PSII in S. salina
and C. vulgaris. The maximum quantum yield of primary
photochemistry in dark-adapted state (Fv/Fm ratio) was
higher in the mesophilic strain of Chlorella than the Ant-
arctic isolates, while Fv/Fm ratio was similar in both the
strains of S. salina (Fig. 1). UV-B induces inhibition in the
photochemistry of PSII in all the strains and the deleterious
effect increased with the duration of irradiance (Fig. 1).
The Fv/Fm ratio of both mesophilic and Antarctic strains of
Chlorella was 32–35 % lower after 60 min treatment with
UV-B radiation compared to the respective control values
(Fig. 1). Unlike the green algae, the sensitivity of both the
cyanobacterial strains to UV-B was very high. The UV-B
treated mesophilic Synechocystis showed 80 % inhibition
in the photochemistry of PSII compared to that of 60 % in
the Antarctic strain (Fig. 1), which suggests an increased
sensitivity of the mesophilic strain compared to that of the
Antarctic strain of Synechocystis. The lower value of Fv/Fm
ratio in the strains of S. salina compare to that of C. vul-
garis (Fig. 1), could be a result of the contribution of PBS-
pigment fluorescence that might have elevated the F0 value
resulting in a reduced Fv/Fm ratio in the cyanobacterium
(Campbell et al. 1998). Comparison of the susceptibility of
four examined strains to the harmful effect of UV-B
reveals that Synechocystis isolates from mesophilic envi-
ronment are the most affected (Fig. 1).
In order to get more detailed information on the UV-B
induced inhibition of photosynthesis, photosynthetic oxygen
evolution was measured by an oxygen rate polarographic
electrode. The values of oxygen flash yields after fourth flash
(Y4) and the amplitudes of the oxygen burst under continuous
irradiation (A) were used to assess the effect of UV-B radia-
tion on the oxygen evolution. The amplitude of the oxygen
burst (A) corresponds to the number of functionally active
PSII centres (Zeinalov 2009, 2010), i.e., fast and slow oper-
ating centers (Dobrikova et al. 2013).
The typical induction curves of oxygen evolution under
continuous illumination of Chlorella and Synechocytis
cells before and after UV-B treatment are shown in Fig. 2.
An inhibition of the initial oxygen burst after treatment
with UV-B radiation in all the four studied strains indicates
suppression of the oxygen evolution as a result of the
decrease in the functionally active PSII centers (Table 1).
The inhibition of the oxygen evolution could be a result of
an impaired electron transport from the Mn clusters of the
123

Fig. 1 The time course of the
UV-B induced changes in
maximum quantum yield of
primary photochemistry (Fv/Fm)
of S. salina (a) and C. vulgaris
(b). Data are mean ± SE of five
independent experiments.
Asterik mark shows significant
differences between control and
UV treated cells
oxygen evolving complex to Tyr-Z? and P680? by UV-B
light (Vass et al. 1999) and depends on the duration of
treatment (Table 1). However, there were differences in the
inhibition of four strains. The amplitude of the oxygen
burst (A) decreased by about 60 % in both mesophilic and
Antarctic Chlorella cells (Table 1). The effect of UV-B
radiation was more pronounced in the cells of mesophilic
Synechocystis strain. The oxygen evolution after 30 min
exposure to UV-B in this strain was completely inhibited,
while that of the Antarctic Synechocystis strain was
inhibited up to 85 %. A stronger inhibition of oxygen
evolution by UV-B irradiation in the cells of mesophilic
Synechocystis was in accordance with the inhibition of PSII
photochemistry in this strain (Fig. 1).
The flash oxygen evolution in all studied cells showed a
characteristic sequence with the highest oxygen evolution
after four flash (Y4). The oxygen evolution during flashes was
more affected by UV-B radiation than the oxygen evolution
under continuous illumination (Table 1) in all strains, which
suggests stronger UV-B effect on the fast operating centers
(centers evolving oxygen by the Kok’s non-cooperative
mechanism) of oxygen production. Our earlier investigations
have revealed that UV-A radiation also leads to a damage of
fast operating PSII centers in higher plants (Ivanova et al.
2008). However, the effect of UV-B on the flash oxygen
evolution was stronger in Synechocystis than in Chlorella. The
effect was similar (about 80 % inhibitions after 60 min of
irradiation) in both strains of Chlorella (Table 1). Compara-
tively the mesophilic strain of Synechocystis was more
affected by UV-B than the Antarctic strain (Table 1). A
complete inhibition of flash oxygen evolution was observed in
123
Ind J Plant Physiol.
the mesophilic Synechocystis after 30 min of illumination
with UV-B, while the inhibition was to 80 % (of control value)
in the Antarctic strain.
UV-B radiation also affected the ratio Y4/Y3 (Table 1).
Analysis of the flash oxygen evolution showed differences in
Si state distribution among control and UV-B treated cells. It is
known that the water oxidation is catalysed by Mn clusters
passing through five oxidation states termed S0 to S4. In the
dark S0 and S1 states are stable. The Y4/Y3 ratio, correspond to
the S0/S1 ratio. This was higher than 1 in untreated cells in all
the strains, which can be explained by the higher S0 than the S1
population of PSII centers in darkness (Table 1). The Y4/Y3
ratio was higher in the mesophilic representatives of both
species, which suggests differences in the distribution of S
states in the oxygen evolving complexes among the meso-
philic and Antarctic strains. This modification might influence
the number of functionally active PSII centres, resulting in the
different amplitude in the initial oxygen burst (Fig. 2). The
results show that after UV-B irradiation the Y4/Y3 ratio
increased by 30 and 40 %, respectively in mesophilic and
Antarctic strains of Chlorella, but that decreased in the Syn-
echocystis (Table 1).
Discussion
UV-B induces structural changes in both algal cells (Juan
et al. 2005) and cyanobacteria (Wu et al. 2005). In addition
UV-B damages the primary and secondary quinone elec-
tron acceptors, Mn clusters of OEC, tyrosine (Tz) electron
donors (Vass et al. 2005; Vass 2012), and light harvesting
Ind J Plant Physiol.

Fig. 2 The initial oxygen bursts

(induction curves) on
continuous illumination of
(a) Antarctic C. vulgaris;
(b) mesophilic C. vulgaris;
(c) Antarctic S. salina and
(d) mesophilic S. salina. (1)
untreated cells; (2) after 60 min
of UV-B treatment. The curves
are representative. The arrows
indicate the turn on uparrow
and turn off downarrow of the
light

complexes (Thornber 1975; Bhandari and Sharma 2011).
These effects could influence the PSII functions as depicted
in Fig. 1 and Table 1, which is the primary target of UV
radiation. Comparative analysis showed that the UV-
induced inhibition of PSII photochemistry is much stronger
in S. salina than in C. vulgaris (Fig. 1). This difference
between species could be due to the significant absorption
of UV-B by cyanobacterial PBS complex (Sah et al. 1998;
Six et al. 2007) that causes deleterious effects in the light
harvesting antenna of PSII and thus, retard the energy
transfer in the complex (Apostolova et al. 2010). It has
been shown that phycocyanin was bleached more rapidly
and drastically than any other photosynthetic pigments
(Sinha et al. 2001). Moreover, UV-B radiation leads to a
partial uncoupling of PBS from the PSII core complex (Lao
and Glaser 1996; Sah et al. 1998; Rinalducci et al. 2006;
Apostolova et al. 2010) and altered the energy transfer
efficiency of phycocyanine to PSII reaction centres (Zee-
sham and Prasad, 2009). All these changes taken together
suggest a relatively stronger effect of UV-B on the pho-
tochemistry of PSII in the cyanobacteria, which was greater
in the mesophilic Synechocystis than the Antarctic isolates.
The decreased amount of carotenoids in mesophilic strain
in comparison to the Antarctic one is the most probable
reason for the different UV sensitivity of the both strains
(unpublished results). These data corroborate with the
results of Shukla and Kashyap (2003) for different carot-
enoid in Antarctic and tropical strains of cyanobacteria.
Two parallel mechanisms, non-cooperative and coop-
erative mechanisms were suggested to explain the process
of the oxygen production at PSII (Apostolova et al. 2006;
Zeinalov 2005, 2009, 2010; Dobrikova et al. 2013). It was

123
 Ind J Plant Physiol.

Table 1 The effect of UV-B radiation on photosynthetic oxygen was observed (Table 1). Also, S0 population in green algae
evolution of C. vulgaris and S. salina, isolated from Antarctic and increased under UV-B irradiation (Table 1). These changes
mesophilic environments
are similar to that in the photosynthetic apparatus of the
UV-B treatment Parameter Time higher plants after UV treatment (Ivanova et al. 2008). To
0 15 30 60 the contrary, the amount of the S0 state in cyanobacteria
decreased under UV-B irradiation. This contrasting effect
Antarctic A[%] 100 68 ± 7 58 ± 6 36 ± 5 of the UV-B on the S0–S1 state distribution in green algae
Chlorella Y4[%] 100 57 ± 6 35 ± 4 16 ± 4 and cyanobacteria could be due to the differences in the
Y4/Y3 1.20 1.29 1.33 1.67 organization of the OEC in these two organisms.
Mesophilic A[%] 100 80 ± 9 62 ± 6 39 ± 4 In conclusion, these data showed that UV-B induced
Chlorella Y4[%] 100 60 ± 7 34 ± 5 22 ± 3 inhibition of the photosynthetic oxygen evolution and the
Y4/Y3 1.42 1.75 1.80 1.84 photochemistry of PSII (lower Fv/Fm ratio) in green algae
Antarctic A[%] 100 87 ± 6 43 ± 4 15 ± 4 and cyanobacteria (Table 1; Fig. 1) was due to the both the
Synechocystis Y4[%] 100 58 ± 5 20 ± 4 – donor and acceptor side modifications of PSII. The inhi-
Y4/Y3 1.35 1.15 0.85 – bition of oxygen evolution was more pronounced in com-
Mesophilic A[%] 100 51 ± 5** 34 ± 3* – parison to the PSII photochemistry of both the
Synechocystis Y4[%] 100 41 ± 4* – – cyanobacteria and the green algae, which suggested a
Y4/Y3 1.57 1.00 – – stronger UV-B damage on the donor side of PSII complex.
The data are mean value, ± SE of five independent experiments.
The inhibition of oxygen evolution could be a result of the
There were non-significant differences between the samples from decrease in the centers evolving oxygen by both coopera-
Antarctic and mesophilic origin of C. vulgaris. Asterik mark shows tive and non-cooperative mechanisms (i.e., fast and slow
significant differences between UV-B induced changes of Antarctic operating centers), but the effect was more pronounced for
Synechocystis in comparison to the mesophilic Synechocystis
the fast operating centers, which released oxygen by non-
A amplitude of the oxygen burst under continuous illumination, Y3
cooperative mechanism. Comparing the sensitivity of the
and Y4 amplitudes of the oxygen evolution after third and fourth
flashes, respectively PS II photochemistry to UV-B radiation, in Synechocystis
** P \ 0.01, * P \ 0.05 and Chlorella, it was observed that the cyanobacteria were
more susceptible than the green algae. Moreover, the S.
salina cultures, isolated from mesophytic strain are more
supposed that the cooperative mechanism involves sensitive to the UV-B radiation than those of Antarctic
recombination of oxygen precursors, obtained from dif- origin, suggesting a quicker adaptive response of the Ant-
ferent oxygen evolving centers and realized by the slow arctic cyanobacterium to UV radiation compared to that of
operating PSII centers. It was characterized by a slower the mesophilic strains.
rate constant than the rate constant of the centers evolving
oxygen by non-cooperative Kok’s mechanism, which was Acknowledgments This article is the result of cooperation under
realized by the fast operating PSII centers (Zeinalov 2005; Bulgarian-Indian Inter-Governmental Programme of Cooperation in
Science and Technology, project BIn-01/07 of the National Science
Dobrikova et al. 2013). The oxygen burst under continuous Fund of Bulgaria and project Grant No. INT/BULGARIA/B70/06 by
illumination provides information about the PSII centers Department of Science & Technology, Govt. of India.
operating by the both mechanisms, while the oxygen
evolution under flash irradiation is generated mainly by the
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