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Effects of Solar UV Radiation on Photosynthetic Performance of The

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Algae 2014, 29(1): 27-34
http://dx.doi.org/10.4490/algae.2014.29.1.027
Open Access
Research Article
Copyright © 2014 The Korean Society of Phycology 27 http://e-algae.kr pISSN: 1226-2617 eISSN: 2093-0860
Effects of solar UV radiation on photosynthetic performance of the
diatom Skeletonema costatum grown under nitrate limited condition
Gang Li
1,2
and Kunshan Gao
1,
*
1
State Key Laboratory of Marine Environmental Science, Xiamen University, Xiamen, Fujian 361005, China
2
Key Laboratory of Tropical Marine Bio-resources and Ecology, South China Sea Institute of Oceanology, CAS, Guangzhou,
Guangdong 510301, China
Availability of nutrients is known to influence marine primary production; and it is of general interest to see how nutri-
ent limitation mediates phytoplankton responses to solar ultraviolet radiation (UVR, 280-400 nm). The red tide diatom
Skeletonema costatum was cultured under nitrate (N)-limited and N-replete conditions and exposed to different solar
irradiation treatments with or without UV-A (315-400 nm) and UV-B (280-315 nm) radiation. Its photochemical quantum
yield decreased by 13.6% in N-limited cells as compared to that in N-replete ones under photosynthetically active radia-
tion (PAR)-alone treatment, and the presence of UV-A or UV-B decreased the yield further by 2.8 and 3.1%, respectively.
The non-photochemical quenching (NPQ), when the cells were exposed to stressful light condition, was higher in N-lim-
ited than in N-replete grown cells by 180% under PAR alone, by 204% under PAR + UV-A and by 76% under PAR + UV-A +
UV-B treatments. Our results indicate that the N limitation exacerbates the UVR effects on the S. costatum photosynthetic
performance and stimulate its NPQ.
Key Words: diatom; N limitation; N repletion; photosynthesis; Skeletonema costatum; UVR
INTRODUCTION
Solar ultraviolet radiation (UVR, 280-400 nm) is a cru-
cial environmental factor to influence marine primary
productivity and consequently the marine ecosystems
(Häder 2011). UVR can decrease phytoplankton growth
and photosynthesis as well as nutrients uptake (Sobrino
et al. 2004, Gao et al. 2007a, Korbee et al. 2010), harm
DNA or protein molecules (Roy 2000, Wei et al. 2004) and
even lead to cell death (Agustí and Llabrés 2007), and
therefore, can alter community structures (Marcoval et al.
2008, Beardall et al. 2009). On the other hand, longer UV-A
wavebands (320-400 nm) are known to function in photo-
repairing the UV-B induced damages to DNA (Buma et al.
2003), trigger chlorophyll fluorescence (Halldal 1967) and
energize the photosynthesis of coastal phytoplankton
assemblages (Helbling et al. 2003, Mengelt and Prézelin
2005, Gao et al. 2007b, Li and Gao 2013).
Availability of nutrients is known to affect the photo-
synthetic responses of algae to UVR (Beardall et al. 2001,
2009). Nutrient limitation reduced the sensitivity of the
diatom Chaetoceros brevis to photo-induced viability loss
(van de Poll et al. 2005). A greater UV-A induced reduction
on the dimethysulfide production of the diatom Thalas-
siosira oceanica was observed under nitrate-limited con-
dition (Harada et al. 2009), as well as the reduced contents
of saturated fatty acids in the diatoms Phaeodactylum
tricornutum and Chaetoceros muelleri (Liang et al. 2006).
Received

September 17, 2013,

Accepted February 24, 2014
*Corresponding Author
E-mail: [email protected]
Tel: +86-592-218-7963, Fax: +86-592-218-7963
This is an Open Access article distributed under the
terms of the Creative Commons Attribution Non-Com-
mercial License (http://creativecommons.org/licenses/by-nc/3.0/) which
permits unrestricted non-commercial use, distribution, and reproduction
in any medium, provided the original work is properly cited.
Algae 2014, 29(1): 27-34
http://dx.doi.org/10.4490/algae.2014.29.1.027 28
MATERIALS AND METHODS
Organism and culture
The diatom Skeletonema costatum (Greville) Cleve
(strain 2042) was obtained from the algal species con-
versation center of Xiamen University and was grown
in sterilized artificial seawater at 20°C and 350 µmol
photons m
-2
s
-1
(~75 W m
-2
) photosynthetically active ra-
diation (PAR) irradiance (12 : 12 LD cycle). Two levels of
nitrate were set: 830 µmol L
-1
nitrate of the standard f/2
medium (N-replete, HN) and 0.83 µmol L
-1
(N-limited,
LN) of nitrate, the same f/2 medium with the nitrate re-
duced to be equivalent to the surface level of the South
China Sea (Li et al. 2012). The cells at mid-exponential
phase (Fig. 1) were diluted to 30,000-40,000 cells mL
-1

with fresh medium (LN or HN) in the evening before the
outdoor experiments started next morning.
Irradiance treatments and measurements
In the early morning (7:00 am) of August 4 and 8 of 2010,
both the diluted cultures (LN or HN) were dispensed into
500 mL UV-transparent quartz tubes that were incubated
in a flow-through water tank to control temperature (20 ±
0.5°C) and exposed to 3 irradiation treatments (triplicate
tubes for each nutrient level): a) uncovered quartz tubes,
the cells received full sunlight (PAR + UV-A +UV-B [PAB],
irradiances above 280 nm); b) quartz tubes wrapped in
Folex 320 (Montagefolie, No. 10155099; Folex, Dreieich,
Germany), the cells received PAR + UV-A (PA, irradiances
above 320 nm); and c) quartz tubes covered with Ultrap-
han film 395 (UV Opak; Digefra, Munich, Germany), the
cells received PAR alone (P, irradiances above 395 nm). The
transmission spectra of the tubes and filters are available
elsewhere (Sobrino et al. 2004). A radiometer (Eldonet
XP; Real Time Computers Inc., Möhrendorf, Germany)
was used to monitor the incident solar radiation; it mea-
sures every second of UV-B (280-315 nm), UV-A (315-400
nm), and PAR irradiance (400-700 nm) and records the
minute-averaged values (Häder et al. 1999). This device
has been regularly calibrated with a certified calibration
lamp (DH 2000; Oceanic Optics Inc., Dunedin, FL, USA).
The PAR irradiance was converted from W m
-2
to photon
flux (µmol photons m
-2
s
-1
) by multiplying by 4.60 accord-
ing to Neale et al. (2001).
Photophysiological parameter measurements
During the incubations (7:00 am to 18:00 pm), 5 mL
The increased UVR sensitivity of the dinoflagellates Gym-
nodinium sanguineum and Gymnodinium cf. instriatum
was also found under nitrate-limited conditions (Litch-
man et al. 2002), as well as the increased tolerance of the
dinoflagellates Heterocapsa sp. to UVR stress under ni-
trate replete conditions (Korbee et al. 2010). However, the
knowledge on the combined effects of UVR and nitrate
limitation has been scarcely documented, especially on
the photophysiology of diatoms.
The diatom Skeletonema costatum is distributed abun-
dantly and cosmopolitanly in the word’s oceans (Koois-
tra et al. 2008) and is well known as a typical species of
harmful algal blooms (Wang et al. 2008). Long-term UV-B
exposure increased its contents of carotenoids and UV-
absorbing compounds (Wu et al. 2009); short-term UV-B
exposure decreased its protein expression (Wei et al.
2004), but increased its competitive ability as compared to
the dinoflagellate Alexandrium tamarense and thus broke
their competition balance in growth (Zhang et al. 2007).
Nevertheless, this diatom showed a rapid acclimation to
solar UVR, even after having been maintained indoor for
decades under low UVR-free light condition (Guan and
Gao 2008). Since S. costatum is found in waters of varied
nitrate concentrations of e.g., from 0 to 12.3 μmol L
-1
in
the South China Sea (Ning et al. 2004), and little is known
about the combined effects of UVR and nitrate limitation
on its photochemical performance. Therefore, the aim of
this study was to examine the effects of solar UVR on the
photosynthetic performance of the diatom S. costatum
while growing under nitrate-limited and replete condi-
tions.
0
0
HN
LN
1 2
Time (days)
C
e
l
l
s

(
×
1
0
4
m
L
-
1
)
3 4 5
40
80
120
160
Fig. 1. Cell concentrations of Skeletonema costatum grown in N-
replete (HN) or N-starved (LN) conditions during the cultured period.
The arrow indicates that the culture was taken and diluted to 3-4
× 10
4
cell mL
-1
in the evening before the outdoor experiments next
morning. Vertical bars represent the standard deviations (n = 3).
Li & Gao Efects of UVR on Diatom
29 http://e-algae.kr
it indeed happens in natural conditions such as after ty-
phoon event (Li et al. 2009) or after heavy cloud covers
(Gao et al. 2007a) and so provides very useful information
to accomplish this study’s objective.
Data analyses
UV-A or UV-B induced inhibition of Y was calculated
as:
UV-B
Inh
= (Y
PA
- Y
PAB
) / Y
P
× 100%;
UV-A
Inh
= (Y
P
- Y
PA
) / Y
P
× 100%
, where UV-B
Inh
and UV-A
Inh
indicate UV-B and UV-A in-
duced inhibition; Y
PAB
, Y
PA
, and Y
P
indicate Y values of the
cells under PAB, PA, and P treatments, respectively.
To determine the significant differences (p < 0.05)
among three light treatments and between two nutrient
samples were taken every hour from each tube to deter-
mine the photosynthetic performance of S. costatum with
a pulse amplitude modulated fluorometer (Xe-PAM; Walz,
Effeltrich, Germany). Effective photochemical quantum
yield (Y) was determined by measuring the instant maxi-
mal fluorescence (F
m
′) and steady state fluorescence (F
t
)
of light-adapted cells, and calculated according to Genty
et al. (1990) as: Y = (F
m
′ - F
t
) / F
m
′. The non-photochemical
quenching (NPQ) was determined (van Kooten and Snel
1990) as NPQ = (F
m
- F
m
′) / F
m
′, where F
m
was the maxi-
mal fluorescence of dark-acclimated (overnight) cells ob-
tained prior to the outdoor exposure. The saturating pulse
was set at 4,800 µmol photons m
-2
s
-1
for 600 ms and the
actinic light at 350 µmol photons m
-2
s
-1
(~75 W m
-2
) for
the effective quantum yield measurement. We are aware
the effects of solar UVR could be exaggerated by shifting
the cells cultured indoor to the outdoor conditions, but
Fig. 2. (A) Representive incident solar photosynthetically active radiation (PAR, 400-700 nm), UV-A (315-400 nm), and UV-B (280-320 nm)
irradiances in W m
-2
. (B) Diurnal variations in efective quantum yield (Y). (C) Non-photochemical quenching (NPQ) of Skeletonema costatum cells
grown under nitrate (N)-limited condition (LN) and exposed to PAR + UV-A + UV-B (PAB, 280-700 nm), PAR + UV-A (PA, 320-700 nm), and PAR
(P, 400-700 nm), and their ratios to that of the cells grown under N-replete condition (HN). Vertical bars represent the standard deviations (n = 3).
0
06:00 12:00
Time (h)
09:00 15:00 18:00
0.2
0.3
0.4
0.5
I
r
r
a
d
i
a
n
c
e

(
W

m
-
2
)
Y

(
L
N
)
N
P
Q

(
L
N
)
0.6
0
0.7
100
300
200
400
PAR
PAB
PAB
PAB
PAB
UV-A
PA
PA
PA
PA
UV-B × 100
P
P
P
P 1
2
3
1.5
Y
H
N
/
Y
L
N
N
P
Q
H
N
/
N
P
Q
L
N
1.0
1.0
0.5
0.0
A
B
C
Algae 2014, 29(1): 27-34
http://dx.doi.org/10.4490/algae.2014.29.1.027 30
indicating a higher heat dissipation. UVR significantly in-
creased the NPQ (p < 0.05), by approximately 57% in LN
and 30% in HN-grown cells at noon (Fig. 2C).
When PAR intensity increased over 1,500 µmol pho-
tons m
-2
s
-1
(326 W m
-2
), the Y values decreased by approxi-
mately 60% as compared to the initials in LN grown cells
(Fig. 3A & B) with the presence of UV-A reducing the yield
by 2.2-21% and addition of UV-B further decreasing it by
6.0-24%, the total inhibition caused by UVR being 12 to
30%. The NPQ value reached 0.89 in LN-grown cells as the
PAR was over 1,500 µmol photons m
-2
s
-1
(326 W m
-2
), be-
ing elevated by 46 and 31% respectively by solar UV-A and
UV-B. The N limitation enhanced the NPQ by 180% un-
der PAR alone, by 204% under PA and by 76% under PAB,
compared to that in N repletion (Fig. 3C & D). Moreover, a
clear threshold of NPQ of LN-grown cells (Fig. 3C & D) oc-
curred when the PAR irradiance was ~230 µmol photons
m
-2
s
-1
(50 W m
-2
) ‒ one fourth of that in HN-grown cells,
providing evidence that the lower light energy is needed
to spike the NPQ under N-limited conditions.
Fig. 4 showed the relationships of the Y values, UV-A
and UV-B caused inhibition between LN- and HN-grown
cells. The LN-grown cells showed about 13% lower Y
values than that of HN-grown cells (Fig. 4A), and 24.4
and 21.4% higher inhibition caused by UV-A and UV-B,
treatments, paired-t test was used for the whole day’s
comparisons and one way-ANOVA was used for the each
time-point comparisons. Non-linear curve fit was used to
obtain the relationships between Y (or NPQ) and PAR ir-
radiance, whereas Kendall’s τ test was used to establish
the correlations of Y and UV inhibition between the HN
and LN treatments.
RESULTS
During a diurnal cycle of solar radiation (Fig. 2A), the
effective quantum yield (Y) decreased with increasing so-
lar radiation regardless of the radiation treatments with
or without UVR, to a minimum value at noon, and then
increased with decreasing solar radiation (Fig. 2B). The
cells grown under nitrate (N)-limited condition had a
relatively lower Y value than those under N-repletion e.g.,
0.44 in the early morning, that decreased to a minimum
of 0.29 at noon and almost completely recovered in the
late afternoon (Fig. 2B). The diurnal changes of NPQ dis-
played an opposite pattern to Y (Fig. 2C), with the higher
values in the presence of UVR than that in PAR alone (p <
0.01). In view of the NPQ ratios of HN to LN grown cells,
higher NPQ were found in the LN-grown cells (Fig. 1C),
0.7
2.4 2.4
0.7
PAB
PA
P
0.5
1.2 1.2
0.5
Y
N
P
Q
N
P
Q
Y
0.3
0.6 0.6
0.3
0.6
1.8 1.8
0.6
0.4 0.4
0.2
0.0 0.0
0.2
0
0
0
0
500
500
500
500
1,000
1,000
PAR (μmol photons m
-2
s
-1
) PAR (μmol photons m
-2
s
-1
)
1,000
1,000
1,500
1,500
1,500
1,500
2,000
2,000
2,000
2,000
A
C D
B
Fig. 3. Effective quantum yield (Y) (A & B) and non-photochemical quenching (NPQ) (C & D) of Skeletonema costatum cells grown under
N-limited (A & C) or N-replete (B & D) conditions and exposed to photosynthetically active radiation (PAR) + UV-A + UV-B (PAB, 280-700 nm), PAR
+ UVA (PA, 320-700 nm), and PAR (P, 400-700 nm) of overall two days experiments, as a function of PAR. Vertical and horizontal bars represent the
standard deviations (n = 3).
Li & Gao Efects of UVR on Diatom
31 http://e-algae.kr
diatoms use to attenuate the photoinhibitory oxidative
damage caused by light stress (Lavaud et al. 2007, Kor-
bee et al. 2010). The LN-grown cells had significantly (p <
0.01) higher NPQ and lower light to trigger NPQ, compa-
rable to the HN-grown ones (Fig. 3C & D); they could have
respectively (Fig. 4B & C), indicating the N limitation ex-
acerbated the UVR effects on the diatom photosynthetic
performance.
DISCUSSION
Grown under nitrate limited condition, the diatom S.
costatum exhibited lower effective quantum yields (Y)
and higher NPQ, as well as higher sensitivity to UVR in
contrast to that under N-replete condition. The PAR in-
tensity that initiated the NPQ of N-limited grown cells
was one fourth of that of N-replete grown ones. Light his-
tory would affect the photophysiological performances
of phytoplankton when being shifted from the indoor- to
outdoor-conditions, such as the S. costatum strain main-
tained in the laboratory for decades showed differential
responses to UV compared to the strain isolated from
coastal water (Guan and Gao 2008), and the Thalassio-
sira pseudonana showed differential photoinactivations
of photosystem II after acclimating to different light lev-
els (Li and Campbell 2013). In natural environments, the
light acclimation from very low to very high levels with
or without UVR also happens, such as that after typhoon
event (Li et al. 2009) or after heavy cloud covers for days
or during a diel cycle (Gao et al. 2007a), which would
cause the exaggerated photoinhibition of S. costatum by
solar PAR or UVR (Figs 2 & 3) although this diatom species
could rapidly acclimate to the field light conditions (Guan
and Gao 2008).
While S. costatum showed similar diurnal patterns of
both the yield and NPQ under sunlight to other phyto-
plankton species or communities (e.g., van de Poll et al.
2005, Marcoval et al. 2008), nitrate limitation decreased
its yield and increased its NPQ either in the presence or
absence of solar UVR (Figs 3 & 4). Higher availability of
nitrogen usually leads to less inhibition by stressful light
(Litchman et al. 2002, Korbee et al. 2010, Loebl et al. 2010),
since the repair of photodamage can be better achieved
with more N-requiring enzymes and / or protein cofac-
tors (Roy 2000, Beardall et al. 2001). Other enzymes such
as peroxidase and catalase, that also need N, and can de-
toxify UVR-induced reactive oxygen species (Lesser 1996)
and might also be responsible for the smaller UVR effects
under N replete conditions.
The threshold of light intensity that triggers the NPQ
in LN-grown cells was one-fourth of that of HN-grown
cells (Fig. 3C & D). The NPQ, an important strategy for
phytoplankton to rapidly (seconds to minutes) regulate
photochemistry, is one of the first lines of defense that
Fig. 4. Effective quantum yield (A), UV-A induced (B), and UV-B
induced (C) inhibition on Skeletonema costatum cells grown under N-
limited condition (LN) versus that of the cells grown under N-replete
condition (HN). The bold lines show significant relationships, with
r
2
of 0.93 for YP, 0.26 for UV-A and 0.47 for UV-B inhibition (p < 0.01),
respectively. Vertical and horizontal bars represent the standard
deviations (n = 3). rA = 0.92912, p < 0.0001; rB = 0.5074, p = 0.00219;
rC = 0.68274, p < 0.0001.
0.8
30
30
0.8
20
20
30
30
0.6
20
20
Y
P

(
L
N
)
U
V
-
A

i
n
h
i
b
i
t
i
o
n

(
%
)

(
L
N
)
U
V
-
B

i
n
h
i
b
i
t
i
o
n

(
%
)

(
L
N
)
YP (HN)
0.6
10
10
UV-A inhibition (%) (HN)
UV-B inhibition (%) (HN)
0.4
10
10
0.4
0
0
0.2
0
0
-10
-10
0.2
-10
-10
A
C
B
Algae 2014, 29(1): 27-34
http://dx.doi.org/10.4490/algae.2014.29.1.027 32
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dissipated the excessive energy more effectively under
stressful light condition, thus protecting the cells from
photoinhibition and maintaining their photosynthetic
activity. The field measurements of NPQ by Kashino et al.
(2002) and Fujiki et al. (2003) also indicated that the NPQ
process is of importance to maintain the photosynthetic
activity of phytoplankton. On the other hand, the sub-
stances, that need N for their synthesis, e.g., UV-screen-
ing compounds like mycosporine-like amino acids were
recorded to increase with increasing nitrogen levels (Li-
tchman et al. 2002, Korbee et al. 2010, Barufi et al. 2011)
and might also attribute to the higher UVR sensitivity in
LN- than in HN-grown cells.
The diatom grown under N-limited condition exhibit-
ed higher sensitivity to UVR than that grown under N-re-
plete condition, based on the changes in the photochem-
ical quantum yield and NPQ, which indicates that the N
limitation exacerbates the effects of UVR on its photosyn-
thetic performance and stimulate its NPQ. Presently, the
increased global temperature has directly and indirectly
altered the natural conditions of aquatic bodies, e.g., in-
creasing the stratification of surface ocean and making it
more oligotrophic (Boyd et al. 2010). Taking into account
the worldwide oligotrophic oceans wherein the growth of
phytoplankton is limited and the limitation could be ex-
acerbated by the decreased nutrient levels within the up-
per mixed layer; the negative effects caused by solar UVR
would be exacerbated, making phytoplankton cells more
sensitive to ambient UVR stress.
ACKNOWLEDGEMENTS
We would like to thank the comments of the two anon-
ymous reviewers that helped to improve this manuscript.
This study was supported by the National Natural Science
Foundation (40930846, 41120164007, 41206132), Pro-
gram for Changjiang Scholars and Innovative Research
Team (IRT_13R51), China-Japan collaboration project
from MOST (S2012GR0290), Special Research Fund for
the National Non-profit Institutes (2008M15) and MEL
Visiting Fellowship Program (MELRS1006). The authors
are grateful to Ying Zheng, Guang Gao, Guangyan Ni, Kai
Xu, Guiyan Yang and Peng Jin for their experimental as-
sistance.
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