全 文 ：广 西 植 物 Guihaia 24(2)：166— 173 2004年 3月
紫球藻多糖浓度增加对其他逆境适应性的改变
刘晓灿1，Avigad Vonshak2
(1．广西师范大学生命科学学院 ，广西桂林 541004；2．本一古里安大学沙漠研究所 ，以色列 84990)
摘 要：紫球藻(Porphyridium sp．)是一种海水单细胞红藻，是多种天然产物的来源。在其培养繁殖过程
中，能够合成藻胆蛋白、高不饱和脂肪酸、硫酸酯多糖等生物活性物质，具有广阔的应用前景。盐胁迫会导致
紫球藻的结合态多糖浓度的增加，由此可能产生相应的耐盐性的提高，并有利于对其他逆境的适应。该项研
究采用外加紫球藻多糖或采用盐逆境诱导紫球藻多糖的积累，然后解除盐逆境的胁迫的方法获得多糖含量有
显著提高的紫球藻试材，再给与其他的逆境：如光抑制，低温处理，并测定主要的生理生化参数。试验结果表
明，外加0．05％紫球藻多糖的藻细胞光合效率，在光抑制条件下，低于不加多糖的对照，但在低温(4℃)时，高
于对照。外加多糖对 PsⅡ没有显著影响。紫球藻在去盐后的48 h恢复培养时间内，多糖的含量以及光抑制
和低温条件下的光合效率都逐渐恢复到对照的水平。但是，去盐恢复培养的紫球藻 PsⅡ效率在光抑制条件
下却高于加盐及未加盐的两种对照，显示盐诱导的紫球藻多糖可能增加了PsⅡ对光抑制的忍耐程度。
关键词 ：紫球藻 ；盐胁迫 ；多糖；光抑制；低温
中图分类号 ：Q945．78 文献标识码：A 文章编号：lOOO一3142(2004)02—0166—08
M odified responses of Porphyridium sp．cells
with an in,：reased 1)’ ’ ‘d level to stressc olysaccIiarl e V 0S cI
LIU Xiao—canI，Avigad Vonshak
(1．Colege D，L fe Sciences．Guangxi Normal University，Guilin 541004，China；
2．Microalgal B D￡，lef，lnDZDg，Laboratory，the Jacob Blaustein Institute for Desert
Research．Ben-Gurion University of the Negev，84990．Israe1)
Abstract：In this study，the responses of Porphyridium sp．cels with salt—elevated bound polysaccharide to the
stress of high proton flux density(HPFD)or chiling temperature(4℃ )was studied in order to evaluate pos-
sible biological roles of the induced polysaccha rides under environmental stresses．Addition of 0．05 polysac—
charides to the Porphyridium sp．culture caused the photosynthetic activity decreased under HPFD but in-
creased under chiling temperature(4℃)compared to control(culture without external addition of polysac—
charide)．The PSⅡ efficiency(Fv／Fm)decline was not significantly affected with the exogenous polysaccha—
ride．W ithin 48 h after removal of salt from the cultures，both photosynthetic activity of the salt pre-treated
cells measured under HPFD and chilling temperature(4℃)and bound polysaccharide content returned to the
levels of un-treated cels．However，the PS I efficiency of the recovery cultures measured under HPFD stil
kept at a higher level，especialy after 6 hours，compared with control and salt treated cultures，suggesting that
the high polysaccharide content induced by the salt stress may enhance PS I tolerance to high photon flux den—
sity．
Key words：Porphyridium sp．；salt stress；polysaccharide；photoinhibition；chiling temperature
Received date．2003_ 04-‘24 Accepted date：2003—-06—-23
作者简介：刘晓灿(1963～)，女，广西马山县人，壮族，硕士，讲师，从事生物化学及基因工程教学工作。
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2期 刘晓灿等：紫球藻多糖浓度增加对其他逆境适应性的改变 167
1 Intr0ducti0n
Porphyridium sp．ceils are attractive for bito—
technological purpose because they synthesize u—
nique cell wall sulfated polysacchrides，accessory
photosynthetic pigments (phycobilins and carote—
noids)．and essential fatty acids(Arad，2000，1999；
Berge et a1．，2002)．
The wall—like capsules of sulphated polysac—
charides around Porphyridium sp．ceils has a high
molecular mass of about 5～ 7×10 Da and is com—
posed of about 1 0 different sugars，among which
xylose，galactose and glucose are the main compo—
nents．It also contains some minor sugars，protein，
sulfate，and glucyronic acid．The]atter two confers
fl negative charge on the polysaccharide． These
polysaccharides are water soluble，highly viscous，
and resistant to biodegradation (Arad，2000)．Ra—
mus(1972)found that the capsules are thin in the
logarithmic phase and become thicker in the sta—
tionary phase．Accordingly to Ramus(1 9 7 2) the
rate of production of the polysaccharide is higher
than its rate of solubilization during the stationary
phase．Several functions have been suggested for
the capsular polysaccharides．The polysaccharides
have already been shown to exert biological activi—
ty；it has been found that polysaccharides of Por—
phyridium sp．are a good antioxidant (Ramus，
1 9 7 2) and exhibit antiviral activity against H er—
pes simplex viruses (H SV 1，2)(Huheihel et
nZ．，2002) and Varicella zoster virus (Huheihel
& Arad，2001)． Furthermore，they may provide
mechanical protection for the cell and form impen—
etrable barriers to gases and water and protect the
ceils from desiccation． They may also create a
buffer layer around the ceils to protect them from
extreme environmental conditions(Arad，2 0 0 0)．
In addition，the polysaccharide may also serve as
fin ion exchanger or fin ion reservoir(M ariani et
n￡．，1985；Ritehie & Larkam ，1982)． There—
fore。it is reasonable to speculate that increased
sulfated polysaccharides of Porphyridium sp．
may play fl role in cell protection against environ—
mental stresses．
Light is the ultimate source of energy that
drives photosynthesis． However，excess light can
also be harmful to the photosynthetic apparatus．
The efficiency of photosynthesis can be significant—
ly reduced when ceils are exposed to high light in—
tensity，particularly under adverse environmental
conditions (Barber 8L Andersson，1992；Kyle，
1987)．Photoinhibition is defined as a reduction in
photosynthetic efficiency due to damage caused by
photon flux densities above that photosynthesis is
saturated(Torzillo & Vonshak，1 998；Vonshak et
a1．，1996)． A general mechanism of photoinhibi—
tion can be summarized as follows：high irradiance
causes a marked increase in the turnover rate of Dl
protein。which is linked to the repair PSⅡ after it
has been damaged by photoinhibitory irradiation．
Photoinhibition is controlled by the balance be-
tween damage to D1 protein and recovery of D1
protein (Anderson et a1．，1997；Baroli& Melis，
1996：Tyystjarvi& Aro，1996)．For both phyto—
plankton and terrestrial plants，photodamage to PS
1 reaction centers can be detected with high sensi—
tivity from changes in variable chlorophyll fluores—
cence(Baker eta1．，1994；Bj6rkman，1987a，b；Long
P￡nZ．，1994；Neale，1987)． The ease with which
variable fluorescence measurements can be made
has led to their common usage as a tool to diagnose
for photoinhibition，although the consequence of PS
Ⅱ inactivation on photosynthetic electron flow re—
mains controversial(Anastasios，1 9 9 9)．
The most striking characteristic of red algae is
the presence of supplementary external antennae，
the phycobilisomes (PBSs) in addition to all the
functional elements needed for trapping and tras—
ducing light energy into chemical energy as in high—
er plants (Schirmer et a1．，1985，1986) Conse—
quently，in red algae energy is transferred，via phy—
coerythrin一> phycocyanin一> allophycocyanin to
PSII reaction centers through chromophores differ—
ently positioned along the transfer channel of PBS
rods(Talarico，1999)．
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168 广 西 植 物 24卷
In this study，we reported the effect of the in-
creased content of bound polysaccharides of Por—
phyridium sp．ceils on the photosynthetic activity
as well as the modified responses of those Porphy—
ridium sp．cells with increased polysaccharides to
HPFD and chilling temperature(4℃ )．
2 M aterials and M ethods
2．1 Preparation of Porphyridium sp．cultures with
salt elevated polysaccharides and their recovery culti-
vation after salt removal
Porphyridium sp．cultures all with 5 mg／L
chlorophyll fls an initial cell concentration in 100
mL of artificial seawater(Jones et a1．，1 963)with
or without 1．5 mol／L NaC1 were kept in 250 mL
shaken Erlenmeyer flasks and incubated at 24～ 25
℃．Air enriched with 1 9／6 CO2 was sparged into
the incubators． A bank of fluorescent lamps was
used as illumination source giving photon flux den—
sities(PFD)in the range of 100～ 110／~mol rrr。S- ．
Porphyridium sp．ceils grown in ASW+1．5 mol／L
NaC1 at optimal condition(25℃ ，light intensity of 100
～ 110／~molm 。S- )were harvested at log phase(8～ 10
／~g／mL of chlorophyll concentration)，washed twice
th ASW (50 mLX 2)，and then resuspended in fresh
medium ASW．Ceils were incubated in a shaker for 6。
12。48 h respectively．Meanwhile non-salt treated cells
were used as contro1．Then the cultures were exposed
to HPFD (high photon flux density)or chilling tem—
perature as described before (Xiaocan&Vonshak，
2003)．
2．2 Variable chlorophyll fluorescence
PSⅡ activity was determined following the
variable fluorescence parameters of Fo and Fm and
calculating the ratio of (Fm—Fo)／Fm — Fv／Fm
(Torzill& Vonshak，1994)．Algal samples were
incubated in the dark for 5 min to allow for ful
dark adaptation．Measurements were performed u—
sing the Plant Efficiency Analyzer (Hansatech，
UK)．
2．3 Addition of the exogenous polysaccharide into
non-stressed Porphyridium sp．cultures
W hen algal cells reached at log phase of
growth were harvested and resuspended in fresh
medium ASW with the addition of 2O mmol／L
NaHCO3 to final chlorophyll contents 5／~g／mL，
O．O5 po1ysaccharides isolated from Porphyridi—
um (kindly provided by Prof．Arad，Ben-Gurion U—
niversity of Negev，Israe1)were added．The same
cultures without addition of the externa1 polysac—
charides used as contro1．
2．4 Measurement of bound polysaccharide concen—
trations
The bound and water soluble polysaccharide of
Porphyridium sp．cells were separated and deter—
mined according to Dubois with the following mod—
ifications：the culture(5 mL)was centrifuged at
l O O00 rpm for 10 min．The pellets were used to
determine the bound polysaccharide content． The
pellets was washed with 7 mL of phosphate buffer，
pH7．5，and then centrifuged again．The superna—
tant was then discarded，and 10 mL of 1 N H2SO4
was added to the pellet．The mixture was kept in
the boiling water for 1 h．Then，25 mL of the mix—
ture and 975 mL distilled water were taken．1 mL
5 phenol and 5 mL 98 sulphuric acid were add—
ed and mixed wel1．After 3O min，the concentration
of bound polysaccharide was determined OD at 490
nm．A calibration curve was constructed with a se—
ries of concentrations of D-galactose．
3 Results
3．1 Stress‘modified responses of Porphyridium sp．
cells with increased polysaccharide level
In order to evaluate the role of the elevated
polysaccharide content in salt—-stressed Porphyrid—-
ium sp．cells two experimental approaches were
employed．One was to induce high polysaccharide
production by exposing the ceils to stress foflowed
by a recovery time that will restore the metabolic
activity of the cells． Another was to add external
polysaccharide to non-stressed Porphyridium sp．
cells assuming that we can somehow produce a
similar condition．
3．1．1 Non-stressed Porphyridiurn sp．culture with
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2期 刘晓灿等：紫球藻多糖浓度增加对其他逆境适应性的改变 169
the addition of external polysaccharides
Polysaccharides isolated from Porphyridiurn
were added to fl culture before exposing it to the
HPFD stress．W ith the addition of 0．05 external
polysaccharide to the Porphyridium sp．culture the
decline in the photosynthetic activity measured un—
der HPFD with time intervals proceeded faster and
reached to fl slightly lower level as compared to the
culture without the addition of polysaccharide
(Fig．1：A)．Interestingly the PS I efficiency(Fv／
Time tlmin
0
Fm)decline was not significantly affected(Fig．1：
B)．
However，when Porphyridium sp． culture
with the addition of 0．05 exogenous polysaccha—
rides was exposed to low temperature(4 ℃)the
decline in oxygen evolution rate was slightly higher
than the control(Fig．2：A)whereas there was no
significant difference in the PS I efficiency(Fv／
Fm)(Fig．2：B)between the cells with or without
the addition of external polysaccharide．
0．
0．
0．
Time tlmin
Fig．1 External polysaccharide on the oxygen evolution rate
(A)and maximal photochemical efficiency of PS I (Fv／Fm)I(B)of Porphyridium sp．cells under HPFD
0 10 20 30 40 50 60 70
Time in 4。C tlmin
Fig．2 External polysaeeharide
(A)and maximal photochemical efficiency of PSI (Fv／Fm)I(B)
3．1．2 Changes of pOlysaccharide content and pho—
tosynthetic parameters of Porphyridium sp．cells
recovered from salt stress
In order to study the modified responses of
salt treated cells with relatively high content bound
polysaccharide to light and chilling temperature
0
0 10 20 30 40 50 60 70
Time in 4。C t／m in
on the oxygen evolution rate
of PDr ^ 一diHm sp．cels under chiling temperature(4℃ )．
stresses，recovery experiments were designed as
described in the part of materials and methods．
Bound polysaccharide concentration，oxygen evolu—
tion rate and PS I efficiency were determined．
Increased bound p0lysaccharide concentration
and reduced photosynthetic activity and PS I effi—
O O O
暑-!I／
3 2 2 1 1
一，．q，-二3z0 Io昌1f
。_矗．I葺。 II_。 。葺。∞ 】【0
昌-!I／
O O O O O O O =2 伯 5
一 qI-oIqu N0 Io昌3
。_矗．I盘0一_昌一0 。盘。 Jc O
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17O 广 西 植 物 24卷
ciency of salt grown cultures recovered to the lev—
els of control cultures within 48 h after removing
salt stress．It should be noted that PSⅡefficiency
recovered faster than the oxygen evolution rate and
polysaccharide content(Table 4)．
3．1．3 Responses of salt pretreated Porphyridium
sp．with increased endogenous polysaccharide to
photoinhibition and chilling temperature(4 ℃ )
Salinity stress causes Porphyridium sp．ceils
to accumulate relatively high levels of bound poly—
saccharides．After removal of the salt stress，the
3
2
2
Time timin
O
Table 4 Time-course changes of bound polysaccharide
and photosynthetic activity of salt adapted Porphy-
ridium sp．cels after removing of salinity stress
*the values with the same letter in the same column have no sig—
nificant difference，p=0．05．
昌
、
昌
、
昌
、
Time timin
O
Fig．3 Effect of HPFD on PS I]efficiency(Fv／Fm)and oxygen evolution rate of Porphyridium sp．cells
with or without(as contro1)1．5 M NaCI recovered for 6，1 2，48 h after salt was removed
一．．ql-o互 H0 Io昌TI)
0 矗．I盘0罩薯一0 0 I10眦 】【0 ．^．q1．olIu 0一暑_3 矗I I0霉薯一0 0 I10咖 0 ．^ql-oIqu H0一宝暑 0_矗I盘0 _薯一0 0盘0咖 0
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2期 刘晓灿等：紫球藻多糖浓度增加对其他逆境适应性的改变 171
decline of photosynthetic activity of the salt pre—
treated cels under photoinhibition stress gradualy
returned to the level of control cells．But the PS I
efficiency was kept at a higher level，especially af—
ter 6 h，compared with control and salt treated cul-
tures，suggesting that the high polysaccharide con—
ter~t induced by the salt stress may enhance PS I
Timein4℃ tlmin
O
tolerance to high photon flux density(Fig．3)．
Similar to high light intensity，removal of salt
stress causes the decline of photosynthetic activity
as well as PS I efficiency of the salt pretreated
cells under chilling temperature stress to gradually
(within 48 h)return to the level of control cells
(Fig．4)．
O．6
O．5
量 0．4
O．3
O．2
O．1
O．6
O．5
o．4
O．3
O．2
O．1
O．6
O．5
量 0．4
O．3
O．2
O．1
O 1O 2O 3O 40 5O 6O 7O
Timein4C tlrain
Fig．4 Effect of 4℃ on the maximal PS I photochemical efficiency(Fv／Fm)of Porphyridium sp．cultures
grown with or without(as contro1)1．5 M NaCI recovered for 6，12，48 h after salt was removed
4 Discussion
It was found in our experiment that saline
stress induced accumulation of bound polysaccha-
ride in Porphyridium sp．cells as occurred under
nitrate and sulfate deficiencies(Arad，1992)．W hen
saline stress was removed，the bound polysaccha—
ride content started to decrease．M eanwhile，pho—
tosynthetic activity also gradually recovered． Our
一．-II_-0II10 N0_鸯 竹) 3矗I目召置一0 ∞目a盏 H0 一_ _-0Iq0 N0 10昌TI一 矗．I目0召暑_0 0目0 H0 一．-q_-0Iq0 N0 10昌TI一 矗I目譬置一0 0目＆ H0
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172 广 西 植 物 24卷
results showed further that the elevated polysac—
charide content induced by the salt stress seemed
to enhance PS 1 tolerance to high photon flux den—
sity．This indicated that the elevated polysaccha—
ride contents observed in Porphyridium sp．stress
cells modified responses of these cells to the
stress．The polysaccharides exist in fl typical gel
form ，which is fl stable net structure formed by fl
solution of polymers． They may create fl buffer
layer around the cells to protect them from extreme
environmental condition(Arad，2000)．
However，addition of 0．05 polysaccharide to
cultures had no significant effect to prevent the de—
crease of photosynthetic rate and the maximal pho—
tochemical efficiency of PS Ⅱ (Fv／Fm) under
HPFD (2 500 t*molm。S- )or chilling temperature
(4℃ )．Although in this experiment the prepara—
tion of polysaccharides added to the cultures was
derived from Porphyridium sp．cells themselves，
we still can be certain that the external polysaccha—
rides evenly dissolved in the cultures could not
function in the same way as do the salt—induced
bound polysaccharides encapsulating the cells．Mo—
reover，addition of external polysaccharide increa—
ses the viscosity of the medium ，which might cause
fl decrease in the diffusion coefficients of nutrients．
Rotem et a1．(1992) further proved that the
polysaccharide inhibits the rate of carbon uptake by
the cells and as fl result photosynthesis of cells is
also inhibited．
In conclusion，adaptation to increased concen—
tration of NaC1 modifies the response of Porphy—
ridium sp．to HPFD and chilling temperature stres—
ses． However，the relatively high 1evel of bound
polysaccharide of Porphyridium sp．cells induced
by salt stress can somehow enhance PS I1 tolerance
to high photon flux density．W e propose that the
bound po1ysaccharide of Porphyridium sp．cells
plays fl role in the modification of cells in stress．
Further work may be required in order to bet—
ter understand the correlation of the bound poly—
saccharide of Porphyridium sp．cells to fl modifica—
tion in PSI1．
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