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Longitudinal Photosynthetic Gradient in Crust Lichens'
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Article in Microbial Ecology · January
2014
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SOIL MICROBIOLOGY
Longitudinal Photosynthetic Gradient in Crust Lichens’
Thalli
Li Wu & Gaoke Zhang & Shubin Lan & Delu Zhang
&Chunxiang Hu
Received: 10 September 2013 /Accepted: 6 January 2014 /Published
online: 30 January 2014# Springer Science+Business Media New York
2014
Abstract In order to evaluate the self-shading protection
forinner photobionts, the photosynthetic activities of three
crustlichens were detected using Microscope-Imaging-PAM. Thefalse
color images showed that longitudinal photosyntheticgradient was
found in both the green algal lichen Placidiumsp. and the
cyanolichen Peltula sp. In longitudinal direction,all the four
chlorophyll fluorescence parameters Fv/Fm, Yield,qP, and rETR
gradually decreased with depth in the thalli ofboth of these two
lichens. In Placidium sp., qN values de-creased with depth, whereas
an opposite trend was found inPeltula sp. However, no such
photosynthetic heterogeneitywas found in the thalli ofCollema sp.
in longitudinal direction.Microscope observation showed that
photobiont cells arecompactly arranged in Placidium sp. and Peltula
sp. whileloosely distributed in Collema sp. It was considered that
thelongitudinal photosynthetic heterogeneity was ascribed to
theresult of gradual decrease of incidence caused by the
compactarrangement of photobiont cells in the thalli. The
resultsindicate a good protection from the self-shading for the
innerphotobionts against high radiation in crust lichens.
Introduction
As an important component of biological soil crusts
(BSCs),lichens are exposed to harsh desert stresses in global arid
andsemiarid regions, where extremely strong radiation
(includingboth UV and visible light) always brings damages to
living
cells. Excess energy caught by light-harvesting complexes
caninduce the formation of triplet excited chlorophyll
molecules(3Chl*) and also the reactive oxygen species (ROS) [1],
whichcan attack photosynthetic reaction centers and cause the
deg-radation of D1 proteins of photosystem II (PSII) [2]. Someother
studies also propose that light can directly affect oxygen-evolving
complexes, and ROS inhibits the repair of damagedPSII by
suppressing the de novo synthesis of proteins [2]. As amutagenic
factor, UV can cause damages to DNA, lipids, andproteins [3]. Even
under no stress conditions, ROS can also beproduced by normal
metabolic activities such as respiration andphotosynthesis, and
enhanced by environmental stresses [4].
To cope with high radiation, lichens develop many strate-gies.
Unlike higher plants, lichens lack epidermic cells con-taining high
content of flavonoid polyphenolics to resist highradiation [5, 6].
Compact cortex formed by symbiotic fungicompensates this lack in
some extent. All kinds of UV-screening compounds, such as
scytonemin [7], mycosporine-like amino acids [7], phenolics [8, 9],
melanin, and parietin[10], secreted by lichens can effectively
reduce the transmis-sion of radiation [8, 11], and the reducing
effect is moreeffective in dehydrated thalli [11]. Buffoni Hall et
al. foundthat just due to the accumulation of UV-screening
compoundphenolics in Cladonia arbuscula (Wallr.) Flot. ssp.
mitis(Sandst.) Ruoss, the UV transmission in the thalli was
effec-tively reduced; therefore, both the UV radiation at 280
and310 nm decreased to 0 at 30–40 μm depth in the thalli
[8].Gauslaa and Solhaug [11] found that more UV-screeningpigments
are deposited in sun-exposed Lobaria pulmonaria,so that sun-exposed
thalli had lower transmission efficiencythan the shade-adapted
ones. The transmission efficiency ofUV radiation at 280–340 nm was
about 2 % in the sun-exposed thalli (both the hydrated and
dehydrated ones),whereas the transmission efficiency gradually
increased withwavelength and reached a peak (approximately 57 %)
at600 nm [11]. Other research demonstrates that the apotheciain
Teloschistes lacunosus (P. Rupr.) Savicz (the current nameis
Seirophora lacunosa (Rupr.) Frödén) quench as high as91.5 % of the
incident photosynthetically active radiation
L. Wu :G. ZhangSchool of Resources and Environmental
Engineering, WuhanUniversity of Technology, Wuhan 430072, China
L. Wu : S. Lan : C. Hu (*)Key Laboratory of Algal Biology,
Institute of Hydrobiology, ChineseAcademy of Sciences, Wuhan
430072, Chinae-mail: [email protected]
D. ZhangSchool of Sciences, Wuhan University of Technology,Wuhan
430070, China
Microb Ecol (2014) 67:888–896DOI 10.1007/s00248-014-0366-9
-
(PAR) [12]. Lichens can also dissipate excess energy caughtby
antennae in the form of nonradiation energy [13–16].
For crust lichens in desert regions, high radiation is acommon
and inescapable stress. Together with other environ-mental
stresses, high radiation severely restricts the survivaland
development of organisms in these regions. Althoughlichens
developed many adaptation strategies to high radia-tion, Gauslaa
and Solhaug [11] considered that inner symbi-otic algae received
rather incomplete protection [8]. Actually,different lichen species
are different in thallus thickness, cor-tex, pigments types and
contents, and photobiont species andcompaction, and these
differences are likely to lead to differ-ent adaptation abilities
and physical characteristics. Therefore,this study detects the
photosynthetic activities of differentlichen thalli in longitudinal
directions, aiming at evaluatingthe self-shading protection given
to the phototrophic cells bytheir position in the thalli against
high radiation in desertenvironments.
Materials and Methods
Samples
All the samples used in this study were collected from
anonirrigated area on the north side of the railway at theShapotou
Desert Research and Experimentation Station ofthe Chinese Academy
of Sciences (37°32′N and 105°02′E, Tengger Desert, Ningxia Hui
Autonomous Region ofChina). The samples were collected in June
2009, and thisexperiment was conducted in November 2010. The
crustsamples were kept in the desiccators after
collection.According to our field investigation, this area is
dominat-ed by cyanolichen soil crusts, more than 80 % of whichare
Collema spp. Other cyanolichens and green algallichens only occupy
a small proportion. Thereby threecrust lichens were selected in
this experiment, includingtwo cyanolichens, Collema sp. and Peltula
sp., respective-ly, and a green algal lichen, Placidium sp. The
details areshown in Table 1.
Methods
Photosynthetic Recovery of Crust Lichens and
SamplePreparation
The selected lichen soil crusts with intact lichens were
fullyrehydrated with sterilized distilled water and then
weretransported to a greenhouse (25±2 °C) to naturally dry
again(for 2 days). This process was defined as a
rehydration/desiccation cycle. A cool white light lamp was used to
supplylight. Then these crusts that experienced
rehydration/desiccation cycle as described were rehydrated to
recover their
photosynthetic activities in the light (40 μmol photonsm−2
s−1).After a recovery period of about 42–48 h, the lichen thalli
wereseparated from the crusts and sliced into thin pieces in
longitu-dinal direction with a scalpel under stereomicroscope.
Thenthese slices were put on the slides and detected
withMicroscope-Imaging-PAM later.
Table 1 Characteristics of the three selected crust lichens
Lichen Type Color Photoboint Coverageon crusts
Placidium sp. Squamulose Brown green alga
-
Chlorophyll a Fluorescence Measurement
Microscope-Imaging-PAM was used to detect the photosyn-thetic
activities of crust lichens in this experiment. Differentfrom other
versions of pulse amplitude modulation (PAM)fluorometry,
Microscope-Imaging-PAM connects with a mi-croscope, so that it
allows a rather small fluorescence imagingarea (830×613 μm), using
false color images to exhibit theheterogeneity of a chlorophyll
fluorescence parameter overthe whole imaging area.
After a period of dark adaptation (about 10 min), aweak light
lower than 1 μmol photons m−2 s−1 wasapplied to induce the minimal
fluorescence Fo, and thena saturating light pulse ~3000 μmol
photons m−2 s−1 wasused to determine the maximal fluorescence Fm.
Thesetwo fluorescence values (Fo and Fm) were used to calcu-late
several chlorophyll fluorescence parameters in the
fol-lowingmeasurement.When illuminated for a period of time,
asaturating light pulse (3000 μmol photons m−2 s−1) was
alsosupplied to determine Fm’, and the stable fluorescence Fsunder
this light intensity would also be recorded at the sametime.
Different chlorophyll fluorescence parameters,reflecting the
photosynthetic activities of PSII, are calculatedas follows:
Fv = Fm ¼ Fm−Foð Þ = FmYield ΦIIð Þ ¼ Fm’−Fsð Þ=Fm’rETR ¼ Yield
� PARqP ¼ Fm’−Fsð Þ= Fm’−Fo’ð ÞqN ¼ Fm−Fm’ð Þ= Fm−Fo’ð Þ
Fo’ is the minimum fluorescence yield in light-adaptedstate, and
it cannot be imaged with the existing imagingsystem. Therefore, Fo’
is estimated through an equation ac-cording to Oxborough and Baker
[17]. All these chlorophyllfluorescence parameters will be
calculated by software auto-matically and presented in the form of
false color images.
Fv/Fm is the maximum quantum yield of PSII primaryphotochemistry
[18], and is always stable in unstressed plants[19]. Yield (ФPSII)
is the effective quantum yield of PSII in thelight, reflecting the
light energy that is absorbed by PSII andused in photochemistry
[17, 20]. Both Fv/Fm and Yield are thecharacteristics of
photosystems and are not linked with theamount of chlorophyll [21].
Therefore, the estimation of elec-tron transport rate is a relative
one, defined as rETR, giving anoverall estimation of the
photosynthetic performance. The“photochemical quenching” qP is, by
definition, a value closeto Yield superficially, but not exactly
the same. Yield is theabsorbed light energy being used in
photochemistry, while qPprovides an indication of open PSII centers
under a certainlight [17, 20]. The parameter qN refers to the
energy dissipa-tion in the form of heat [22], reflecting the
protective abilityagainst high radiation.
Rapid light curve (RLC) is a powerful tool to assess
pho-tosynthetic activities. RLC can assess not only the
presentphotosynthetic capacity but also the samples’ potential
activ-ity over a wide range of ambient light [21]. RLC shows
therETR variations as a function of PAR. In our experiment, ninePAR
levels (0, 17, 26, 53, 81, 154, 200, 255, and310 μmol photons m−2
s−1) were set with a preinstalledsoftware routine, which was used
to measure the RLC. Theillumination duration for each PAR level was
10 s. One thing
.50
.55
.60
.65
.70
.1
.2
.3
.4
.5
0.00 .02 .04 .06 .08 .10 .12 .14.2
.3
.4
.5
.6
.7
.8
0.00 .02 .04 .06 .08 .10 .12 .14.30
.35
.40
.45
.50
.55
Fv/
Fm
Yie
ld
qP qN
Depth (mm) Depth (mm)
y= -59.72x3+15.27x2-1.842x+0.668
R2=0.93
y= 12.39x2-3.773x+0.446
R2=0.984
y=17.51x2-5.81x+0.795
R2=0.978
y=175.3x3-29.46x2-0.326x+0.528
R2=0.905
Fig. 2 Curve estimation betweendifferent chlorophyll
fluorescenceparameters and the depth ofphotoboint layer in
Placidium sp.at 108 μmol photons m−2 s−1 (theupper border of
photoboint layerwas treated as 0-μm depth)
890 L. Wu et al.
-
that must be pointed was that the Fv/Fm values were deter-mined
in the dark after 10-min dark adaptation, and wedisplayed the
result together with Yield, and the result ofYield at 0 μmol m−2
s−1 was actually the result of Fv/Fm. Infact, Yield is the absorbed
light energy being used in photo-chemistry; therefore, the actual
Yield value was 0 in the dark.
Data Analysis
Variance of each parameter between the upper and lowerlayers of
a lichen thallus from low- to high-PAR level wasanalyzed using
paired samples t test. Variance of each param-eter between
different layers of lichen thalli was analyzedusing one-way ANOVA.
All the above data analyses werecarried out using SPSS 13.0. The
curve estimations betweenthe chlorophyll fluorescence parameters
and the depth oflichen thallus were carried out using Sigmaplot
11.0.
Results
In this study, more than five replicate samples were studied
foreach lichen species, and similar trends were found
amongdifferent replicates for each lichen species. Therefore, we
justshowed the false color results of photosynthetic
characteristicsof one sample for each lichen species.
Placidium sp.
The longitudinal photosynthetic gradient was evident inPlacidium
sp. thallus, as shown in Fig. 1. This figure showsthe false color
images of three parameters (Yield, qP, and qN) inPlacidium sp.
during the RLC measurement. Different colorsrepresented different
values of the chlorophyll fluorescenceparameters. The results
showed the obvious heterogeneity ofeach chlorophyll fluorescence
parameter in longitudinal direc-tion under a certain PAR level.
Especially, once PAR exceeded53 μmol photons m−2 s−1, the
heterogeneity was particularlyobvious. At each radiation intensity,
the upper layer ofphotobiont had the higher Yield, qP, and qN
values than therelative lower layer (P
-
and the lower band was red. Once the PAR reached154 μmol photons
m−2 s−1, the upper half band was red andthe lower half disappeared.
The results of curve estimationbetween fluorescence parameters and
the depth of thephotobiont layer (we took the results at 81 μmol
m−2 s−1 foran example) showed that all the three parameters,
Fv/Fm,Yield, and qP, linearly decreased with the depth of
photobiontlayer, whereas qN gradually increased with the depth
ofphotobiont layer, and the increasing rate of early
stage(depth
-
40- to 60-μm thickness of the thalli in Peltula sp., so that
thislayer showed brown color, whereas the photobiont cells
underthis thickness showed blue-green color without any
depositedUV-screening pigment (Fig. 7c). Alcian blue staining
resultshowed that Collema sp. lacked the upper cortex, and theupper
surface contained polysaccharide materials, but notthe symbiotic
hyphae (Fig. 7f, white arrow). Dark brownUV-screening pigments
mainly concentrated the thallus sur-face of Collema sp. (Fig. 7e),
while it was also found that theinner symbiotic cyanobacterial
filaments did not show freshblue-green color as the photobiont of
Peltula sp. (Fig. 7c, e).
Discussion
Longitudinal stratification is a common phenomenon inBSCs, and
light is an important environmental factor affecting
the distribution of photosynthetic organisms [23–25].Different
from most of the crust organisms, lichens directlydistribute on the
crust surface, suffering high radiation un-avoidably. Self-shading
is an important strategy for lichens toresist high radiation
including both UV and visible light.Because of the gradual
attenuation of incident light, thephotobiont cells of the upper
layer receive more light thanthe lower layer in lichen thalli. Our
results showed that Fv/Fm,Yield, and qP gradually decreased with
the depth in bothPlacidium sp. and Peltula sp. thalli under a
certain PAR level(from low to high PAR). The results imply that
crust lichensreceive a relative complete protection from
self-shading effectagainst high-light stress (including visible
light and UV-radiation).
There are many studies on the self-shading effects in li-chen’s
resistant ability against high radiation [7–11]. Gauslaaand Solhaug
[11] considered that the inner photobiont cells ofthe sun-exposed
thalli received rather incomplete protection.However, our results
seemingly do not support their view-point. If the protection is not
complete, the relative upper layershould have lower Fv/Fm, Yield,
and qP values, because theyreceive much more solar radiation
(especially of UV) than thelower layer. The fact is just the
opposite. In both Placidium sp.and Peltula sp., the Yield and qP
values gradually decreasedwith thallus depth in the longitudinal
direction from the low tohigh PAR, so did Fv/Fm. Additionally, we
also found that UV-screening pigments deposited in the upper 40- to
60-μmthickness of the thalli in Peltula sp., and no such pigmentwas
found around the photobiont cells below this depth. Aswe know, it
is an important strategy for cyanobacteriumChroococcidiopsis to
secrete scytonemin, a brown pigment,in resisting UV stress [7, 26].
Therefore, we consider thatphotobiont in Peltula sp. receives
protection against UV radi-ation well, that is the self-shading
protection for crust lichens’photobionts is complete. Other
researchers’ study also dem-onstrated that the UV radiation at 280
and 310 nm decreasedto 0 at 30- to 40-μm depth in lichen thalli
[8], and this depthwas basically coincident with both the
pigment-depositeddepth in Peltula sp. and the upper cortex
thickness inPlacidium sp. in the present study.
As far as we know, it is the first study on the
longitudinalphotosynthetic characteristics of lichens, and it
provides somenew information that differs from previous
observations.Although many experts have detected the radiation
attenua-tion within the lichen thalli [8, 11, 27], the effect of
attenuatedlight on photobiont has not yet been evaluated. The
possibilitywas once proposed that both the position and thickness
ofphotobiont layer in the lichen thallus could be determined bythe
PAR attenuation [27]. The PAR attenuation at the upperborder of the
photobiont layer would be low enough and at thelower border, it
would be high enough (above the photosyn-thetic compensation point)
for the growth of photobionts [27].Our results of the gradual
decreasing photosynthetic activity
Fig. 5 Series of images (Yield, qP, and qN) measured during a
rapid lightcurve (RLC) of cyanolichen Collema sp. over seven PAR
levels. Differentcolors (bar at the bottom) indicate different
values of each parameter, and themaximum value of each parameter
has been adjusted to 1. All these picturesare a longitudinal
section of the lichen thallus with its uppermost surface up
Longitudinal Photosynthetic Gradient in Crust Lichens’ Thalli
893
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in the longitudinal direction imply that the PAR intensity at
theupper border of the photobiont layer was not high enough tocause
obvious damages to photobiont cells. Additionally, a
significantly inverse relationship between the amount of
sym-biotic alga and the intracellular chlorophyll concentration
wasfound in the lichen family Umbilicariaceae, and this result
was
Yie
ld
0.0
.1
.2
.3
.4
.5
.6
rET
R
0
2
4
6
8
IsidiumUpper layerLower layer
0 50 100 150 200 250 300 0 50 100 150 200 250 300
qP
-.2
0.0
.2
.4
.6
.8
1.0
qN0.0
.2
.4
.6
IsidiumUpper layerLower layer
IsidiumUpper layerLower layer
IsidiumUpper layerLower layer
Isidium
Upper layer
Lower layer
PAR µ mol photons m-2 s-1 PAR µ mol photons m-2 s-1
Fig. 6 Change of chlorophyll fluorescence parameters (Yield,
rETR, qPand qN) of Collema sp. thallus under different
photosynthetically activeradiation (PAR). For each parameter, the
data change is compared among
the isidium, upper layer and lower layer, three different
regions of thethallus. In each region (the isidium, upper layer or
lower layer), three tofour data areas are selected as shown in the
colored picture on the right
100 µm 30 µm
30 µm
100 µm 10 µm
30 µm
a b
c d
fe
Fig. 7 The inner structures of thethree crust lichens. a,
bPlacidiumsp., c, dPeltula sp., and e, fCollema sp. b, d the
magnificationpictures of the circled areas in aandc, respectively.
The red arrow in bindicates the polysaccharides layeroutside the
upper cortex; the whiteone indicates the upper cortex withdeposited
UV-screening pigments.The red arrow in c indicates thephotoboint
cells that showed theblue-green color. The arrow in dindicates the
photoboint cells closeto the uppermost surface of lichenthallus. e
the picture of Collema sp.under microscope without anytreatment,
and fwas stained withAlcian blue. The arrows in e andf indicate the
filaments of thephotoboint distributing within thepolysaccharides
matrix of thethallus
894 L. Wu et al.
-
ascribed to the mechanism of avoiding the excess loss ofvisible
light caused by pigment self-shading [28]. Both ourresults in this
study and other results mentioned above supportour viewpoint that
inner photobiont cells receive relativecomplete protection against
high radiation including both theUVand visible radiation.
The upper layer having higher photosynthetic activitiessuggests
a good adaptation of crust lichens to desert environ-ments. It has
been demonstrated that the light compensation ofcrust lichens will
change with the water content; therefore, nomatter how limited the
water resource is, it still can be effec-tively used by crust
lichens to fix carbon [29]. When limitedwater occurs, the upper
layer of photobiont with high photo-synthetic efficiency has an
advantage to activate photosyn-thetic activity preferentially, so
that more carbon will be fixed,and this characteristic maybe is an
important strategy for thesurvival and development of crust lichens
in desert regions.
Our results showed that not all the crust lichens had
thelongitudinal photosynthetic gradient phenomenon. The
chlo-rophyll fluorescence parameters Fv/Fm, Yield, and qP did
notexhibit obvious change with the depth in Collema sp. thalli.We
ascribe the difference in longitudinal photosynthetic gra-dient
between lichen species to the different inner structures ofthe
thalli, and it has no relationship with the specific species ofthe
photobiont (a cyanobacterium or a green alga). The obser-vation
results under microscope showed that the photobiontcells are
compactly arranged in Placidium sp. and Peltula sp.thalli, and
UV-screening pigments are mainly distributed inthe upper 40-μm
thickness (brown), under which photobiontcells showed green
(Placidium sp.) or blue-green color(Peltula sp.). However,
photobiont cells are loosely distributedin Collema sp. The brown
UV-screening pigments are mainlyconcentrated in the thallus’
surface, while the inner symbioticcyanobacterial filaments did not
show fresh blue-green coloras the photobiont in Peltula sp., and
this result was ascribed tothe UV-screening pigments secretion
around thesecyanobacterial filaments. In addition, the brown
UV-screening pigments were also found near the lower surfaceof
Collema sp. thalli (result not shown here). In some otherspecies of
the same genus Collema having much thicker thallithan the species
used in this study, we also found the photo-synthetic gradient
phenomenon in longitudinal direction (datanot shown). Therefore, we
speculate that the lower photobiontcell density leading to relative
homogeneous light circum-stance may be the cause of the
disappearance of photosynthet-ic gradient in Collema sp.
Additionally, the photosyntheticgradient phenomenon is also found
in several other crustlichens in the same area (data not shown);
therefore, it is acommon but not absolute characteristic.
The results of microscope observation of the lichen struc-tures
also showed us an interesting phenomenon: all the crustcyanolichens
in our study field lacked upper cortices, and theupper border of
the photobiont layer was quite near the
uppermost surface of the thalli. To the contrary, green
algallichens’ photobionts receive protection from the upper
corti-ces, where UV-screening pigments are deposited.
Thecyanolichens found in our study area were with Scytonemasp.,
Nostoc sp., and Chroococcidiopsis sp., as photobionts,respectively.
According to our observation, besides forminglichens with fungi,
the free-living forms of the above threecyanobacteria are also
widely distributed in arid and semiaridregions [30, 31].
Especially, Nostoc and Scytonema are evendirectly distributed on
crust surface [24, 25, 31], while greenalgae are distributed at the
relative deeper depth [24]. Theseresults imply that free-living
cyanobacteria have a strongability in resisting high radiation in
desert regions. However,water ecosystems are considered to be the
evolutionary originof green algae, and their free-living forms
without the protec-tion from symbiosis rarely dominate purely
terrestrial ecosys-tems [11]. From this perspective, the protection
from fungi isindispensable for the green algal photobiont, whereas
is non-essential for cyanobiont of crust lichens. Therefore, we
spec-ulate that the symbiotic relationship is not uniform for
alllichen species, and it may have a close relationship with
thespecies of inner photobionts.
In general, longitudinal gradient phenomenon exists notonly in
the whole BSCs system [24, 25], but also in single-crust organisms
such as the lichens in this study. The photo-synthetic gradient in
crust lichens is the intuitive reflection ofself-shading protection
given to the phototrophic cells by theirposition in the thalli.
Additionally, our study implies that innerphotobiont cells of crust
lichens receive complete protectionfrom self-shading effect against
high radiation in desertregions.
Acknowledgments This study was kindly supported by grants
fromthe China Postdoctoral Science Foundation (2013 M542077),
NationalNatural Science Foundation of China (Nos. 31300100 and
31170464),and National Forestry Public Welfare Industry Research
project(201404204).
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https://www.researchgate.net/publication/259985690
Longitudinal Photosynthetic Gradient in Crust Lichens’
ThalliAbstractIntroductionMaterials and
MethodsSamplesMethodsPhotosynthetic Recovery of Crust Lichens and
Sample PreparationChlorophyll a Fluorescence MeasurementData
Analysis
ResultsPlacidium sp.Peltula sp.Collema sp.Inner Structures of
Crust Lichens
DiscussionReferences