Abstract—Vertical
migration of two benthic[JH1] diatoms was studied inas a response to different light intensityy and
temperature[JH2] . Using An[JH3] Imaging-PAM (P pulse-amplitude-modulated) fluorometer (Imaging-PAM), and [JH4] minimal fluorescence (F0) waswere used to monitor diatom biomass variation in surface sediments, and
rapid light curves (RLCs) were usedapplied to assess the photosynthetic activities of the tested diatoms. Both Cylindrotheca closterium and Nitzschia sp.[JH5] presented increasing motility under higher-temperature conditions. However, C. closterium, with its long valves, hadshowed more than twice the migratory speed asof the shorter-valved Nitzschia sp.[JH6] with shorter valves. The Ttwo light intensities, of 100 and 250 µmol photon[JH7] m-2 s-1, had different effects on C. closterium, but had not effects on Nitzschia sp. Consequently, there
was no light/temperature interaction between light and
temperatureeffect on the vertical migration of Nitzschia sp. With
lower photosynthetic capacity and smaller cell size, Nitzschia
sp., with its low
photosynthetic capacity and smaller cell size, responded differently from C. closterium.
Although withthe mechanism is[JH8] complicated, mechanism, light
and temperature were proved to greatly influence the migratory behavior of
the benthic diatoms, and
inducethrough species-specific response of different diatom speciesinducements.
Keywords-: benthic diatom; chlorophyll
fluorescence; light; temperature; vertical migration
I.
Introduction
Benthic diatoms inhabiting intertidal sediments exhibit
vertical migratory rhythms within the upper sediment
layers, which are associated with diurnal and tidal cycles [1, 2, 3, 4].[JH9] Typically, when large numbers of
diatoms aggregate inon thea
sediment surface, they forming a
biofilm, which, due to
the fucoxanthin pigment, exhibits a
golden brown color is easilyreadily observed withapparent
to the naked eye due to the fucoxanthin
pigment of diatoms [5, 6].
Since
vVertical migration of benthic
diatoms,
hashaving
been largelywidely recognized as a key controlling
factor ofdetermining[JH10] short-term variability in benthic primary
productivity, it has been studiedreceived
increasingly research attention in recent
years [7, 8, 9].
Light, As a mainprincipal[JH11] triggering factor for benthic
diatoms’ vertical migration, light controls the migration
rhythms[JH12] [4,
10, 11], and also affects
the
photosynthetic activity of benthic diatoms [12, 13, 14]. Although And
though the mechanism isis complicated, under laboratory conditions the
temperature does influence the migration rhythmtemperature
has also been found to influence
the migration rhythm of field samples under
laboratory conditions [15,
16], as well as the photosynthesis of field-sample
benthic diatoms [17,
18].
In surface sediments onthe intertidal flats, the light
intensity and temperature haveshow major spatial and temporal
gradients in surface sediment,that
varying alongwith
the rise and recession of with the
tides rising and receding [19]. The lLight
intensity couldcan change from very high
(exceeding 2000 µmol photon m-2
s-1)
at low tide and solar noon[JH13] to
littlevery
low or nothing at high
tide[JH14] [JH15] light reaches the
sediment surface[JH16] during
low tide at solar noon [14,
20]. The sSurface temperature has been reported
that
hadexhibited a maximum daily
change up toas large as 18 oC, atfor
a rate of 3 oC
h-1 [12],;
and
in temperate regions, temperature in the upper 200 µm
of muddy
sediments can easily changeshift by 10 oC during
emersion periods, withat rates ofas
high as 4 oC
h-1 [21].
Responding to varying environmental factors,The
migratory ability of benthic diatoms in response to varying light,
temperature and other factors enables
their success within the sedimentary environment. It has been observed in situ that
the
diatoms concentrated at a depth of 1 mm can migrate up[JH17] to the
surface in 1.5 hours[JH18] in situ [22]. And thethis migration has been found isto be species-specific, viz.that is, species’ surfacings altereddiffered at differentaccording to the time during aof day [9,
16, 23]. [JH19]
Fluorescence techniques usingutilizing
thean
imaging
pulse-amplitude-modulated
fluorometer (Imaging-PAM) hashave
been widely used onapplied to the measurement
of microphytobenthic biomass and photosynthetic activity [14, 24, 25, 26, 27]. ThePAM-measured
minimum fluorescence (F0) measured by
PAM is proved to have
a linear relationship with microphytobenthic biomass [24, 28, 29, 30]. And Aamong
the various
PAMs, Imaging-PAM not only allows the quick,
non-intrusive and sensitive measurement as others[JH20] , but also hasoffers
the uniquely
advantageouss
utility
of measuring larger areas and numbers of interesting points
simultaneously onin one image. Using Imaging-PAM, then,
can decreaseminimize experimental error which
caused byresulting from the prolonged
time required for measuring samples individually.
Until now, no study has investigated the two-factor effects of light and temperature on the vertical migration of benthic
diatoms. In thisthe present study, using
Imaging-PAM and a miniaturized setup, we aimed to investigated
the vertical migration of two diatom species in response to different
temperature and light conditions, and
analyzed
their
migration mechanisms both photo-[JH21] physiologically and morphologically, in
order to assistenhance further the synthetic
understanding of the microphytobenthos (MPB)
ecology in in situtheir[JH22] environments.
II.
Materials
and Methods
Unialgal
cultures of Cylindrotheca closterium (hereafter
C. closterium) and Nitzschia sp. (supplied by the Korea
Marine Microalgae Culture Center, Busan, South Korea) were grown in 2 L flasks[JH23] with f/2 medium [31] withand pre-filtered
seawater (0.2 µm membrane filter; salinity,: 34
psu). All[JH24] of the cultures were incubated
under constant conditions atincluding 20 oC
temperature withand a 12 h: 12 h light
(100 µmol photon m-2 s-1):
dark photoperiod. of 12 h: 12 h. The
growth rates were monitored through increases in the chlorophyll a concentration and cell number. Once
the cultures reached the stationary phase, diatom cells were deposited
homogenously[JH25] on glass microfiber filters (porosity: 2.3 µm) by slow filtration (< 0.1 MPa),
forming artificial biofilms. The Ccell sizes of C. closterium and Nitzschia diatomssp. waswere
measured under a light microscopy using an AxioVision
LE (Allied High Tech Products, Inc.,; Rancho
Dominguez, California, USA)., and The sizesfound to be (mean ±
SD) of C. closterium and Nitzschia sp. were 103 ±
6.3 × 4.1 ± 0.3 µm and 18 ± 2. 1 × 2.1 ± 0.2 µm, respectively.
Prior to the experiment, the
samples in 24-well plates were prepared from the
adjusteding sample height
with 3.0 g treated sediment (removed of all organic materials). in a well[JH26] . Small circulare [JH27] biofilms were cut from the
artificial biofilms into the same size of the inner diameter of the wells, and
then were putplaced on the top of the 3.0 g sediment base. The Iinitial minimum
fluorescence (F0)[JH28] was measured by Imaging-PAM
after a 5 min dark-adaptation period. Rapid light curves (RLCs) were useddrawn forto assessing the photosynthetic activities, wherethe samples werehaving been exposed to twelve incremental steps of irradiance (10s per step) ranging
from 0 to 701 µmol photon m-2 s-1. Relative electron
transport rates (rETR) were givenobtained byfrom the RLCs. measurement[JH29] . Three Pphotosynthetic parameters, including the maximum rETR (rETRmax), the minimum saturating irradiance (Ekk)
and the Llight utilization coefficient (α), were derived from thean rETR light response curve fitted to the model of Platt
et al.’s
model [32]. After measuring the F0 and RLCs, these circularle biofilms were covered with a
sediment layer approximately 2 mm thick sediments
(125–250 µm). All of the wells with
samples were maintained saturated with f/2 medium duringthroughout the experiment. process
with f/2 medium.
The well plate
with samples was put on a fixed mounting stand position under the measuring
head of the Imaging-PAM (Max/L, underin Live Video Mode,. with the same size of circle samples. The
same AOIs were used consistently used duringover
the course of the whole experimentation. The fFluorescence was induced by royal blue (450 nm) 3 W Luxeon LEDs, which
have standard intensity of 0.5 µmol m-2
s-1 standard
intensity and 1 ~ 8
Hz modulation frequency. between 1 and 8 Hz.
The experiment
of the light and temperature effects on the two
species’ vertical migrations was carried on two specieswere
studied under two light intensityies[JH30] (100 and 250 µmol photon m-2
s-1) and three temperature (10, 20, 30 oC) conditions,
viz. incubated the prepared well-plate samples were incubated under 10 oC-100 µmol
photon m-2 s-1, 20 oC-100
µmol photon m-2 s-1, 30 oC-100
µmol photon m-2 s-1, 10 oC-250
µmol photon m-2 s-1, 20 oC-250
µmol photon m-2 s-1, and 30 oC-250 µmol photon m-2
s-1, environments, representing
a totally of six treatments for each species. Each treatment had four replicates. The F0 was measured by Imaging-PAM, after a 5 min dark adaptation, at 0 h, 1 h, 2 h, 3.5 h, 5.5 h and 7 h.
The sediment surface F0 of each sample was
usedreferenced to monitordetermine[JH31] the surface biomass increase
due to the diatoms’ migrating
upmigration from the circulare biofilm to the sediment surface.
To compare the effects of the different incubation conditions on the two species (i.e. to determine the significant differences), a univariate analysis of variance, followed
by post-hoc Tukey tests waswere carried out to test significant
difference using SPSS 17.0 (SPSS Inc., Chicago, IL, USA).
III.
Results
The
initial F0, values, which as measured on the small circulare biofilms before the
latter were covereding with sediment, were 0.0440 ±
0.0026, 0.0422 ± 0.0021 (arbitrary units) for C. closterium and Nitzschia sp., respectively. The Tthree photosynthetic parameters (Ek, α
and (rETRmax, Ek and α)[JH32] of C. closterium arewere all higher than those of Nitzschia sp. (Table I). The
migratory responses of the two
species to the different light intensities and temperatures are illustrated in Fig.1.
After 2 h incubation, for 2
hours, diatoms cells of the two species began migrate up to the sediment surface. From 2 to
7 h incubation, moreadditional[JH33] diatoms cells of the two species migrated, up and presentinged a different migratory response to the individual[JH34] conditions.
Generally, the diatom cells migrated quickerfaster at higher temperatures than at lower temperatureones, with sequence ofin the
order 30 oC
> 20 oC > 10 oC
for both species. And C. closterium showed a higher motility by
almost twice F0 as that ofthan did Nitzschia sp., sp.almost twice its F0[JH35] , after 3.5 h incubation.
Comparing the effects of the six conditions on the two species afterfor certainthe several[JH36] incubation timetimes, two species showedthere
was no significant (P > 0.05) difference at 2 h incubation, but there were extremely significant (P <
0.001) differences
at 3.5 h, 5.5 h and 7 h incubation. under
the same light and temperature conditions[JH37] . With
respect to temperature, the two
species responded significantly (0.01 <
P < 0.05) differently forbetween 2 h toand 7 h incubation. There was no statistically significant difference
between two speciesthem in response to the two light
intensities at 2 h, but they
differed significantly at 3.5 h, very
significantly (0.001 < P <
0.01) at 5.5 h and extremely significantly at 7 h incubation (Table II). Generally, the differences between individual conditions increased
along
with incubation time.
For C. closterium,
the light intensity showed no statistically significant effects on upward
migration at 2 h incubation, but haddid so significantly difference
at 3.5 h and extremely significantly difference at 5.5 h and 7 h
incubation. However, it was obvious that at 10 oC
of 3.5 h, 20 oC of 3.5 h and 7 h, the F0 values showed no
significant difference between 100 and 250 µmol photon m-2 s-1.
Visually, the 100 µmol photon m-2 s-1 light
intensity induced more migration than did 250 µmol photon m-2 s-1 for C. closterium at 10 and
30 oC. The temperature effects on the vertical migration of C. closterium were significant from 2 h to
7 h incubation. A Ssignificant or extremely significant difference existedwas
evident in each temperature
pair comparison between temperatures for 2
h toand 7 h incubation. The interaction between light intensity and temperature
for C. closterium was not significant at 2 h incubation, but was significant at 3.5 h, 5.5 h and 7 h incubation (Table II).
TABLE
I.
Photosynthetic
Parameters of Two Species
|
Species |
rETRmax (relative units) |
α (relative units) |
Ek (µmol e m-2
s-1) |
|
Cylindrotheca closterium |
41.74 |
0.28 |
149 |
|
Nitzschia sp. |
36.11 |
0.25 |
147 |
Figure
1. 
Effect[JH38] s[JH39] of light intensity and temperature on the two
species’ upward migration of two species with
incubation time.
For Nitzschia sp., the light intensity had no statistically[JH40] different effect from 2 h to 7 h incubation. The temperature effects on its vertical migration,
of
Nitzschia sp.though,
were significant from 2 h to 7
h incubation. WithIn respect ofof
each pair comparison betweenof temperatures, the post-hoc
Tukey tests showed no difference between 10 and 30 oC, or
20 and 30 oC
at 2 h incubation, as well
asor indeed between 20 and 30 oC
at 3.5 h incubation,;
however, showedthere were manifestly significant,
or
very significant, or even extremely significant
differences between the temperatures
at the other
incubation times. There was no interaction
between light intensity and temperature for Nitzschia
sp. under the designed experimental
conditions (Table II).
IV.
Discussion
A. Effects of light and temperature
Lower light intensity usually
induces morelarger benthic diatoms
migrationsg
up
to the sediment surface. On intact
biofilms of estuarine sediments, Serôdio et al. [25] reported that, on intact biofilms of estuarine
sediment, the surface biomass increases under irradiances below
100 µmol photon m-2 s-1 and reaches maximum values under
100-250 µmol photon m-2
s-1, but decreases gradually under higher irradiances as (1000-1500 µmol photon m-2 s-1).
In our previous study, we found thethat
TABLE II.
Significant
Values offrom Univariate Analysis on Two Species Incubated
Under 2
Lights and 3 Temperatures
Conditions
|
Species |
Source |
2h |
3.5h |
5.5h |
7h |
|
Cylindrotheca
closterium and Nitzschia sp. |
Temp |
0.000 |
0.000 |
0.000 |
0.000 |
|
Light |
NS |
NS |
0.001 |
0.001 |
|
|
Species |
NS |
0.000 |
0.000 |
0.000 |
|
|
Temp * Light |
NS |
0.048 |
NS |
0.011 |
|
|
Temp * Species |
0.000 |
0.000 |
0.000 |
0.000 |
|
|
Light * Species |
NS |
0.049 |
0.001 |
0.000 |
|
|
Cylindrotheca
closterium |
Temp |
0.000 |
0.000 |
0.000 |
0.000 |
|
Light |
NS |
0.038 |
0.000 |
0.000 |
|
|
Temp * Light |
NS |
0.049 |
0.034 |
0.002 |
|
|
10*20 |
0.017 |
0.000 |
0.000 |
0.000 |
|
|
10*30 |
0.000 |
0.000 |
0.000 |
0.000 |
|
|
20*30 |
0.000 |
0.000 |
0.000 |
0.000 |
|
|
Nitzschia sp. |
Temp |
0.025 |
0.001 |
0.000 |
0.000 |
|
Light |
NS |
NS |
NS |
NS |
|
|
Temp * Light |
NS |
NS |
NS |
NS |
|
|
10*20 |
0.022 |
0.045 |
0.006 |
0.004 |
|
|
10*30 |
NS |
0.000 |
0.000 |
0.000 |
|
|
20*30 |
NS |
NS |
0.020 |
0.000 |
NS: Not-significant
concentrated diatoms migrated
up
to the sediment
surface under 50-500 µmol m-2 s-1, but migrated down into
deeper sediment after 4 h of illumination under 500 µmol photon m-2 s-1, and showed no obviously migratory behavior under 1000 µmol photon m-2 s-1 [33]. In thisthe
present study, we usedapplied 100 and 250 µmol photon m-2
s-1, which could causeinduced maximum upward migration, and and
haveto a 2.5 times disparity. AndThat is, the tested species, C.ylindrotheca closterium, presented more upward migration under 100 µmol photon m-2 s-1
than under 250 µmol photon m-2 s-1.
The effect
of temperature on the migration is fewrarely studied with respect to motility. Generally, higher but not extreme
temperatures could increase the motility of unicellular organism [34, 35]. In thisthe study here
concerned, both species showed higher upward
migration at higher temperatures, which
also recorded inresults consistent with the research
of Cohn et al. [36]. However, lLow temperature (2 oC), by
contrast, was reported thathas
been found to markedly reduce the
migration rhythm of diatoms [15]. Similarly,
in our recent field study on temporal variation in the vertical distribution of microphytobenthosMPB, the migration rhythm also was changed, byspecifically when the diatoms[JH41] stayingremained longer in surface sediment at 5.5~6.6 oC
(the daily average temperature) in winter [37]. The Llower motility at lower temperatures could contribute to this phenomenon.
Although the interaction of light and
temperature was found only
found in
C.
closterium in thisthe
present experimentation,
it does not indicatefollow that interactions do not exist in Nitzschia sp. or other species. A prime reason is that temperature is a very
important factor influencing almost all physiological activities, including the photosynthetic
activity and motility [16, 17, 18, 38]. Adding moreadditional sediment levelslayers could help elucidate the
interaction but would also
increase the experimental
complexity.
of
experiment. Therefore, one factor effect on more species is suggested
to be carried in advance.[JH42]
B. Species-specific
response and motility
In this
study,The two species studied
here exhibited different motility responses and motility to[JH43] light and temperature. The Mmotility of C. closterium was about twice as high as
that of Nitzschia sp. As
already mentioned, Nthere
were no effects of light andor of the interaction of light and temperature were found onon Nitzschia sp., which
was also different from those ofcontrastingly to C. closterium. In one of our
previous studiesy, the species-specific
difference also presented itself onin the effects of the light and grain size on the
vertical migration for Amphora
coffeaeformis and C. closterium [33]. The results of ourthe present[JH44] study corroborate again the
field findings of the species-specific variation in
migration [9, 16, 23].
Concerning
these various migratory responses, one main origin is the photo-physiological
characteristics of different diatoms species.
The motive of thebehind upward migration is forthe satisfactionying of their light requirement of their photosynthesis. AndCorrespondingly, species with lower Ek acclimate themselves to lower light
intensity. It has been found that Pleurosigma
angulatum, which is dominant in diatom biofilms at midday, hasd a higher Ek (between 500 and 600 µmol m-2 s-1),
while Nitzschia dubia, which
displayedreflecting its rapid vertical migration away from the surface under increasing
irradiance, hasd a lower Ek of 300 µmol m-2 s-1 [15]. In thisthe
present studyinvestigation, the lower Ek, α and rETRmax indicated that Nitzschia sp. hasd a lower photosynthetic capacity and activity, and that alsoit prefers a lower light intensity than that favored by C. closterium. Therefore,Hence our
finding that lessfewer cells of Nitzschia sp. cells migrated up to the
sediment surface. [JH45]
Morphological
characteristics could also partly explain the difference ofin the migratory responses, especially the
motility difference. Comparing their cell sizes, the C. closterium
has long valves (approx. 103 × 4.1
µm
or so), but Nitzschia
sp. has shorter and thinner valves (approx. 18 × 2.1 µm or so). Small size has been showned to be disadvantageous for cells’ locomotion through
sediment, because this motion also needrequires a substratum to adherewhich by using their extracellular polymeric
substances (EPS) can adhere [39, 40, 41, 42]. Small species such as Navicula species hashave been observed using the trails of larger diatoms Pleurosigma angulatum for upward migration [43]. Furthermore, with
long and only lightly or partially silicified valves, the cells of C. closterium
couldcan move more quicklyer through the sediment
aiding
by rotating their frustules. Therefore,Thus, the motility of C. closterium could be more than twice as that
of Nitzschia sp. in this study. With
regard to the different responses to light intensity, the more efficiently light harvesting of a small cell
due to the smaller packaging effect [44] could be a reason for whyfor the disparity offact
that 100 and 250 µmol photon m-2
s-1 hadve no effect on small species as Nitzschia sp[JH46] .
Another morphological
index, the SA/V
ratios (i.e. the ratio of surface area
to volume), also could
also help to
elucidate[JH47] the lesser upward migration of Nitzschia sp. under higher temperatures.
In the study ofby Yun et al. [38], the
photosynthetic activities of smaller species with larger SA/V (ratio
of surface area to volume)[JH48] ratios were more negatively affected by
higher temperature than larger species with smaller SA/V ratios. And they
measuredIndeed, the SA/V ratios
of Nitzschia sp., in
Yun et al.’s measurement, was 2.88 ± 0.08 µm-1,
which
is more than twice than that of C. closterium (about
1.3µm-1)[1].
Acknowledgment
This research was supported by the Korean Ministry of
Land, Transport and Maritime Affairs as “Greenhouse Gas Emission Reduction
using Seaweeds.” We especially appreciate the financial supported
byof
“the Fundamental Research Funds for the Central Universities” of the Ministry
of Education of towhich
aided
the completione of this
manuscript.
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