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Effects of turbulence on alkaline phosphatase activity of phytoplankton and bacterioplankton in Lake Taihu

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Effects of turbulence on alkaline phosphatase activity of phytoplankton and bacterioplankton in Lake Taihu

Abstract

Alkaline phosphatase (AP), an inducible and hydrolytic enzyme, plays a key role in the biogeochemical cycle of phosphorus (P) in lakes. Activity and regulation of AP has been suggested to be affected by hydrodynamic turbulence. However, many aspects of the coupling of the AP activity (APA) and turbulence are still to be investigated and understood. In this study, mesocosm experiments were carried out to further understand the effects of turbulence on APA and the relative contribution of the different microbial groups to the total APA (TAPA). Specifically, we focused on evaluating the APA of phytoplankton (2–112 lm) and bacterioplankton (0.2–2 lm) and its relationship with P fractions under four turbulence levels. Results showed that turbulent conditions enhanced planktonic APA (PAPA) which dominated TAPA by comprising 66–93% of the total fraction. In particular, PAPA was almost two times higher in the turbulence treatments than in still-water control. On the other hand, bacterioplanktonic APA (BAPA) decreased which could be associated with the competitive advantage of bacteria in nutrient-limited conditions due to surface-to-volume ratio. The results suggest that turbulence can accelerate the biogeo-chemical cycle of P and plays an important role in P strategies of plankton.
PRIMARY RESEARCH PAPER
Effects of turbulence on alkaline phosphatase activity
of phytoplankton and bacterioplankton in Lake Taihu
Jian Zhou
.
Boqiang Qin
.
Ce
´
line Casenave
.
Xiaoxia Han
Received: 20 March 2015 / Revised: 8 June 2015 / Accepted: 16 July 2015
Ó Springer International Publishing Switzerland 2015
Abstract Alkaline phosphatase (AP), an inducible
and hydrolytic enzyme, plays a key role in the
biogeochemical cycle of phosphorus (P) in lakes.
Activity and regulation of AP has been suggested to be
affected by hydrodynamic turbulence. However, many
aspects of the coupling of the AP activity (APA) and
turbulence are still to be investigated and understood.
In this study, mesocosm experiments were carried out
to further understand the effects of turbulence on APA
and the relative contribution of the different microbial
groups to the total APA (TAPA). Specifically, we
focused on evaluating the APA of phytoplankton
(2–112 lm) and bacterioplankton (0.2–2 lm) and its
relationship with P fractions under four turbulence
levels. Results showed that turbulent conditions
enhanced planktonic APA (PAPA) which dominated
TAPA by comprising 66–93% of the total fra ction. In
particular, PAPA was almost two times higher in the
turbulence treatments than in still-water control. On
the other hand, bacterioplanktonic APA (BAPA)
decreased which could be associated with the com-
petitive advantage of bacteria in nutrient-limited
conditions due to surface-to-volume ratio. The results
suggest that turbulence can accele rate the biogeo-
chemical cycle of P and plays an important role in P
strategies of plankton.
Keywords Turbulence Alkaline phosphatase
activity Phytoplankton Bacterioplankton
Phosphorus deficiency Phosphorus strategy
Introduction
Phosphorus (P) is one of the essential elements for all
living organisms (Istva
´
novics, 2008), but its low
availability often constrains the growth and/or bio-
mass of aquatic biota (Carpenter, 2008). Inorganic
phosphate (Pi) is generally regarded as directly
available and most rapidly assimilated by plankton
Handling editor: Judit Padisa
´
k
J. Zhou B. Qin ( &)
State Key Laboratory of Lake Science and Environment,
Nanjing Institute of Geography and Limnology, Chinese
Academy of Sciences, 73 East Beijing Road,
Nanjing 210008, People’s Republic of China
e-mail: qinbq@niglas.ac.cn
J. Zhou
University of Chinese Academy of Sciences,
Beijing 100049, People’s Republic of China
C. Casenave
UMR INRA-SupAgro 0729 MISTEA (Mathematics,
Informatics and Statistics for Environment & Agronomy),
2 Place Pierre Viala, 34060 Montpellier, France
X. Han
College of Resources and Environmental Sciences,
Nanjing Agricultural University, Nanjing 210095,
People’s Republic of China
123
Hydrobiologia
DOI 10.1007/s10750-015-2413-z
(Currie & Kalff, 1984b). However, the quantity of Pi is
often insufficient to satisfy the demand of phytoplank-
ton in lakes (Wetzel, 2001; Gao et al., 2006 ; Nedoma
et al., 2006). The underlying mechanisms involved
and the rate of P regeneration are therefore some of the
important factors that control nutrient status and
primary productivity of lakes (Jansson et al., 1988).
One of the significant ways to regenerate is through the
decomposition of organic matter by enzymes. Partic-
ularly, the enzyme alkaline phosphatase (AP) is
responsible for the hydrolysis of dissolved organic
phosphorus (DOP) to compensate for the lack of P
(Labry et al., 2005).
AP as a hydrolytic enzyme can split phosphate
monoester bonds of organic P and release Pi at alkaline
pH (Tanaka et al., 2008). Its role in the biogeochem-
ical cycle of P has been confirmed by numerous
studies (Labry et al., 2005; Dyhrman & Ruttenberg,
2006; Raheb et al., 2006; Cao et al., 2009b). Alkaline
phosphatase activity (APA) is generally regulated by
external Pi conce ntration (Tanaka et al., 2008;). Also,
several studies indicated that cellular (phosphorus cell
quota) rather than external phosphorus controlled
APA (Litchman & Nguyen, 2008; Meseck et al., 2009;
Cao et al., 2010). As an inducible enzyme, the level of
APA can therefore be used as a convenient indicator of
P deficiency, although several studies also observed
that the relationship between APA and P concentration
was random or insignificant in some aquatic systems
(Jamet et al., 1997; Cao et al., 2009a). Most studies
have shown that phytoplankton and bacteria are the
most known to have significant APA (Labry et al.,
2005; Nedoma et al., 2006; Cao et al., 2009b);
however, some evidence also suggest that AP can
also be released by large zooplankton (Jansson et al.,
1988). Most papers have evaluated the total APA on
unfiltered samples or separate particulate and dis-
solved APA, considering that algae or bacteria repre-
sent the bulk of partic ulate APA (Labry et al., 2005;
Dyhrman & Ruttenberg, 2006). Other studies also
evaluated APA from plank ton fractions, specific
phytoplankton species, or even individual cells
(Rengefors et al., 2001; Hernandez et al., 2002; Raheb
et al., 2006). Even if size fractionation by filtration is
never completely absolute (i.e., overlapping size), it
still provides useful insights on the major microor-
ganisms possibly contributing to APA. However,
surveys dealing with simultaneous fractionation of
algal and bacteria are relatively scarce (Labry et al.,
2005).
Hydrodynamic turbulence is an intrinsic and ubiq-
uitous characteristic of aquatic environments, espe-
cially for the large shallow lakes which are strongly
influenced by wind waves (Cardoso & Marques,
2009). It has been shown that turbulence can accel-
erate nutrient transport toward a cell and enhance
nutrient uptake, especially at low nutrient levels
(Barton et al., 2014). Generally, in lakes, P is
considered as the limiting factor for phytoplankton
growth (Labry et al., 2005; Dyhrman & Ruttenberg,
2006; Tanaka et al., 2006, 2008). As an inducible and
hydrolytic enzyme, AP plays an important role in
phosphorus recycling process when Pi is low in lakes.
Therefore, because water turbulence is important in
nutrient uptake, the expression of APA may also be
related to it. Unfortunately, the direct relationship
between these two significant variables, turbulence
and APA, are rarely explored in lake waters.
Lake Taihu (Taihu) is the third largest freshwater
lake in China, with a total area of 2338 km
2
(Qin et al.,
2007). It is a typical shallow eutrophic lake, with an
average depth of 1.9 m and a maximum depth of
2.6 m, thus, it is strongly influenced by wind waves
(Qin et al., 2007). However, dense surface harmful
cyanobacterial blooms of the cyanobacterium Micro-
cystis have occurred every summer for the past 30
years, even though the Pi levels of aquatic were very
low (Qin et al., 2010). The ability of the cyanobacteria
to survive in nutrient-limited environment suggests
one of the abilities to adapt to such scenarios, one
unexplored possibility, is the regulation of AP to
survive non-optimal conditions. Interestingly, wind
waves were suggested to an important variable that
allowed formation and expansion of cyanobacterial
blooms in Taihu (Wu et al., 2013; Zhu et al., 2014).
In this study, we hypothesize that there is a link
between turbulence and APA, and that this coupling
has significant implications to the growth of some
groups of algae (i.e., cyanobacteria) during nutrient
starvation. To further investigate and provide evidence
to such questions, a mesocosm experiment was carried
out. Specifically, this study aims to (1) better under-
standing the nutrient strategies of phytoplankton and
bacterioplankton in turbulent environments, and (2)
investigate the effects of turbulence on APA of the two
planktonic groups.
Hydrobiologia
123
Materials and methods
Experimental setup
A total of twelve units of customized tanks made of
8-mm-thick Plexiglass and have maximal capacities
of 126 l (Fig. 1 ) were used for the mesocosm
experiments. Artificial waves were generated by
frequency conversion wave-maker pumps (WP,
Jebao, China), and rebounds were reduced by the
slopes (5:1) on the sides (Fig. 1a) where energy
dissipation plates are also fixed (Fig. 1b). Chemical
contamination from the material was avoided by
immersing the tanks in water for 15 days before
being used for any experiment.
Experimental design
Experiments were only conducted for 9 days to lessen
potential variances caused by bottle effects. The
bioassay experiments were performed from the 7 to
the 16 of July 2014 at TLLER (Taihu Laboratory for
Lake Ecosystem Research, Chinese Academy of
Science) on the shores of Lake Taihu, in Wuxi. A
total of 96 l of lake’s subsurface water (\0.2 m) was
filled in the tank. The tanks were then floated and fixed
in an outside artificial pond (10 9 10 9 2 m) which
was filled with lake water and dug 1 m into the ground
to simulate natural conditions. Since adhesion of
microorganisms could occur and affect the result, the
inside walls of each tank (except the bottom) were also
gently brushed at 6:30 p.m. every day.
Turbulence generation
The submerged wave-maker pumps, fixed under
surface water by strong magnets, were used to
generate turbulence simulation to the ones induced
by natural wind waves as demonstrated in previous
studies (Clarke et al., 2005; Pekcan-Hekim et al.,
2013;Ha
¨
rko
¨
nen et al., 2014).
The pump frequency was set to 1 Hz and the
turbulence generated was monitored and measured by
an acoustic Doppler velocimeter (ADV, 10 MHz
ADVField; Sontek/YSI, San Diego, California,
USA). The turbulence intensity was measured from
the middle of the tank with a 25 Hz measurement for a
period of 2 min. Measurements were performed after
the turbulent motion in the tank had reached a steady
state (after 6–7 min).
To define the characteristic speed of the turbulence,
the root mean square (RMS) velocity (cm s
-1
) was
calculated by using the following formula:
RMS ¼
ffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffi
l
2
RMS
x
þ l
2
RMS
y
þ l
2
RMS
z
q
; ð1Þ
where
l
RMS
x
¼
ffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffi
P
l
2
x
P
l
x
ðÞ
2
=n
n 1
s
; ð2Þ
Fig. 1 Diagram of the
mesocosm tank (a) used in
the experiments which
includes an energy
dissipation plate (b) and a
wave-maker pump (c ). All
dimensions are in centimeter
Hydrobiologia
123
is the fluctuation of the flow for Cartesian vector x
(which is similarly calculated for the y and z vectors)
and n is the number of samples per measurement. The
RMS velocities were expressed as averages for the
whole tank. The energy dissipation rate (e,m
2
s
-3
),
which describes the rate at which the turbulent energy
decays over time, was deduced from the RMS velocity
(m s
-1
) following the formula described by Sa nford
(1997):
e ¼ A
1
RMS
3
l
; ð3Þ
where A
1
is an dimensional constant of order 1 (Kundu
& Cohen, 2010), and l is the water depth (m) describing
the size of the largest vortices.
The Reynolds number ( Re, the ratio of inertial
forces to viscous forces) for the given turbulence
levels was calculated following Peters & Redondo
(1997):
Re ¼
RMSl
v
; ð4Þ
where l is the water depth (m ) and v is the kinematic
viscosity for water (8.5 9 10
-7
m
2
s
-1
).
The dif ferent levels of turbulence intensities used in
this study were based on actual conditions previously
observed in Lake Taihu on summer 2013. In Taihu, the
e vari ed between 6.01 9 10
-8
and 2.39 9 10
-4
m
2
s
-3
(Table 1), which corresponded to the range of
values (from 1.07 9 10
-7
to 6.67 9 10
-3
m
2
s
-3
)
previously measured by G.-To
´
th et al. (2011) in the
large shallow Lake Balaton. The calm condition
(0 cm s
-1
) which is without any hydrodynamic
turbulence was the control. The other 3 RMS veloc-
ities which also correspond to the different turbulent
intensities used in the experiments were 0.85 cm s
-1
(low), 2.53 cm s
-1
(medium), and 4.33 cm s
-1
(high). These intensities have corresponding e ranging
from 1.12 9 10
-6
to 1.48 9 10
-4
m
2
s
-3
with Re
between 5500 and 92,620 in Taihu (Table 1). All
treatments were conducted in triplicate.
Measurements
Physical and chemical parameters were measured
every day from day 0 to day 9, between 7:00 and 8:00
in the morning. Water temperature (WT), dissolved
oxygen (DO), and pH were determined using a 6600
multi-sensor sonde (Yellow Springs Instruments, San
Diego, California, USA). Nutrients were also analyzed
including total nitrogen (TN), total dissolved nitrogen
(TDN), total phosphorus (TP), total dissolved phos-
phorus (TDP), and phosphate (Pi), following the
methods described in Zhu et al. (2014). The particulate
fractions of nitrogen (PN ) and phosphate (PP) were
obtained by subtracting the TDN/P from the TN/P. On
the other hand, the dissolved organic phosphorus
(DOP) was estimat ed from difference of the Pi from
the TDP.
Biological samples were also collected by sampling
0.45 l of vertically integrated water everyday using a
tube sampler. The chlorophyll a (Chl a) concentrations
were measured by spectrophotometric method
(Pa
´
pista et al. 2002). Samples were first filtere d
through GF/F filters, frozen at -20°C, and pigments
were extracted with 90% hot acetone. To measure the
APA, water samples were first filtered through a
112 lm mesh net to remove large zooplankton. Then
the sample s were divided into two subsets according to
particle size onto which the APA is associated with.
Size fractionations were carried out with polycarbon-
ate membrane filters (Millpore, Cork, Ireland) with
Table 1 Summary of the root mean square (RMS) velocities,
energy dissipation rates (e), and Reynolds numbers ( Re) of the
four levels turbulence (treatments) used in the experiments
which include the (1) control (calm water), (2) low, (3)
medium, and (4) high turbulence intensities
Turbulence level RMS velocity (cm s
-1
) e (m
2
s
-3
) Re
Control 0 0 0
Low 0.85 1.12 9 10
-6
5500
Medium 2.53 2.95 9 10
-5
16,371
High 4.33 1.48 9 10
-4
92,620
Lake Taihu 0.49–7.69 6.01 9 10
-8
to 2.39 9 10
-4
2882–180,941
Hydrobiologia
123
pore sizes of 0.2 lm for bacterioplankton and 2.0 lm
for the larger phytoplankton (Nedoma et al., 2006).
The enzymatic activit ies were measured in the differ-
ent filters by spectrophotometric method as the release
of p-nitrophenol from the model substrate p-nitro-
phenyl phosphate (pNPP) (Gao et al., 2006). The assay
mixture contained 2 mL of samples, 1 mL of 0.5 mol
l
-1
Tris buffer solution (pH 8.4), and 2 mL of freshly
prepared mi llimolar pNPP. Samples were incubated
for 6 h at 30°C in the dark. The absorbance at 410 nm
was measured with a 1 cm quartz cuvette in a UV–Vis
recording spectrophotometer (UV-2401 PC, Shi-
madzu, Japan). Phosphatase activity was conver ted
to absolute units using a standard curve based on
enzymatically hydrolyzed p-nitrophenol. All samples
were run in triplicate. The APA fra ctions were
classified according to the filtrate from which they
were recovered. In this study, they are referred to as
total (TAPA; 112 lm), dissolved (DAPA; 0.2 lm),
bacterioplanktonic (BAPA; 0.2–2.0 lm), and phyto-
planktonic APAs (PAPA; 2.0–112 lm). The specific
phytoplankton APA was estimated by dividing the
PAPA by Chl a.
Statistical analysis
Test for significant differences among and between the
various treatments, one-way analysis of variance
(ANOVA) was employed. Post hoc multiple compar-
isons of treatment means were performed by Tukey’s
least significant difference procedure and the standard
deviation in the variations of the triplicates was
calculated. Relationships between APA and P
fractions were explored by Pearson’s correlation
coefficient. All statistical calculations were performed
in Statistical Product and Service Solutions (SPSS
22.0) statistical package for personal computers, and
the level of significance used was P \ 0.05 for all tests
(Yockey, 2010).
Results
Physical conditions, N:P, and Chl a
The water temperature ranged from 25.6 to 30.2
°
C
with DO and pH higher in the control than the
treatments (low, medium, and high) during the exper-
iment (Table 2, P [ 0.05). The TN concentrations
were also significantly higher in the treatments
(1.8 ± 0.13 mg l
-1
) than in the control
(1.6 ± 0.19 mg l
-1
, Table 2, P \ 0.05). In addition,
although TN:TP and TDN:TDP ratios were generally
higher in the control than in the treatments, the
differences were not significant (Table 2, P [ 0.05).
However, the opposite was observed for the PN:PP
mass ratio where it was relatively sma ller in the
control than in the treatments (Table 2, P [ 0.05).
The Chl a concentrations fluctuated significantly in
the different treatments and the length of time needed
to reach maximum concentrations also varied. Gener-
ally, it was observed that Chl a increased the fastest to
a maximum of 41.7 and 45.7 lgl
-1
at day 2 in low and
medium treatments, while those in high took more
than 3 days to reach 48.6 lgl
-1
(Fig. 2). On the other
hand, Chl a in the control gradually decreased after
Table 2 Mean and standard deviation of the measured phys-
ical and chemical parameters in the different turbulence
treatments during the experiment which include water temper-
ature (WT), dissolved oxygen (DO), total nitrogen (TN), the
mass ratios of total nitrogen over total phosphorus (TN:TP),
total dissolve nitrogen over total dissolve phosphorus
(TDN:TDP), and of particulate nitrogen over particulate
phosphorus (PN:PP)
Parameters Control Low Medium High
WT (
°
C) 27.51 ± 1.31 27.51 ± 1.36 27.53 ± 1.36 27.49 ± 1.35
pH 8.77 ± 0.33 8.67 ± 0.28 8.57 ± 0.25 8.53 ± 0.23
DO (mg l
-1
) 8.58 ± 1.27 7.71 ± 0.43 7.77 ± 0.46 7.73 ± 0.42
TN (mg l
-1
) 1.64 ± 0.19 1.70 ± 0.15 1.85 ± 0.10 1.83 ± 0.08
TN:TP 35.19 ± 9.93 31.73 ± 7.79 30.30 ± 5.49 31.99 ± 8.14
TDN:TDP 132.51 ± 83.17 100.13 ± 48.32 115.07 ± 95.67 88.17 ± 33.57
PN:PP 14.67 ± 4.98 16.54 ± 6.08 17.06 ± 6.38 16.10 ± 5.58
Hydrobiologia
123
peaking on day 1 with 37.7 lgl
-1
(Fig. 2). Also, the
9-day average of pigment concentrations in the control
(20.5 ± 7.5) was lower compared to the treatments
(low = 27.2 ± 9.6, medium = 31.8 ± 9.1, and
high = 29.2 ± 12.5 lgl
-1
; Fig. 2, P [ 0.05).
P fractions
TP concentrations observed ranged from 0.032 to
0.092 mg l
-1
during the experiment. Fractions of the
different forms of phosphate (TP/PP and TDP/DOP)
fluctuated on the first few days of the experiment but
became stable and continued to increase in the
turbulent conditions after 6 days (Fig. 3). Moreover,
Pi became depleted on the first 4 days but surprisingly
increased again on the succeeding 4 days. In addition,
recovery of the inorganic phosphate was higher in the
treatments (Fig. 3e). Similarly, Pi/Chl a ratio which
reflects the available phosphorus per phytoplankton,
drastically decreased at first but increased after 4 days,
although it was smaller in the treatments than in the
control from day 2 to day 6 (Fig. 3f).
APA fractions
Since the treatments were not supplant ed with nutri-
ents, levels of TAPA increased quickly before day 4
and then remained stable until the end of the study,
except in low treatment where it exhibited stationary
decrease after day 6 (Fig. 4a). Interestingly, TAPA
was lower before day 2 and then became much higher
in the turbulence treatments ([7.2 nmol l
-1
min
-1
)
the succeeding days, generally higher than in the
control (4.5 ± 1.5 nmol l
-1
min
-1
; Fig. 4a). During
the experiment, PAPA consisted most of the TAPA
(66–93%). Like the Chl a, PAPA significantly
increased on the first few days of incubation but
slowly declined toward the end of the study. In
addition, PAPA was significantly higher in the treat-
ments, particularly in medium and high (6.5 ± 2.9 and
6.6 ± 3.0 nmol l
-1
min
-1
), than in the control
(3.2 ± 0.98 nmol l
-1
min
-1
; Fig. 4b, P \ 0.05). On
the other hand, the remaining fractions of TAPA were
shared by BAPA (3.1–21.8%) and DAPA
(1.7–22.6%), both of which increased slowly during
the experiment (Fig. 4c, d). Interestingly, compared to
the PAPA, BAPA and DAPA were lower in
the treatments than in the control before day 6
(P [ 0.05), and then became slightly higher after-
wards (Fig. 4c, d).
The relationship between APA and P fractions
Correlations between APA and P fractions are sum-
marized in Table 3. The TP and PP were significantly
negatively correlated with all APA fractions
(P \ 0.001). The Pi on the other hand only had
negative correlations with TAPA and PAPA
(P \ 0.05). However, no pattern was observed
between TDP, DOP and all APA fractions
(P [ 0.05). The TN:TP and PN:PP ratios are posi-
tively correlated with all APA fractions (P \ 0.001),
while TDN:TDP ratio had significant negative corre-
lations with TAPA and specific PAPA (P \ 0.05).
Discussion
Although many studies have examined the relation-
ship between APA and P (Labry et al., 2005; Tanaka
et al., 2006; Cao et al., 2009a), as well as the spatial
and temporal variation of APA (Zhou & Zhou, 1997;
Nedoma et al., 2006; Zhang et al., 2007), fewer studies
have explored the direct relationship between turbu-
lence and APA fractions in lakes. Results in this study
showed that the phytoplanktonic APA was enhanced
but bacterioplanktonic APA was reduced by turbu-
lence in short-term exposure (6 days, Fig. 4). Also,
total APA was significantly correlated with phospho-
rus (TP, PP, and Pi) and nitrogen-phosphorus ratios
Fig. 2 Variations of Chl a in the different turbulence treat-
ments during the experiment including control (black square),
low (circle), medium (triangle), and high (inverted triangle)
Hydrobiologia
123
(Table 3, P \ 0.05). This suggests that possibly,
turbulence has contributed to the acceleration of the
biogeochemical cycle of P and the growth of phyto-
plankton (mainly harmful Microcystis; Figs. 2, 4). The
same conditions have been suggested to play a role in
the formation of cyanob acterial blooms in Lake Taihu.
For example, strong wind events were found to
stimulate significant algal toxicity and cyanobacterial
growth leading to blooms in the lake on summer (Zhu
et al., 2014).
Most studies have indicated that when external
soluble reactive phosphorus (SRP) are depleted, the
algae and bacteria begin to synthesize AP, which are
relatively stable and can hydrolyze phosphate esters as
an alternative phosphorus source to compensate for
the lack of P (Jan sson et al., 1988; Labry et al., 2005;
Fig. 3 Variations of phosphorus fractions (a, TP; b, PP; c,
TDP; d, DOP; e, Pi) and the ratio of Pi over Chl a (f) in the
different turbulence treatments during the experiment. Control
(black square), low (circle), medium (triangle), and high
(inverted triangle). TP total phosphorus; PP particulate
phosphorus; TDP total dissolved phosphorus; DOP dissolved
organic phosphorus; Pi phosphate
Hydrobiologia
123
Nedoma et al., 2006; Cao et al., 2009a). However, the
inducible threshold of APA is restricted to a certain
level of Pi concentration, which depends on the
ecosystem and its physi cal and chemical characteris-
tics (Labry et al., 2005; G.-To
´
th et al., 2011). In Taihu,
when the concentration of SRP is less than 0.02 mg
Fig. 4 Variations of alkaline phosphatase activity (APA)
fractions in the different turbulence treatments during the
experiment. a, total APA; b, phytoplanktonic APA; c,
bacterioplanktonic APA; d, dissolved APA. Control (black
square), low (circle), medium (triangle), and high (inverted
triangle)
Table 3 Summary of the correlations of alkaline phosphatase activity (APA) fractions such as total (TAPA), phytoplanktonic
(PAPA), bacterioplanktonic (BAPA), dissolved (DAPA), and specific PAPA (PAPA/Chl a) on different P fractions
TAPA PAPA BAPA DAPA Specific PAPA
TP -0.62 -0.49 -0.71 -0.87 -0.80
TDP -0.18 -0.14 -0.22 -0.20 -0.16
PP -0.60 -0.47 -0.70 -0.85 -0.81
DOP -0.081 -0.023 -0.24 -0.27 -0.14
Pi -0.34 -0.39 0.019 0.12 -0.10
TN:TP 0.54 0.41 0.62 0.80 0.77
TDN:TDP -0.33 -0.30 -0.24 -0.26 -0.36
PN:PP 0. 80 0.70 0.68 0.77 0.89
Pearson’s correlation coefficient was applied and the sample number was 40
Bold values indicate that the correlation is significance (P \ 0.05)
Hydrobiologia
123
l
-1
or when the mass ratio of TN over TP is above 22,
the APA significantly increases (Gao et al., 2006),
suggesting it is characteristic of P limitation. In this
study, the average concentration of Pi and TN:TP ratio
were 0.003 ± 0.002 mg l
-1
and 32:1, respectively.
Therefore, to compensate for the lack of P, AP was
naturally synthesized to hydrolyze organic P (Fig. 4).
Moreover, the specific activity of alkaline phosphatase
(APA/Chl a) has been suggested to be a good indicator
of P limitation for algal growth (Nedoma et al., 2006;
Tanaka et al., 2006; Ivancic et al., 2012).
During the experiment, the harmful cyanobac-
terium Microcystis was always the dominant species
in all treatments (except in high after 8 days). Also,
phytoplanktonic APA always dominated the total
APA, which is also widely observed in lakes (Cao
et al., 2009a, 2010) and in coastal waters (Jamet et al.,
1997; Labry et al., 2005). However, unlike APA,
bacterioplanktonic and dissolved APA were reduced
before the day 6 under turbulent conditions (Fig. 4).
Turbulence, which causes mixing and thus affecting
the physical and chemical properties of the water
column, increases the diffusion rate in the cell surface
(reviewed by Guasto et al., 2012) and enhanc es the
uptake of nutrients (Bergstedt et al., 2004; Honzo &
Wuest, 2008; Prairie et al., 2012). These in turn
accelerates the reduction of nutrient in water. How-
ever, in the proce ss of P uptake, the competitive
success of bacteria versus phytoplankton for Pi has
been widely confirmed under turbulent conditions at
low Pi concentration due to surface-to-volume ratio
(Currie & Kalff, 1984a; Drakare, 2002; Honz o &
Wuest, 2008). Therefore, phytoplankter was not
getting sufficient P to support their growth by com-
peting with bacteria, especially with turbulence.
Under these conditions, phyto plankton may also
upregulate proteins and enzymes to aid in P scaveng-
ing (Dyhrman & Ruttenberg, 2006). Another possi-
bility to overcome P limit ation is the abili ty of
phytoplankton to lower their physiological P demand
by as much as 50% (reviewed by Ivancic et al., 2012).
However, under external P limitation, phytoplankton
depends more directly on the intern al rather than
external P concentrations produced from accumulated
and stored excess P (Litchman & Nguyen, 2008). The
most effective way is to decompose the intracellular
stored organic P to compensate for P deficiency, and
alkaline phosphatase plays a key role in this process
(Feuillade et al., 1990), with significant positively
correlations between PN:PP and all APA fractions
(Table 3, P \ 0.001). On the other hand, the exper-
iment showed that the available phosphorus per
phytoplankton (Pi/Chl a ratio) was smaller in the
turbulence treatments than in the control from day 2 to
day 6 (Fig. 3f). Interestingly, at the same time (that is
from day 2 to day 6), phytoplanktonic APA increased
much faster in the tur bulence treatments than in the
control (Fig. 4b). This may explain why phytoplank-
tonic APA was enhanced but the bacterioplanktonic
APA was reduced before 6 days by turbulence.
However, as the available phosphorus depleted in
water, the bacterioplankton also have to synthesize AP
to hydrolyze the stored P in cells (Fig. 4c) resulting to
gradual slow increase toward the end of the experi-
ment. Furthermore, when the intracellular stored
organic phosphorus reservoirs were depleted, the AP
had to be released to hydrolyze DOP in the water so
causing that the dissolved APA to increase (Fig. 4d).
Consequently, turbulence promoted the APA and
increased the Pi concentration that accelerated the
growth of harmful algae (Figs. 2, 3, 4). These results
are consistent with previous observations in Taihu
where the maximal values of APA were detected in
western estuary (river estuary) and central region of
the lake (Gao et al., 2006; Nu et al., 2009), which are
known to be strongly influenced by turbulence.
Similarly, APA is also enhanced by wind wave
turbulence when the artificial sand barrier was opened
in coastal waters (Panosso & Esteves, 2000).
However, even though fractionation was performed
to determine the relative APA contribution of the
different groups, several caveats are still needed to be
considered which may affect the results such as
overlapping sized and breaking of cells (Labry et al.,
2005). Specifically, the proportion of particulate-
bound bacteria was not assessed in this study and the
filtration procedure was unable to evaluate the relative
contribution of the community to total APA. However,
the proportion of BAPA which only makes up a small
portion (1.8–22.6%) of the total APA could also
suggest that the attached bacteria only represented a
small part of phytoplanktonic APA. Consequently, it
can be assumed that the 2–112 lm size fraction
corresponded essentially to the phytoplankton and the
0.2–2 lm size fraction to bacterioplankton.
Because Lake Taihu is very shallow, it is strongly
influenced by wind wave turbulence and the turbulent
kinetic energy content which are much higher than
Hydrobiologia
123
those in stratified deep lakes and even in the open
ocean (G.-To
´
th et al., 2011). However, In Taihu, the
cyanobacterial blooms have occurred every summer
and threaten the supply of drinking water and
fisheries-related products for more than 8 million
people, resulting to great economic losses (Qin et al.
2007). This study has demonstrated that turbulence is
an important driver of biogeochemical perturbations,
and can accelerate the biogeochemical cycle of P,
which have implications on the dynamics of harmful
algal blooms. Thus, it should be carefully considered
and integrated in bloom management and forecasting.
Conclusion
Determination of alkaline phosphatase activity (A PA)
is considered to be a convenient and useful proxy for
detecting P deficiency in Lake Taihu. This study based
on mesocosm experiment demonstrated that turbu-
lence promoted the phytoplanktonic APA and accel-
erated the biogeochemical cycle of P. Also, turbulence
promoted the growth of harmful algae (mainly
Microcystis), which is beneficial to harmful cyanobac-
terial blooms. Our results contribute to the better
understanding the P strategies of phytoplankton and
bacterioplankton in turbulent environment.
Acknowledgments We appreciate the very thorough and
constructive reviews provided by two anonymous reviewers.
This research was supported by the National Natural Science
Foundation of China (41230744).
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