VERTICAL
PRODUCTION
DISTRIBUTION
AND ORGANIC MATTER
OF PHOTOSYNTHETIC
SULFUR BACTERIA
IN JAPANESE LAKES
Masayuki
Botanical
Institute,
Faculty
Takahashi and Shun-ei Ichimura
of Science,
Tokyo
Kyoiku
University,
Otsuka,
Tokyo,
Japan
ABSTRACT
The role of photosynthetic
sulfur bacteria as primary producers in stagnant lakes having
hydrogen sulfide is described.
Photosynthetic
bacteria normally
appear at the boundary
layer of the oxidative and reductive zones, where H& is present and the light intensity is
lower than 10% of the surface value. The water of this layer was milky green or pink
due to dense populations
of Thiorhodaceae
or Chlorobacteriaceae.
The amount of photosynthetic bacterial biomass measured on a chlorophyll
basis ranged from 100 to 828 mg/m3
for Chl-650, 60.7 to 79.5 mg/m3 for Chl-660, and 19.8 to 186 mg/m* for BChl in the
growing period from July to October.
In the lakes studied, organic matter was produced by phytoplankton
in the epilimnion
and mainly by photosynthetic
sulfur bacteria in the reducing zone. The organic matter
synthesized by these bacteria ranged from 9 to 25% of the total annual production
in
lakes rich in H,S and from about 3 to 5% in lakes poor in it.
INTRODUCTION
WC express our sincere thanks to Dr.
T. R. Parsons for his kind help in prcparation of this manuscript.
The interest of aquatic ecologists in organic matter production has been focused
on green plants, including phytoplankton
METHODS
and phytobenthos
as principal
primary
producers in the aquatic ecosystem.
Measurcmcnts were made in 10 lakes
In certain waters having an anoxic envi( Fig. 1) having an anoxic layer throughronment, such as meromictic lakes, hydroout the year or during summer stagnation.
gcn sulfide can be detected in the hypoWater samples were taken from various
limnion
throughout
the year, while in depths with plastic Van Dorn samplers.
others it can only be detected during
Light attenuation was measured with a
summer stratification.
During these pcriselenium underwater
photometer
fitted
ods, photosynthetic
bacteria frequently
with a neutral glass filter, temperature
grow vigorously in the upper layer of the with a thermistor thermometer. Chemical
I-12s zone. To understand fully the proanalysts were made according to the production of organic matter in these bodies
cedures of the American Public Health
of water, one must cxplorc the role of Association
( 1960). After careful samof 1-12s was carphotosynthetic
sulfur bacteria as well as pling, the determination
that of the phytoplankton.
ricd out by iodometry in waters rich in it
A number of investigators have studied
and by calorimetry
in waters with low
concentrations. The rate of photosynthesis
the distribution of photosynthetic bacteria
was mcasurcd in an incubator and in situ
in natural waters (Kuznetsov 1958; Konusing radioactive
carbon. Total carbon
drat’eva 1965; Wood 1965; Pfennig 1967).
Studies of these bacteria from the standdioxide in the water sample to be used
for the estimation of photosynthetic
rate
point of organic matter production arc rclwas measured by a modified Conway’s
atively few aside from those of Kuznetsov
method.
The density of
( 1959) and Sorokin ( 1964)) although the microdiffusion
phytoplankton
and photosynthetic bacteria
of this field has gradually
importance
in water was determined by measuring
This study was unbecome recognized.
dcrtaken to expand our knowledge of this pigments or by counting cells. Materials
for the analysis of pigment were collcctcd
aspect.
644
PHOTOSYNTIIETIC
4
0
I
SULFUR BACTERIA
1’
‘J
645
PRODUCTION
--r
km
FIG. 1. Bathymetric
features of lakes. x indicates sampling station; number is water depth in meMesotrophic-eutrophic
lake: 8. Hiters. Mesotrophic
lakes: 1. Haruna;
2. Yuno-ko;
6. Hamana.
7. Suigetsu;
9. Suga;
4. Shinsci;
5. Kisaratsu Reservoir;
ruga. Eutrophic
lakes : 3. Waku-ikc;
10. IIarutori.
by filtering
water samples of 0.5 to 2
liters through an HA Milliporc filter in the
field.
The filters were kept cold and
brought back to the laboratory; pigments
were extracted in 90% acetone after treatmcnt with a sonic oscillator ( Sonicator, 10
kc, Kubota Co. Ltd., Tokyo) for 10 min.
Determination
of chlorophyll a was made
by the method of Richards with Thompson
( 1952). Optical densities were measured
with a Hitachi Beckman Model 137 spcctrophotometer. Chlorobium chlorophyll 650
( Chl-650) and chlorophyll 660 ( Chl-660)
were determined
equations :
from
the
following
Chl-650 (mg/m3) = 10.2 x Des4 x F;
Chl-660 ( mg/m3) = 10.8 x DGezx F.
Both equations were obtained using the
specific absorption coefficients of 98.0 ml
mg-l cm for Chl-650 and 92.1 ml (mg cm)-l
for Chl-660 in acctonc (Stanier and Smith
1960).
Smith and Benitez (1955) gave a spccific absorption coefficient of 46.2 ml (mg
cm)-l for bacteriochlorophyll
( BChl) in
646
MASAYUKI
TAKAHASHI
methanol. This value could not be used
directly
in our study for determining
BChl, because pigments were extracted
with 90% acetone. The factor was recalculated from a direct comparison of absorbance in 90% acetone and in methanol.
From the values obtained, the following
provisional equation was derived :
AND SHUN-E1
ICHIMURA
LIGHT
INTENSIIV
(%I
BChl (mg/m3) = 25.2 x OTT2X F.
D is the optical density determined in a
l-cm ccl1 after correcting for a blank at
850 m,u. F was calculated from the exprcssion :
1
F=+xz,
where v was the volume of the 90%
acetone extract in ml, V was the volume of
water sample filtered in liters, and L was
the length of light path through the absorption cell in cm.
Phytoplankton
samples were prepared
by centrifuging lake water and resuspending in l/lo the volume oI the original
sample; the cells were counted in a l-ml
chamber. Counts of bacteria wcrc made
on a Millipore filter stained with Lijffler’s
mcthylene
blue.
Although
new media
have been reported by Schlegel and Pfennig ( 1961)) cultures of photosynthetic sulfur bacteria were made using the classical
inorganic medium of Larsen for green
sulfur bacteria and that of Van Niel for
purple sulfur bacteria.
RESULTS AND DISCUSSION
Physicochemical conditions of the lakes
during summer stratification
During
summer stagnation, all lakes
were well stratified. The intensity of light
decreased exponentially
with depth until
the upper layer of the reductive zone
where there was a sharp break below
by
which light was absorbed rapidly
highly turbid water (Fig. 2). Approximately
0.5 to 10% of the surface illumination
penetrated into the upper layer of the reductive zone.
Thermal stratification was present in all
lakes (Fig. 3) and was most pronounced
in Lake Waku-ike, where there was a
FIG. 2.
Light
attenuation
rates.
Horizontal
lines indicate
border layer between photic and
reductive
zones. 1. Waku-ike,
17 July 1965; 2.
Harutori,
9 September
1965; 3. Kisaratsu,
18
August 1966; 4. Same, 2 September 1965; 5.
Suga, 20 July 1966; 6. Suigetsu, 20 July 1966;
7. Yuno-ko,
30 August 1966; 8. Haruna,
14
October 1964; 9. Hiruga, 21 July 1966.
temperature gradient of 12C in the thcrmoclinc.
There was a definite stratification
of
dissolved oxygen, and almost all lakes had
a more or less reductive zone in the hypolimnion ( Fig. 3). Oxygen concentration in
the surface water varied from 6 mg/liter
to 10 mg/liter.
A maximum oxygen concentration, probably due to photosynthesis of phytoplankton,
was generally measurcd in waters of 2- to 4-m depth, except
that in Kisaratsu Reservoir and Lake
Suigetsu oxygen was nearly uniform within
the photic zone. Oxygen decreased rapidly in the metalimnion and disappeared
or was present in very small quantities in
the hypolimnion.
Hydrogen sulfide was
present in the reductive zone and there
was an abundance of it in the layer near
the bottom where no oxygen was detected.
The amount of H2S ranged from 0.5 to
1.6 mg S/liter in freshwater lakes and from
3.0 to 413 mg S/liter in brackish lakes.
Chloride concentration was low in freshwater lakes, but in brackish lakes showed
a noticeable stratification:
The surface
layer contained relatively
little chloride,
but the hypolimnion 7 to 16 times as much.
A typical example is shown in Kisaratsu
PIIOTOSYNTHETIC
SULFUR
cl-g/l
mg/ I
a 02- 5
0 0
IO
“c
BACTERIA
647
PRODUCTION
HIS-S “‘g/l
10 0 , , . . so
,
FIG.
3. Vertical changes of dissolved oxygen ( 0 ), hydrogen
sulfide ( S ), water temperature
(T ),
chlorinity
( CL ), and pH (pH ) . 1. Yuno-ko, 30 August 1966; 2. Hamana, 29 August 1965; 3. Suga,
20 July 1966; 4. Harutori,
9 September 1965; 5A. Waku-ike,
17 July 1965; 5B. Same, 26 February
1939; 6. Shinsei, 8 July 1966; 7. Kisaratsu, 18 August 1966; 8. Haruna, 14 October 1964; 9. Suigetsu, 20 July 1966; 10. Hiruga, 21 July 1966.
Reservoir, where low salinity water (to
5-m depth) overlaid higher salinity water
beneath.
The surface water was generally alkaline and the hypolimnion neutral. Vertical
changes in pI% were considerable in freshwater and slight in brackish lalcs.
In
freshwater Lake Shinsei, the maximum pH
was 9.0 in the surface water with a minimum of 7.0 in the hypolimnion.
The high
PI-I of the surface water was presumably
the result of photosynthesis
by phytoplankton.
Vertical
of the crude extracts in 90% acetone for
surface water and for colored waters from
the anoxic layers are shown in Fig. 4. The
dominant
species in the surface water
were diatoms. The colored waters con-
distribution
of photosynthetic
bacteria
Pigments of planktonic organisms
Changes in the propertics of planktonic
populations
with depth were estimated
by comparing the absorption spectra of
acetone extracts of residues collected from
various depths. Typical absorption spectra
400
5io
.
600
WbVE~LENGTtl
600
700
'
fl!J
FIG.
4. Absorption
spectra of crude extracts in
90% acetone from the surface water of a mesotrophic lake (A) and from colored waters taken
from anoxic layers of stagnant lakes (B, C, D),
648
MASAYUKI
TABLE 1.
Maximum
chlorophyll
TAKAHASHI
content
Max
chlorophyll
I
II
III
(mg/m”)
Chl
a
Shinsei
Yuno-ko
Hirugn
2.0
1.0
1.0
80.9
9e8
6.1
Harutori
Waku-ike
Hamana
1.0
2.0
5.0
20.8
76.1
3.6
10.0
1.0
7.0
8.5
13-14
11.0
23.5
19.8
( 9.3
( 13.0
( 19.8
Kisaratsu
Reservoir
1.0
2.3
Kisaratsu
Reservoir
Suigetsu
Suga
1.0
6.0
5.0
1.6
8.6
6.8
Chl650
Depth
(m)
chlorophyll
Plant
Depth
(4
Haruna
Depth
(m)
ICIIlMUl?A
Total
Bact.
Lake
(7.0
IV
SHUN-E1
in unit water volume and total chlorophyll
meter in waters studied
Plant
Pattern
AND
Chl660
Depth
(m)
BChl
Chl
content
(mg/ms)
Bact.
a
Chl650
Chl660
BChl
206
56.8
51.7
3.6
543
3.0
11.0
65.1
86.0
20.4
79.5
60.7
587
235
71.9?
56.4
98.2
36.1
8.5?
6.2
8.5
8.6
828
100
148
tained hydrogen sulfide and their green
or pink color was due to large populations
of sulfur bacteria. The curve for a surface
sample showed a maximum absorption in
the blue region and a second peak at
about 663 rnp, coinciding fairly well with
that of green plants. The curves for colored waters exhibited two sharp bands at
either 654 rnp or 662 rnp in greenish water
and at 663 mp and 772 rnp in pink water.
In the range of 400-500 rnp, a distinct
peak was shown at 470 rnp in green water
an d near 450 rnp in pink water. The peculiar peaks at 654, 662, and 772 rnp in
the red range were presumably due to the
absorption by such pigments as Chlorobium chlorophyll
650, 660, and bacteriochlorophyll
(Stanier and Smith 1960).
Chlorobium
chlorophyll
650 is probably
similar to Chlorobium kimicola chlorophyll
(Czeczuga 1965). Czeczuga has shown
that an 86% ethanol extraction of residues
collected from the thermocline of several
lakes in Poland has only one peak at 655
rnp, in contrast with a peak at 662.5 rnp
for samples collected in the photic zone.
Attempts to culture the green sulfur
bacteria in the absence of H2S were unsuccessful owing to the growth of a large
number of contaminating organisms. Samples of green water were then inoculated
into bottles containing Larsen’s medium
6.2
8.5
8.6
186
81.3
120
11.4
37.3
24.8
per square
24.9?
352
182
119
84.2
138
79.3
Date
8 Jul
31 Aug
21 Jul
1966
1966
1966
9 Sep
4 Aug
31 Aug
1965
1965
1965
15 Ott
2.2 Ott
1964
1966
1 Sep
16
20
20
Aug
Jul
Jul
1965
1966
1966
1966
through which H2S had been bubbled and
the bottles exposed to a continuous illumination of 3,000 lux. With exposure to
light, HZS disappeared from the medium a
few days after inoculation;
in the dark
thcrc was no such change, and no growth
of colored bacteria was observed. Thus,
the minute organisms coloring the water
of the reductive layer opaque green rcquired light and HZS for growth. These
organisms appeared to be green sulfur
bacteria,
possibly
Chlorobium
(Breed,
Murray, and Smith 1957). Jimbo ( 1938)
has shown that the dominant species in
the milky green water of the H$ zone in
Japancsc lakes are Chlorobium
limicola
and Chloronium
mirabile (= Chlorochromatium aggregatum >.
Similar culture experiments showed that
the bacteria predominating
in the pink
water layers also required light and HZS
for growth. Because acetone extracts of
the organisms exhibit an absorption maximum at 772 rnp, the organisms arc obviously Thiorhodaceae; morphologically
they
resemble Chromatium. This is in line with
the observations of Jimbo ( 1938), who reported that Chromatium okenii, C. weissei,
C. minus, C. vinosum, and C. minutissimum were dominant in the reddish water
of the H2S zone in Japanese lakes.
Since the peculiar absorption bands at
PHOTOSYNTHETIC
SULFUR
654, 662, 663, and 772 rnp observed in
acetone extracts are characteristic for individual samples taken from various depths
in the lakes, a comparison of the absorption curve for the samples was made in
the red region of 600-800 mp. Samples
taken from the photic layer showed one
absorption maximum at 663 rnp in the
range between 600 rnp and 800 rnp, indicating that phytoplankton
is dominant in
this zone. The position of the absorption
bands for the samples taken from the
anoxic layers was different for individual
lakes; the main absorption bands were
found at 654 and 662 rnp or 772 rnp, showing that photosynthetic sulfur bacteria are
dominant in the reductive zone.
The patterns of vertical distribution
of
planktonic organisms in lakes can be classified into four types according to the fcatures of their absorption spectra. The first
type is that in which the organisms in
the whole photosynthetic
layer are charactcrizcd by absorption curves with one
maximum peak at 663 rnp; the other
three types are distinguished respectively
through the presence or absence of Chlorobium chlorophyll or bacteriochlorophyll.
The pattern is not fixed in individual lakes
but changes seasonally or successionally.
In Kisaratsu Reservoir, which was built to
provide an industrial
water supply for
Kisaratsu on the eastern shore of Tokyo
Bay, the monimolimnion
water was pink
in September 1965 owing to the growth of
purple sulfur bacteria, but greenish red in
August 1966 owing to the prcsencc of both
green and purple sulfur bacteria.
Quantitative distribution
sulfur bacteria
of photosynthetic
Vertical changes in the quantities of
planktonic organisms measured by their
photosynthetic pigments are shown in Fig.
5. In lakes belonging to the first category
of chlorophyll
distribution,
chlorophyll
n
was dominant in both the oxidative and
reductive zones, but the amount of pigment contained in the reductive zone was
only 5 to 10% of the total amount of pigment in the lake (Table 1). Therefore, the
BACTERIA
l?RODUCTION
649
photosynthetic
production in these lakes
must be carried out mostly by phytoplankton living in the upper layer of the oxidative zone. In nearly all lakes of the
other three categories there was a considerable accumulation
of bacteria at the
boundary between the oxidative and reductive zones. Such a characteristic distribution of photosynthetic
sulfur bacteria
has been reported by Kuznetsov ( 1958),
Sorokin ( 1.964, 1966), and Anagnostidis
and Overbeck ( 1966) using direct counts
of bacterial cells. The amount of bacterial
chlorophyll we found ranges, at the maximal growth period, from 100 to 828 mg/
m3 for Chl-650, 60.7 to 79.5 mg/m3 for
Chl-660, and 19.8 to 186 mg/m3 for BChl.
These values were usually higher than the
total amount of plant chlorophyll
in the
euphotic zone. When an abundant mixed
population of green and purple sulfur bacteria was present, bacterial chlorophylls as
high as 1,000 mg/m3 were found, whereas
plant chlorophyll did not exceed 100 mg/
m3 from dense populations
in the oxidative zone. During stratification,
the total amount of bacterial chlorophylls
per
square meter of lake was 3 to 9 times that
of plant chlorophyll,
although the layer
containing
photosynthetic
bacteria
was
normally only 2 to 3 m thick. The same
relationship holds on a dry weight basis.
The bacteriochlorophyll
content is betwccn 1.6 and 2% of dry weight for cultured Chromatium
( Kondrat’eva
1965))
and a value of 0.6 to 1.2% would be expected for the chlorophyll of natural freshwater phytoplankton.
With these conversion factors ( on a dry weight basis), 1.5 to
4.5 times higher values can be estimated
for sulfur bacterial biomass than for phytoplankton.
In some lakes, nonsulfur purple bacteria such as Rhodospirillum
were
found among the photosynthetic
sulfur
bacteria, but they were not as abundant.
Primary
production by photosynthetic
bat teria
Vertical variation of in situ photosynthetic production and dark carbon uptake
of waters are illustrated in Fig. 6. The
650
MASAYUKI
TAKAIIASHI
AND SHUN-E1
ICHIMURA
]
Chl-a
ES4 Chl-650,
Chl-660
BChl
=
Chb650,
Chlm660,
BChl
0
5
50
55
FIG.
5. Vertical distribution
of chlorophyll
a, C1&wobium
660, and bacteriochlorophyll.
Dotted line indicates the upper
1966; 2. Yuno-ko, 30 August 1966; 3A. Kisaratsu, 14 July
Hiruga, 21 July 1966; 5. Suigetsu, 20 July 1966; 6. Suga, 20
8. Kisaratsu, 18 August 1966; 9. Hamana, 29 August 1965;
tori, 9 September 1965.
profiles with two photosynthetic
maxima,
one in the upper layer of the euphotic zone
and the other in the reductive zone, were
parallel with those of pigment distribution.
The upper photosynthetic
maximum is
common in phytoplankton
communities,
and it depends on the relationship between
photosynthesis
of surface phytoplankton
and the vertical gradient of light intensity
in the water. The deeper maximum rcsults mainly from photosynthetic
activity
of sulfur bacteria at the depth in question,
since vigorous growth of phytoplankton
will not occur in such a reducing environ-
chlorophyll
650, Chlorobiunt
chlorophyll
limit of anoxic zone. 1. Shinsei, 8 July
1965; 3B. Same, 10 August 1965; 4.
July 1966; 7. Haruna, 22 October 1966;
10. Waku-ike,
17 July 1965; 11. Haru-
mcnt and where light intensity is only 5 to
0.1% of the surface value. Dark fixation
of carbon was detected in the layer near
the bottom.
Table 2 shows that the maximum rate
of in situ photosynthesis by phytoplankton
during the most active period was 4.7-9.2
mg C m-3 hr-l; it was 0.3-154 mg C m-3
hr-l in areas where photosynthetic
sulfur
bacteria predominated.
The total daily
production of organic matter was 167-411
mg C m-2 day-l in the oxidative zone and
5-62 mg C m-2 day-l in the reductive zone.
Photosynthesis by bacteria accounted for
l?IIOTOSYNTHETIC
1 50.
SULFUR
. . .100 o;,
651
BACTEKCA PRODUCTION
, ,
50
.
. . . 1po. 1 - _150
IL
,
0
about 3.0-13% of the total synthesis of organic matter. The role of photosynthetic
bacteria as primary producers, therefore,
cannot be overlooked.
This is true year
round in brackish lakes, where there is a
permanent anoxic zone and photosynthetic
sulfur bacteria appear throughout the year.
In thcsc regions, annual production
by
photosynthetic bacteria can be expected to
bc 9-25% of the total annual primary production.
In freshwater
lakes, when an
anoxic zone is found during stratification,
bacterial photosynthetic
production
may
continue from July to October. In Lake
5do
IIaruna, which is a mesotrophic caldera
lake of 8 km2 area and 13 m maximum
depth, the summer stagnation
usually
begins in June and lasts for about five
months. The seasonal variations of physicochcmical
and biological
stratification
observed in this lake in 1964 are shown
in Fig. 7. ‘With the progress of thermal
stratification, dissolved oxygen was rapidly
depleted in the hypolimnion
and an appreciable amount of H2S was formed in
the bottom waters by the middle of July.
In succeeding months, H2S was present in
the water to a depth of 11 m, and its
4.1
0.30
0.07
0.15
0.38
0.59
0.57
0.89
1.74
0.9
4.3
0.05
0.05
0.05
0.00
0.19
0.07
0.01
0.02
1.20
0.47
0.00
29.7
0.07
1.10
3.50
0.22
0.25
0.45
A
060
B
0.37
A
027
0.12
0.05
(1.20)?
0.00
Bact.
Hiruga
Jul 1966)
3.50
L470
0.20
(22.8)?
A
(21
in the stagnation
0.40
0.25
0.98
Phyt.
method
19.8
7.0
7.4
A89
A
1.8
0.0
4.6
b.o
0.0
0.0
Bact.
22.1
L922
1.08
3.57
4.81
A
565
Phyt.
A
Kisaratsu
Aug 1966)
1.28
5.00
5.74
154
94.1
Bact.
(16
3.5
0.37
0.52
L331
0.79
0.10
0.28
B
of water (mg C m-’ hr-‘) and of a unit water
Underlined
figure is the maximum calue
Waku-ike
(4 Aug 1965)
Phyt.
period.
(A) and dark carbon uptake (B) capacities
4.78
Total (mg C
me2 hr-‘)
36.3
s.5
3
4
5
5.5
6
6.5
7
9
10
11
12
15.
20
25
27
30
35
40
6.39
B
Yuno-ko
Aug 1966)
L731
A
(30
Photosynthetic
1
2.
0
Depth
(ml
TABLE
12.0
0.67
2.32
3.03
3.26
Phyt.
column
A
10.6
0.19
0.00
2.5
0.05
0.07
L190
0.07
0.12
0.11
211
A
Bact.
B
by in situ
Kisaratsu
(2 Sep 1965)
measured
PIIOTOSYNTHETIC
SUL,FUR
BACTERIA
PRODUCTION
653
PROOUCTlON
9
FIG.
6. Vertical changes of in situ photosynthetic
productivity
(open
1. Haruna, 14 October 1.964;
take ( closed circles).
In mg C m-* day-‘:
9 September 1965; 8. Suigetsu, 20
6. Suga, 20 July 1966; 7. IIarutori,
17 July 1965. In mg C m-”
2. Yuno-ko, 30 August 1966; 3. Waku-ikc,
gust 1966; 5B. Same, 2 September 1965; 9, Hiruga, 21 July 1966.
concentration reached a maximum of 1.6
mg S/liter
or more near the bottom.
Growth of the photosynthetic
sulfur bacteria, particularly
of Chromatium,
began
in the anoxic layer with the appearance of
H2S in the water; it reached a maximum
density of 300 to 700 x lo3 cells/ml in
October just before the beginning of the
Possible mechanisms infall overturn.
volved in these seasonal changes have been
discussed (Takahashi
1967). The depth
to rate profiles of bacterial photosynthesis
and dark fixation of carbon measured in
situ coincided fairly well with those of the
bacterial population
density.
Based on
these data, the annual bacterial photosynthesis in the lake should be about 3.6 g C/
m2, and this value is almost 4% of total
primary production.
In addition to bacteria, an enormous
population
of photosynthetic
flagellates
(Cryptomonas spp.) appeared at the bot-
circles) and dark carbon up4. Hamana, 29 August 1965;
July 1966. In mg C m-’ hr-I:
3 hr-I: 5h. Kisaratsu, 18 Au-
tom of the thermocline, near the base of
the euphotic zone, and in contact with the
H2S zone. The total daily photosynthetic
production by Cryptomonas was mcasurcd
as 11 g C rn2 day-l; this value would be
near 5% of the total primary production
of the lake.
As has been reported previously, photosynthetic
sulfur bacteria can probably
serve as food for zooplankton
such as
copepods which have been observed at the
layer just above the anoxic zone where
photosynthetic sulfur bacteria grow. These
zooplankters were usually dark red, apparently a result of heavy grazing on red
sulfur bacteria. Direct evidence in support of this :hypothcsis has been obtained
from our experiments using a 14C technique, The 14C labeled photosynthetic sulfur bacteria can bc dctectcd in copepods.
Sorokin (1966) has shown similar results
in studies on photosynthetic bacteria.
P
654
Y2
MASAYUKI
0
0
2
4
8
8
10
TAKAHASHI
AND
SHUN-E1
ICIIIMURA
DISSOLVEDOXYGEN(Olmg/L)
WATER TEMPERATURE(‘G)
10 0
IO
0
10
20 0
10
20
I
e
a
w
n
0
&O
21 Nov
,
0 ?I 2
I
H2
0 1 2
s (S-me/l)
Q I
2
4
=
318Jul 1 Au! 14 Au4
2 Sep
fl
x 10SCELLS/ML
1.5 nf?t
I,
012345
x 10 G-mg/@day
DAILYPHOTOSYNTHESIS
ANDDARKCARBON
UPTAKE
l?IIOTOSYNTIIETIC
SULFUR
REFERENCES
AMENCAN PUBLIC IIEALTH ASSOCIATION. 1960.
Standard
methods
for the examination
of
water
and wastewater,
11th ed.
APHA,
New York. 626 p.
ANAGNOSTIDIS, K., AND J. OVERBECK. 1966.
Methanoxydierer
und hypolimnische
Schwefelbakterien.
Studien zur ijkologischen
Biociinotik der Gewassermikroorganismen.
Ber.
Deut. Botan. Ges., 79: 163-174.
BREED, R. S., E. G. D. MUJXUY, AND N. R. SMITH
[EDs.]. 1957.
Bergey’s manual of determinativc bacteriology,
7th ed. Williams and
Wilkins, Baltimore, Md. 1094 p.
CZECZUGA,B. 1965. Chlorobium
limicola Nads.
(Chlorobacteriaceae)
and the distribution
of
chlorophyll
in some lakes of the Mazur lake
district.
Hydrobiologia,
25 : 412423.
JIMBO, T.
1938.
Beobachtungcn
einiger thiotropher Seen Japans mit besonderer Beriicksichtigung
der Schwefelbakterien.
1. Sci.
Rept. Tohoku Univ., Fourth Ser., 13: 259269.
KONDRAT’EVA, E, N. 1965. Photosynthetic
bacteria.
Oldborne Press, London.
KUZNETSOV, S. I. 1958. A study of the size of
bacterial
populations
and of organic matter
production
due to photo- and chemosynthesis
in water bodies of different
types.
Verhandl. Intern. Ver. Limnol., 13: 156-169.
-.
1959. Die Rolle der Mikroorganismen
im Stoffkreislauf
der Seen. VEB Deut. Verlag Wiss., Berlin.
301 p.
BACTERIA
PRODUCTION
655
PFENNIG, N.
Photosynthetic
bacteria.
1967.
Rev, Microbial.,
21: 285-324.
RICIIARDS, F. A., WITH T. G. THOMPSON. 1952.
The estimation and characterization
of plankton populations
by pigment analysis.
II. A
spectrophotometric
method for the estimation of plankton pigments.
J. Marine Res.,
11: 156-172.
SCHLEGEL, H. G., AND N. PFENNIG. 1961. Die
Anreicherungskultur
einiger Schwefelpurpurbakterien.
Arch. Mikrobiol.,
38: l-39.
SMITH, J. H. C., AND A. BENITEZ. 1955. Chlorophylls:
analysis in plant materials, p. 142196.
In K. Peach ,and M. Tracey
[eds.],
Moderne
Methoden
der Pflanzenanalyse,
v.
4. Springer, Berlin.
SOROKIN,Yu. I. 1964. On the primary production and bacterial activities in the Black Sea.
J. Conseil, Conseil Perm. Intern. Exploration
Mer, 24: 41-60.
-.
1966. On the trophic role of chemosynthesis and bacterial biosynthesis
in water
bodies, p. 187-250.
In C. R. Goldman [ed.],
Primary
productivity
in aquatic
environments. Univ. California
Press.
STANIER, R. Y., AND J. H. C. SMITH. 1960. The
chlorophylls
of green bacteria.
Biochim.
Biophys. Acta, 41: 478484.
TAKAHASIII, M. 1967. Ecological studies of photosynthetic
bacteria
in lakes.
MS. Thesis,
Tokyo Kyoiku University.
61 p.
WOOD, E. J. F. 1965. Marine microbial
ecology. Chapman and Hall, London.
Ann.
c
FIG. 7. Seasonal variations of physicochemical
and biological
stratification
observed in Lake Haruna in 1964. Upper panel: O-dissolved
oxygen; S-hydrogen
sulfide; T-water
temperature.
Lower
panel: white area -cell
number of purple sulfur bacteria and bacterial photosynthesis;
stippled areaflagellate photosynthesis;
ruled areT‘-cell
number of nonpurple bacteria and dark carbon uptake.