FEMS Microbiology Ecology 25 (1998) 171^178
Light causes selection among two phycoerythrin-rich
Synechococcus isolates from Lake Constance
Christine Postius a; *, Ulrich Kenter b , Alexander Wacker a , Anneliese Ernst a ,
Peter Boëger a
a
Lehrstuhl fuër Physiologie und Biochemie der P£anzen, Universitaët Konstanz, D-78457 Konstanz, Germany
b
Limnologisches Institut, Universitaët Konstanz, D-78434 Konstanz, Germany
Received 30 June 1997; revised 27 October 1997; accepted 30 October 1997
Abstract
The phycoerythrin (PE)-rich unicellular cyanobacteria Synechococcus spp. strains BO 8808 and BO 9203, from the pelagic
zone of Lake Constance, exhibited different responses when cultured under low light and light stress conditions. Under light
stress caused by continuous illumination at elevated light intensity, strain BO 8808 ceased growth, the PE/chlorophyll ratio was
slowly reduced and the zeaxanthin content was significantly decreased. By contrast, strain BO 9203 grew faster under high light
compared to low light intensities. This strain responded to increased light by a rapid reduction of the PE/chlorophyll ratio while
the zeaxanthin content remained constant. Both of these alterations may have protecting effects for BO 9203 against light
toxicity. In mixtures of both strains, the predominance of the light-tolerant strain BO 9203 was demonstrated by restriction
fragment length polymorphism of psbA genes under light stress conditions. Apparently, strain BO 9203, isolated from an algal
bloom in the spring, can cope better with high light intensities than strain BO 8808, isolated in the autumn. z 1998
Federation of European Microbiological Societies. Published by Elsevier Science B.V.
Keywords : Autotrophic picoplankton; Cyanobacteria ; Phycoerythrin ; Restriction fragment length polymorphism ; Synechococcus ; Zeaxanthin
1. Introduction
Cyanobacteria are photoautotrophs which have
developed a variety of strategies that enable them
to respond adequately to changes in environmental
conditions such as light and nutrient £uctuations.
With this capability they are able to colonize nearly
all ecosystems [1]. In spite of their widespread occur* Corresponding author.
Tel.: +49 (7531) 882809; Fax: +49 (7531) 883042;
E-mail: [email protected]
rence and their signi¢cant contribution to overall
primary production of marine and freshwater systems (see [2] for review), unicellular cyanobacteria
of the Synechococcus type were observed in Lake
Constance for the ¢rst time in 1986 [3]. Since then,
their presence as part of the autotrophic picoplankton (APP) and their seasonal variation in numbers,
biomass and production has been well documented
[4,5]. As in some other prealpine lakes, the APP of
this meso-eutrophic lake is dominated by phycoerythrin (PE)-rich cyanobacteria of the Synechococcus
type. Over the course of several years we isolated
0168-6496 / 98 / $19.00 ß 1998 Federation of European Microbiological Societies. Published by Elsevier Science B.V.
PII S 0 1 6 8 - 6 4 9 6 ( 9 7 ) 0 0 0 9 3 - 7
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18 unicellular PE-rich cyanobacterial strains from a
single sampling site in the pelagic zone of Lake Constance.
DNA characterization by RFLP (restriction fragment length polymorphism) of three psbA genes
present in Synechococcus spp. revealed a high genetic
diversity among these isolates, as eight of 18 isolates
were shown to be genetically di¡erent [6,7]. Although
obtained from di¡erent phases of the growth period
of the year 1994, the other 10 isolates exhibited identical DNA fragment patterns, demonstrating the persistence of one strain in the pelagic zone during the
course of one year [7]. Temporal abundance of genetically distinct strains may be due to di¡erential
physiological responses to environmental changes.
However, despite high genetic diversity, remarkable
physiological di¡erences were only observed between
di¡erent pigment types, i.e. when PE- and PC (phycocyanin)-rich isolates were compared under nutrient
de¢ciency conditions (C. Postius, unpublished results). Among PE-rich isolates, two strains exhibited
special structural features of the outer membrane:
one of them had a highly glycosylated surface layer
[8], the other one carried a permanent, thick slime
layer (C. Postius, unpublished results). When grown
under standard dim light culture conditions the other
PE-rich strains exhibited no signi¢cant di¡erences in
size, shape and composition of major pigments despite their genetic diversity [9].
Cyanobacterial strains may respond di¡erently
when exposed to changing light and nutrient conditions [1,10]. Most remarkable is the alteration of the
pigment composition, often described for PC-rich
cyanobacteria. However, only few reports describe
the impact of light on PE-rich unicellular cyanobacteria. In aquatic ecology, cyanobacteria are mainly
described as organisms that prefer low light intensities [11]. However, mixing processes in the water
column may lead to an exposure to high light intensities which may be lethal to these organisms [12,13].
In natural aquatic systems light intensity changes in
various ways and on di¡erent time scales [14,15]. The
shortest changes in light regime are caused by waveinduced `£icker e¡ects'. Variations of irradiance due
to vertical mixing of the water column include intermediate, variable scales, plus major changes imposed
by the diurnal rhythm and actual weather conditions
[16]. Longer-term alterations result from seasonal
changes and from changes in the trophic situation
that a¡ect cell density and therefore light penetration
through the water column [17,18]. Accordingly, photoacclimative changes in phytoplankton populations
occur on time scales ranging between hours, months
or even years, as in the case of eutrophication or
oligotrophication situations [19]. Rapid responses
to altered light conditions may be achieved by
changes in cellular reactions, i.e. changes in pigment
composition as often described for cyanobacteria
[1,10]. On the other hand, long-term £uctuations of
the light regime may lead to varying compositions of
the population.
The objective of this study was to compare two
genetically di¡erent PE-rich Synechococcus strains
with respect to growth and pigment composition
under standard dim light culture conditions and
under a light stress situation caused by continuous
illumination at increased light intensity. DNA analysis was performed to demonstrate the selection of
the better adapted organism under the two growth
conditions in mixed cultures.
2. Materials and methods
2.1. Isolation and culture conditions
Samples of Synechococcus spp. strains BO 8808
and BO 9203 (hereafter referred to as BO 8808 and
BO 9203) were obtained from the pelagic zone (0^8
m) of the northwestern part of Lake Constance, the
ë berlinger See', at the site of maximum depth (147
`U
m). BO 8808 was isolated in early autumn of the year
1988 by plating 50 Wl of a mixed water sample from
the pelagic zone on modi¢ed BG11 medium [20] solidi¢ed with 1.5% agar (w/v). Single colonies were
inoculated in liquid medium and cultivated as described elsewhere [7,21]. Strain BO 9203 was obtained in the spring of 1992 by enrichment upon
prolonged maintenance at 20 WE m32 s31 green light.
Cyanobacterial cultures were maintained, under
shaking, at 23³C in liquid cultures (40 ml) in BG11
medium with lowered nitrate supply (5 mM). The
illumination was 10^30 WE m32 s31 for 12 day hours
and was reduced to approximately 1 WE m32 s31 for
a 12-h dark interval. These conditions are referred to
as low or dim light conditions. For exposure to light
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173
stress conditions, also referred to as high light conditions, 250-ml cultures were illuminated continuously with 100 WE m32 s31 white light. Mixed cultures, exposed to light stress or dim light, were
started with the same inoculum for both strains (¢nal
OD750 = 0.1) and maintained at the indicated conditions for approximately 3 weeks.
2.2. Pigment determination by absorption
measurements
Absorption measurements of whole cells and clear
solutions were carried out with a U 2000 spectrophotometer (Hitachi, Tokyo, Japan). In vivo absorption
spectra of whole cells were recorded with a UV 3000
double-beam spectrophotometer (Shimadzu, Kyoto,
Japan). For chlorophyll a (chl a) determination, cells
(1 ml) were extracted with 90% (v/v) methanol for 10
min at 60³C, followed by centrifugation at 10 000Ug
for 5 min. The chlorophyll a content was calculated
from the absorbance of the methanolic extract at 665
nm [22]. The PE/chl a ratio was estimated by measuring absorption of whole cells at 568 nm for PE
content and 668 nm for chl a content, and calculating the ratio from these data. Total carotenoid content was calculated by absorption at 480 nm of
whole cells. The L-carotene content was assumed to
change proportionally to the chlorophyll a content
[23]. The relative zeaxanthin content was calculated
from the di¡erence of the total carotenoid and the Lcarotene contents. The data calculated from absorption measurements were validated by the determination of pigments using HPLC analysis. Absorption
Fig. 2. Chlorophyll a content of cells (Wg/OD750 ) of Synechococcus spp. strains BO 8808 (a) and BO 9203 (b) at low light and
high light conditions.
measurements for growth and pigment content were
performed in three independent experiments. The
data of a typical experiment are presented.
2.3. Fluorimetric measurements
After gentle resuspension of cells in an ultrasonic
cleaning bath (Labson 200, Bender and Hobein, Germany) £uorescence of pigments of whole cells was
measured at room temperature in a 1-cm cuvette
using a SM-25 £uorimeter (Kontron, Milan, Italy)
with a slit width setting of 10 nm for excitation
and emission wavelengths. Fluorescence of pigments
and energy transfer between pigments were recorded
at the following wavelength settings for excitation
(ex) and emission (em): chl a: ex 440 nm, em 680
nm; PE: ex 550 nm, em 575 nm; PE to allophycocyanin/PSII: ex 550 nm, em 665 nm; PC to allophycocyanin/PSII: ex 620 nm, em 665 nm; for spectra of
the native pigment complexes, see [24].
2.4. HPLC analyses
Fig. 1. Growth of Synechococcus spp. strains BO 8808 (a) and
BO 9203 (b) measured by absorption at 750 nm of cultures
growing at low light (a 12/12-h light/dark regime of 10/1 WE m32
s31 ) and high light (100 WE m32 s31 , continuously illuminated)
conditions.
For HPLC analyses, cultures were ¢ltered on a
Whatman GF/F ¢lter and pigments were extracted
in 95% acetone/5% water (v/v). Carotenoids were
separated by reversed-phase HPLC (Hewlett-Packard Model 1050) using a 250-mm column packed
with 5 Wm particles of Licosphere 100 RP 18. The
pigments were eluted by a gradient composed of solvent A (70% methanol, 30% H2 O and 0.625% tetraethylammonium acetate; v/v/w) and solvent B (60%
methanol and 40% acetone; v/v) with the initial proportion of A:B being 50:50 and the ¢nal proportion
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light conditions (Fig. 1b). Initially, BO 8808 also
grew better at increased light intensities, but 5 days
after changing from dim light to high light conditions growth stopped and optical density remained
at a constant level (Fig. 1a).
3.2. Changes in pigment contents
Fig. 3. Phycoerythrin/chlorophyll a ratio of Synechococcus spp.
strains BO 8808 (a) and BO 9203 (b) at low light and high light
conditions measured by absorption of whole cells at 568 nm and
668 nm, respectively.
99.5:0.5. Identi¢cation and quanti¢cation of pigments was performed using a Waters diode array
detector (Model 991; Waters, Millipore Corporation, Milford, MA).
2.5. DNA preparation and RFLP of psbA genes
DNA was isolated from 250 ml of 2^3-week-old
cultures. For preparation of DNA from freshly
mixed cell cultures, 125 ml of both cultures were
adjusted to the same cell density (OD750 =1.0), mixed
and immediately harvested for DNA isolation. DNA
was isolated as described by Brass et al. [24]. For
RFLP analysis the DNA was digested with the restriction endonuclease BamHI and analyzed by
Southern blot hybridization (hybridization temperature 50³C) using a probe derived from an internal
BstEII fragment of psbA1. This gene, cloned in
pDAN1, encodes the D1 protein of photosystem II
of Synechococcus sp. PCC 7942 ([25], for further details see references [6,7]).
Chlorophyll a content of cells grown under low
light conditions decreased slightly after inoculation
but recovered after one generation (Fig. 2). Transfer
to increased, continuous illumination caused a stronger decline in chl a/OD750 indicating that strains initiated a major photoacclimation process (Figs. 2 and
4). Strain BO 9203 started to recover after one generation as indicated by a slow increase in chl a/OD750
(Fig. 2b) and a net increase of chl a/ml (data not
shown). However, in BO 8808 degradation of chlorophyll a continued even after cell growth was
arrested (compare Figs. 1a and 2a). After 2 weeks
of cultivation under stress conditions BO 8808 exhibited a threefold lower chlorophyll content than
BO 9203.
Changes in phycobiliprotein content were recorded
as the absorption ratio of PE/chl a (Fig. 3a,b). BO
9203 showed a rapid response, starting immediately
after the cultures were transferred to the stress situation. The reduction of the PE/chl a ratio of BO
8808 was much slower and less distinct than that of
BO 9203. Fluorescence emission intensities of PE (ex
550/em 575) and chlorophyll a (ex 440/em 680) revealed a distinct decrease of the emission of PE for
BO 9203 at 100 WE m32 s31 (Fig. 4b), while for BO
8808 this decrease was retarded and less than for BO
3. Results
3.1. Changes in growth
The isolates were routinely grown at 10 WE m32
s
with dark intervals of 12 h. Under these dim
light conditions, growth of BO 9203 was slightly
slower than that of BO 8808 (Fig. 1a,b). Under
high light conditions (100 WE m32 s31 , continuous
illumination), BO 9203 grew faster than under low
31
Fig. 4. Fluorescence emission (arbitrary units) of PE (ex 550/em
575) and chlorophyll a (ex 440/em 680) of Synechococcus spp.
strains BO 8808 (a) and BO 9203 (b) at low light and high light
conditions.
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175
9203 (Fig. 4a). When exposed to high light intensities, the L-carotene content decreased in both
strains (data not shown), while the zeaxanthin content showed a di¡erent response in the compared
strains (Fig. 5a,b). For BO 9203, the cellular concentration of zeaxanthin increased slightly under dim
light but remained constant under high light intensities. On the other hand, the zeaxanthin content of
strain BO 8808 remained constant at low light conditions, but decreased continuously at high light intensities, indicating reduction of zeaxanthin under
stress conditions for this strain.
3.3. DNA analysis of unialgal and mixed cell cultures
by RFLP of psbA genes
The isolates BO 8808 and BO 9203 exhibited a
distinct restriction fragment pattern when probed
with the internal BstEII fragment of the psbAI
gene from Synechococcus PCC 7942. This probe recognizes three homologous genes in the PC-rich parent strain represented by three labeled fragments in
a BamHI digest. The PE-rich isolates BO 8808 and
BO 9203 exhibited characteristic patterns, each consisting of four fragments (Fig. 6). When the DNA
was isolated immediately after mixing the isolates,
characteristic fragments of both strains were visible.
Cultivating mixed cultures for 3 weeks under dim
light conditions (30 WE m32 s31 ) caused prevalence
of the characteristic fragment pattern of BO 8808. In
contrast, RFLP analyses from mixed strains which
had been cultivated for 3 weeks under light stress
Fig. 6. DNA analysis (RFLP) of pure and mixed cultures of Synechococcus spp. strains BO 8808 and BO 9203. DNA was digested with BamHI and probed with an internal fragment of
psbA1 from Synechococcus sp. PCC 7942 as mentioned in Section
2. The position of DNA molecular weight markers (M) is indicated. On top of the gel the source of the DNA (strain numbers)
are indicated. Culture conditions under which cells were maintained: lanes 1 and 2: pure cultures cultivated under 10 WE m32
s31 ; lane 3: mixed cultures at the start of cultivation ; lane 4:
mixed cultures after 3 weeks under low light ; lane 5: mixed cultures after 3 weeks under light stress.
conditions revealed the characteristic pattern of BO
9203, the strain which showed superior growth under
these conditions. By these experimental procedures a
selection of the ¢ttest strain occurred in mixed cultures, according to the environmental conditions.
4. Discussion
Fig. 5. Relative zeaxanthin content of Synechococcus spp. strains
BO 8808 (a) and BO 9203 (b) at low light and high light culture
conditions. Values represent the di¡erence of total carotenoid
content and L-carotene content. Symbols R/S (10 WE m32 s31 )
and O/P (100 WE m32 s31 ) mark the relative pigment contents
detected by HPLC analysis of the same data set.
This study shows that di¡erent light conditions
lead to a selection of di¡erent strains from mixed
cultures. The predominance of strain Synechococcus
BO 9203 at high light conditions was caused by a
higher growth rate induced by increased light intensity, while BO 8808 grew better under low light conditions (Fig. 1). After transfer to high light, both
strains initiated an acclimation process during which
the amount of photosynthetic membranes was reduced [26]. In BO 9203 loss of chlorophyll a was
accompanied by a rapid decomposition of phycobilisomes (Fig. 4b). This destruction of the light-har-
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vesting system may limit the phototoxic e¡ects of
high light. Similar acclimation processes were observed in PC-rich and marine PE-rich Synechococcus
isolates [26,27]. On the other hand, in strain BO 8808
delayed reduction of PE may lead to sustained phototoxicity and to progressive destruction of chlorophyll a and other cell components (Figs. 2a and 4a).
In particular, the decrease of zeaxanthin under light
stress conditions may limit the photoprotective e¡ect
of this carotenoid located primarily in the cytoplasmic or outer cell wall membrane [23]. Maintenance
of a high zeaxanthin level in strain BO 9203 exposed
to light stress situations may be bene¢cial to these
cells since zeaxanthin is thought to quench oxygen
radicals generated by the photochemically non-productive excitation of chlorophyll molecules [28].
With respect to destruction of PE and maintenance
of zeaxanthin, strain BO 9203 resembled the highlight-tolerant marine Synechococcus strain WH
7803 [23,26]. To our knowledge, a dim-light-adjusted
Synechococcus strain comparable to strain BO 8808
has not been described before. The apparent light
stress experienced by this strain may have been enhanced by other factors. In particular, we did not
examine whether the lack of a dark period under
high light conditions had an additional adverse e¡ect
on this strain.
The di¡erent reactions of strains compared under
laboratory conditions may be relevant for population dynamics in natural environments. Within a picoplankton community Lindell and Post [29] described a seasonal succession of Prochlorococcus,
eukaryotic algae and Synechococcus spp. populations
in the Gulf of Aqaba. In the pelagic zone of Lake
Constance, Weisse and Kenter [4] studied the succession of APP, dominated by PE-rich Synechococcus
spp. Over the course of several years, the abundance
of these picocyanobacteria suggested spring and
summer populations in this environment. Several
possibilities may account for £uctuations in population dynamics of those picocyanobacteria. The presence of di¡erent predators and selective predation
may cause a change in the picoplankton population
during the growth season [30,31]. The £agellate
Paraphysomonas sp., isolated from Lake Constance,
was shown to graze selectively on Synechococcus spp.
from the same environment [32]. Alternatively, the
composition of cyanobacterial populations blooming
in spring may depend on strategies of the organisms
to survive winter. Those organisms surviving in highest numbers may play an important role as inocula
to start the growing season in spring. High levels of
viable picocyanobacteria were found in the aphotic
bottom sediment of Lake Biwa, which are likely to
seed photoautotrophic picoplankton blooms occurring in these waters [33]. In the Baltic Sea even cyanobacteria trapped in the ice interior during winter
are thought to be important contributors to the
spring cyanobacterial community [34]. However,
the survival strategies of APP in Lake Constance
are not yet known. Another possibility is that
changed environmental conditions may cause dominance of the better adapted organism. In Lake Arcas
the contribution and abundance of speci¢c cyanobacterial populations can be explained by the interplay of light regime and presence of sul¢de as the
most determinant ecological parameters [35]. In Lake
Constance we demonstrated high genetic diversity
among Synechococcus strains isolated from a single
site, and in several cases even from a single sample
[7], suggesting a mixed population. Intermittent light
changes, as they occur in natural waters, seem to
be tolerated by most of these picocyanobacteria.
However, seasonally changing parameters, like incident light, may exert stress upon some species and
may result in dominance of those strains that
cope better with the altered situation. The light-tolerant strain BO 9203 was isolated from a sample
collected in the spring while strain BO 8808, sensitive
to high light intensities, was isolated in the autumn
[7], when light stress is less likely to occur. However,
the assumed seasonal population dynamics, that
may be due to a varying light regime, will have
to be con¢rmed `in situ' by speci¢c DNA hybridization.
Acknowledgments
This project was supported by the Deutsche Forschungsgemeinschaft by its Sonderforschungsbereich
248 `Sto¡haushalt des Bodensees'. J. Hirschberg, Jerusalem, supplied the plasmid pDAN1, which is
gratefully acknowledged. We thank R. Grimm and
C. Gebauer for technical assistance in DNA and
HPLC analysis, respectively.
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