Journal of Biomaterials and Nanobiotechnology, 2012, 3, 413-420 Published Online October 2012 (
Formation of Calcium Carbonate Polymorphs Induced by
Living Microalgae
Giulia Santomauro*, Johannes Baier, Wanjing Huang, Stefan Pezold, Joachim Bill
Institute for Materials Science, University of Stuttgart, Stuttgart, Germany.
Email: *
Received August 7th, 2012; revised September 17th, 2012; accepted September 26th, 2012
Calcium carbonate (CaCO3) occurs in the three polymorphs calcite, aragonite and vaterite. The formation of these crys-
tals in inorganic solutions is influenced by parameters like pH, temperature or impurities. Living freshwater microalgae
can also induce the formation of CaCO3 when they live in a suitable environment containing saturated amounts of Ca2+.
Through this biologically induced biomineralization only the formation of the polymorph calcite has been reported yet.
We investigated the precipitates which have been formed in solutions containing the freshwater microalgae Scenedes-
mus obliquus and different zinc amounts (0, 3.27 and 6.53 mg Zn2+/l) by XRD and SEM. As references precipitates
from the same solutions but without algae were investigated. We could show that the presence of living microalgae has
a great influence on the precipitation of calcium carbonate crystals. In algae-containing media without or with a low
zinc amount always calcite and aragonite are formed. In the corresponding medium with 6.53 mg Zn2+/l pure aragonite
crystals were built. In contrast, in the inorganic, algae-free solutions without zinc, pure calcite is precipitated. Both in-
organic solutions with zinc show major calcite precipitation and weak aragonite precipitation. Thus the algae cells ad-
vance significantly the formation of aragonite, which is enhanced by the presence of zinc cations in the media. Possible
mechanisms are discussed.
Keywords: CaCO3 Polymorphs; Biomineralization; Zinc; Microalgae; XRD
1. Introduction
The formation of the three calcium carbonate (CaCO3)
polymorphs calcite, aragonite and vaterite in inorganic
solutions has been the topic of many studies [1-4]. It was
proposed that first an unstable amorphous phase is built
which transforms to the metastable phase vaterite or ara-
gonite, followed by the transformation to the stable phase
calcite [1]. The precipitation of the polymorphs can be
affected by different factors like temperature, pH of the
medium, concentration ratio of individual components,
supersaturation, ionic strength or impurities [3]. The in-
vestigations of Ogino et al. (1987) [1] revealed that ara-
gonite formation is favored at higher temperatures
(>40˚C) in aqueous solution, which has also been sup-
ported in other experiments [4]. At room temperature, the
pH of the solution in a constant-composition environ-
ment is the most important factor for the formation of the
polymorphs [3]. At 24˚C, vaterite is the major product in
the pH range between 8.5 and 10. Aragonite preferably
formed at pH 11; when the pH is higher than 12, calcite
is the dominant product. The precipitation of the different
polymorphs can also be modified by impurities in the
solution. When the ionic radius of the impurities is
smaller than that of the Ca2+ cations, what is the case for
Zn2+ cations [5], aragonite is deposited [6]. This influ-
ence is explained by adsorption phenomena on the crys-
talline faces of the nuclei. Kitano et al. (1976) [7] exam-
ined specifically the adsorption behavior of Zn2+ on
CaCO3 polymorphs in aqueous solutions. They showed
that Zn2+ is strongly adsorbed on aragonite crystals in
comparison to other polymorphs. It was assumed that the
zinc ions inhibit the transformation of aragonite to calcite
[1,7]. The Zn2+ adsorption on the calcite surface occurs
via an exchange of Ca2+ in a surface-adsorbed layer [8].
Also organic additives show an effect on the minerali-
zation of calcium carbonate (reviews in: Meldrum, 2003
[9]; Ren et al., 2011 [10]). Amino acids like glycine,
aspartic acid and glutamic acid or polysaccharides like
cellulose influence the precipitation and morphology of
calcite and vaterite [11-13].
Living organisms like photosynthetic microalgae can
induce the precipitation of CaCO3 through biominerali-
zation. It is known that many freshwater algae build cal-
cite crystals when they live in a supersaturated environ-
ment regarding calcium [14,15]. This is a result of the
*Corresponding author.
Copyright © 2012 SciRes. JBNB
Formation of Calcium Carbonate Polymorphs Induced by Living Microalgae
influence of the algae’s metabolism on their aqueous
environment [16]. Through photosynthesis the algae as-
similate CO2 and/or 3, and release OH [16,17].
This leads to an increase of the pH and the concentration
of carbonate anions within the solution. It is also largely
accepted that the pH affects both number of cell surface
binding sites and metal chemistry within aqueous solu-
tion: in the acidic range, the functional groups of the cell
wall are closely protonated, which limits the approach of
metal cations. The cell walls of green algae consist of
polysaccharides and proteins [18,19]. With increasing pH,
more functional groups, such as carboxyl or amino
groups, are exposed, which increases the biosorption of
metal ions on the negatively charged cell walls. In the
first step, Ca2+ is bound on the cell wall, and afterwards
anions are accumulated and CaCO3 is precipitated
extracellular. This mechanism is named biologically in-
duced [16], because the calcification is not actively con-
trolled by the organisms. In the biologically controlled
biomineralization, different types of biominerals are pro-
duced under the genetic control of the organisms. Up to
now, in the presence of freshwater microalgae only the
extracellular biologically induced formation of calcite is
Positively charged metal ions can also be bound on the
cell surfaces of living organisms [e.g. 20-27]. Zinc is an
essential trace metal for all organisms, but can be toxic
when present in high amounts. Exposure of microalgae to
sublethal Zn2+ concentrations caused inhibition of e.g.
photosynthesis [28]. When the algae are confronted to
toxic elements like Zn2+ in their environment, they de-
toxify it by taking up the ions. The uptake is split in two
steps: the first is a rapid biosorption onto the cell wall,
during the second step the ions are transported into the
cells [29]. Subsequently, the interior of the cells can be
detoxified by chelating the Zn2+ cations to e.g. nontoxic
zinc-phosphate-based nano needles [30].
The aim of this study was to investigate the role of
living algae on the precipitation of different polymorphs
of calcium carbonate. For the experiments the unicellular
alga species Scenedesmus obliquus (Chlorophyta) was
cultivated in media with and without Zn2+ and the results
were compared to the inorganic media without algae.
This alga species was chosen because preliminary ex-
periments have shown that it calcifies readily when cul-
tured in supersaturated media regarding Ca2+.
2. Materials and Methods
2.1. Organisms and Cultures
The experiments were conducted with living Scenedes-
mus obliquus (strain 276-1), obtained from the SAG cul-
ture collection Göttingen. The algae were cultivated in a
modified calcification medium [17], where Na2EDTA,
KH2PO4, (NH4)Mo7O24 and MnCl2 were omitted and
FeCl3 was reduced to 0.01 mg/l to prevent chelate forma-
tion with Zn2+. The solution was saturated regarding Ca2+.
The media contained different amounts of zinc (0 mg
Zn2+/l, 3.27 mg Zn2+/l or 6.53 mg Zn2+/l), added as
ZnSO4·7 H2O (Roth, Karlsruhe). Preparation of the me-
dia: all stock solutions beside Na2CO3 were sterilized
(autoclave Systec V-75) and combined, the pH was ad-
justed to 6.3. The algae were washed in demineralized
water (Millipore), counted with a hemocytometer (Ma-
rienfeld, Lauda-Königshofen) to ensure the same cell
concentration in all cultures and added to the medium
(about 4.0 × 108 cells/l). The culture was held in a rotary
shaker (Infors HT Multitron II, 100 rpm) at 26˚C and
permanent illumination (FL tubes Gro-Lux 15W, 3500
lx). Due to photosynthesis, the pH increased to a value
over 9 during several days. Not till then the Na2CO3 was
added to prevent loss of anions and the pH was
adjusted to 8.5. At this point the experiment started. The
inorganic, algae-free solution was prepared identically;
the pH was adjusted daily according to the organic, al-
gae-containing solution with 0.1 M NaOH. The duration
of the experiment was 72 h. After this time all cultures
were living as revealed by their green color.
2.2. SEM Measurement
Precipitation of crystals was investigated after 2, 4, 6, 24
and 72 h duration of the experiment. For observation in a
scanning electron microscope (Zeiss DSM 982 GEMINI)
the specimens were washed in demineralized water (Mil-
lipore) using a glass vacuum filter system with 0.2 µm/2
µm pore size filter membrane (Millipore) and then
air-dried. To obtain electron conductivity, the mem-
branes were coated with graphite.
2.3. Powder X-Ray Diffractiometry (XRD)
XRD was used to identify the CaCO3 polymorphs after
72 h duration of the experiment. The XRD patterns were
recorded with a D500 diffractometer (Siemens). Meas-
urements were made in Bragg-Brentano geometry, using
CuKα1 radiation (X-ray tubes setting of 30 mA and 40
kV) employing a primary-beam Johansson monochro-
mator in a 2Θ range of 20˚ to 50˚.
3. Results & Discussion
3.1. pH Trend
At the beginning of all experiments the pH of each cul-
ture was adjusted to 8.5. Due to photosynthesis of the
algae, the pH rose up to 10.8 after 48 h in the culture
without zinc; afterwards it stayed nearly constant (Figure
1). In presence of zinc, the pH-shift was retarded and did
not reach the high values of the culture without zinc. This
Copyright © 2012 SciRes. JBNB
Formation of Calcium Carbonate Polymorphs Induced by Living Microalgae
Copyright © 2012 SciRes. JBNB
is due to the fact, that Zn2+ cations restrain photosynthe-
sis of algae. The pH-shift is correlated to Zn2+ concentra-
tion within the solution: the culture with 6.53 mg Zn2+/l
only reached pH 10.1 after 72 h, the culture with 3.27 mg
Zn2+/l reached pH 10.5 after 48 h and remained at this
value. According to the observed pH values in cultures
containing algae, the pH in the media without algae were
adjusted daily with a 0.1 M NaOH solution.
in the cultures without zinc (Figure 2(b)). In the next
hours the crystals grew bigger (data not shown). In the
cultures with zinc, no crystallization occurred during the
first 6 h (data not shown).
After 24 h of incubation, in all solutions precipitates
could be found (data not shown). In the media with algae
and with zinc, big crystals occurred with diameters of
about 50 µm. Always many algae were embedded in
these crystals. In the inorganic solutions with Zn2+, only
very small precipitates were found (Ø below 100 nm;
REM image, data not shown).
3.2. Precipitation of Crystals and Identification
of Polymorphs
After 72 h of incubation, in all solutions crystals were
found which differed greatly in their dimensions and
morphology (Figure 3). The precipitates formed in the
organic solutions contained several (Figures 3(a) and (c))
or many algal cells (Figure 3(b)). The largest precipitate,
where always many algal cells were incorporated, were
The formation of precipitates was investigated at the
starting point of the experiments and after 2 h, 4 h, 6 h,
24 h and 72 h in solutions with algae.
At the starting point of the experiments, there was no
precipitation on the algae (Figure 2(a)). After 2 h of in-
cubation, crystals with embedded algae could be detected
0 24487
time [h]
w ithout Zn
with 3.27 mg Zn/l
with 6.53 mg Zn/l
wit h ou t Zn
with 3.27 mg Zn/l
with 6.53 mg Zn/l
Figure 1. pH shift in the cultures with algae and different zinc amounts during the experimental time of 72 h.
(a) (b)
Figure 2. SEM images. (a) Algae (black arrows) without precipitates at the beginning of the experiment; (b) Crystals (white
arrow) with embedded algae were built afte r 2 h in the medium without zinc.
Formation of Calcium Carbonate Polymorphs Induced by Living Microalgae
(a) (b) (c)
(d) (e) (f)
Figure 3. Crystals after 72 h of incubation. (a)-(c) Cultures with algae and different amounts of zinc: (a) Without zinc; (b)
With 3.27 mg Zn2+/l; (c) With 6.53 mg Zn2+/l. (d)-(f) Inorganic solutions with different amounts of zinc: (d) Without zinc; (e)
With 3.27 mg Zn2+/l; (f) With 6.53 mg Zn2+/l. Black arrows—algae, white arrows—crystals.
found in the organic solution with 3.27 mg Zn2+/l (Fig-
ure 3(b)).
These precipitates appear in the SEM images as big
single-crystals, but could also been formed as many
smaller crystals and afterwards baked together. In the
inorganic solution with zinc, two different crystal types
were found (Figures 3(e) and (f)). Due to the crystal
morphology we assume that the needle-like crystals refer
to aragonite and the rhombohedric to calcite [3].
The crystals found after 72 h in the experimental solu-
tions were washed and then analyzed regarding their
modification by XRD. Representative XRD diagrams are
shown in Figures 4 and 5. In the case of solutions with-
out algae cells the dominant (104) reflection of calcite
(JCPDS card No. 01-072-1650) can be found in all sam-
ples at 29.5˚ (3.02 Å) (Figure 4). Furthermore, the
weaker (012)-, (110)-, (113)-, (202)-, (024)-, (018)-, and
(116)-reflection of calcite are present in the sample,
which contains no Zn2+ cations within solution. In former
studies about precipitation in inorganic solutions, vaterite
was found to be the major product in the pH range be-
tween 8.5 and 10 and at 24˚C [3]. In these experiments,
the experimental solution only contained calcium chlo-
ride and sodium carbonate. In our studies, a culture me-
dium for algae with a more complex composition was
used for all experiments, also for preparing the solutions
without algae. This was probably the reason, why calcite
was built and not vaterite.
In the inorganic sample which has been formed in me-
dium with 3.27 mg Zn2+/l weak intensities (near the de-
tection limit) can also be detected at 26.3˚, 27.2˚, and
46.0˚ which can be attributed to the characteristic (111)-,
(021)- and (221)-reflections of aragonite (JCPDS card
No. 00-003-1067). The reflections of aragonite correspond
with SEM observation of a small amount of a second
acerous phase (cf. Figure 3(e)). The precipitate of the
sample, which has the highest amount of Zn2+ cations
within the media, shows only the dominant (104) reflec-
tion of calcite. A small amount of aragonite crystals
could be observed in this medium by SEM observations
(Figure 3(f)), which is below of detection limit of XRD.
The presence of algae cells has a significant influence
on the CaCO3 precipitation within media in comparison
to media without algal cells, which is demonstrated in
Figure 5. In the case of the Zn2+ free media the precipi-
tate is dominated by the reflections of calcite, but small
intensities of aragonite are also present (Please note that
the strong (104) reflection of calcite at about 29.5˚ is cut
at about 1600 a.u. within Figure 5(a)). With increasing
zinc concentration in the solutions the amount of calcite
decreases dramatically. In fact, in the case of media with
6.53 mg Zn2+/l no calcite reflections can be determined
within the corresponding XRD diagram. Only the reflec-
tions of aragonite are presen(Figure 5(c)). Thus, the t
Copyright © 2012 SciRes. JBNB
Formation of Calcium Carbonate Polymorphs Induced by Living Microalgae 417
Figure 4. XRD diagrams of precipitates in absence of algae (72 h of incubation). (a) Without zinc; (b) With 3.27 mg Zn2+/l; (c)
With 6.53 mg Zn2+/l.
Figure 5. XRD diagrams of precipitates in presence of algae (72 h of incubation). (a) Without zinc; (b) With 3.27 mg Zn2+/l; (c)
With 6.53 mg Zn2+/l.
Copyright © 2012 SciRes. JBNB
Formation of Calcium Carbonate Polymorphs Induced by Living Microalgae
algae cells advance significantly the formation of arago-
nite, which is enhanced by the presence of zinc ions in
the media.
The algae function obviously as heterogeneous nuclea-
tion sites. Since only crystals associated with algae have
been found in the solutions, the cell walls are evidently
directly involved in nucleation. The binding sites of the
cell walls have a great affinity for Ca2+ cations, the
bound Ca2+ attract anions like [16]. Our prelimi-
nary experiments have shown that Scenedesmus obliquus
does not calcify when cultivated in the dark, and the pH
reaches only the maximum of 9. This was also observed
by other authors with different microalga species [17,31].
This shows that the algae do not only act as nucleation
sites for CaCO3 precipitation but are actively involved
through light-dependent photosynthesis and thus alkali-
zation of the medium. The increase of pH was measur-
able in the bulk solution but was probably higher close to
the cells. This was also supposed by other authors
[14,17]. In presence of zinc in the medium the aragonite
modification is favored. In this case, obviously the trans-
formation into the thermodynamically stable calcite mo-
dification is hindered. A possible mechanism that occurs
in micro-environments created by the cells is suggested
in Figure 6. A part of the absorbed Ca2+ on the cell wall
can be exchanged by Zn2+ [18]. The interaction of Zn2+
with the cell wall enables a local enrichment of the ions
which are supposed to stabilize the metastable aragonite
modification [7] and thus prevents its transformation into
thermodynamically stable calcite. Furthermore, Zn2+
ions restrain photosynthesis [28], which is connected
with a lower pH within the micro-environments com-
pared to the algae-containing zinc-free medium. As
mentioned above, the formation of aragonite is favoured
at lower pH compared to the one of calcite [3]. Ac-
cordingly, only aragonite crystals in the media contain-
ing algae and high amounts of zinc are detected. On the
contrary, calcite is produced nearly exclusively in the
media without algae and high amounts of zinc. Only
traces of aragonite are produced, as revealed by SEM
4. Conclusion
We compared the precipitates which have been formed in
solutions with and without algae and with and without
different zinc amounts. We could show that the presence
of living microalgae has a great influence on the precipi-
tation of calcium carbonate crystals. Due to photosynthe-
sis, the pH in the algae-containing organic media in-
creased and CaCO3 crystals are precipitated. In organic
media without zinc or with 3.27 mg Zn2+/l always calcite
and aragonite are formed. In the organic media with 6.53
mg Zn2+/l aragonite is obtained even exclusively. In con-
trast, in the inorganic solutions without zinc, pure calcite
is precipitated. Both inorganic solutions with zinc show
major calcite precipitation and weak aragonite precipita-
tion as revealed by XRD measurements and SEM obser-
vations. Thus, the algae cells advance significantly the
formation of aragonite, which is further enhanced by the
presence of zinc cations in the media. The following ef-
fects of algae and zinc in the solution were supposed:
first, as the algae accumulate, a “micro-environment”
around the clusters is formed, where the CaCO3 is pre-
cipitated (Figure 6). When high Zn2+ amounts are pre-
sent in the solution, photosynthesis is inhibited and the
pH in this “micro-environment” is lower compared to the
“micro-environment” around the algae in solution with-
out Zn. The lower pH prefers the building of aragonite
[3]. Second, the algae function as heterogeneous nuclea-
tion sites where in the first step Ca2+ and Zn2+ ions are
absorbed on the negatively charged cell walls and in the
second step anions like are bound (Figure 6).
The presence of Zn2+ leads to the precipitation of arago-
nite [6]. In the “micro-environment” around the cells
more Zn2+ ions are present than in the corresponding in-
Figure 6. Scheme of possible heterogeneous nucleation of aragonite crystals in presence of algae and zinc. Between several
ggregated cells a “micro-environment” is built leading to a local increase of the pH and Zn2+ ions. a
Copyright © 2012 SciRes. JBNB
Formation of Calcium Carbonate Polymorphs Induced by Living Microalgae 419
organic bulk solution, since these ions are attracted from
the cell walls and bound on them. Zn2+ ions inhibit the
transformation from aragonite to calcite [1]. Hence, ara-
gonite is precipitated in the algae-containing media with
high amount of Zn whereas in the corresponding inor-
ganic solution mainly calcite is found.
5. Acknowledgements
We are grateful for financial support provided by the
Deutsche Forschungsgemeinschaft (BI 469/15-1) within
the scope of the project “Biologische Erzeugung von
Oxidkeramiken” (PAK 410). The authors thank M.
Dudek and F. Predel (both MPI-IS) for XRD and SEM
measurements, respectively. Prof. Dr. P. A. van Aken
(MPI-IS) is thanked for providing the SEM.
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