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INVITED REVIEW
Received: 17 February 2014 Returned for revision: 6 March 2014 Accepted: 1 April 2014
Background The cyanobacterial genus Nostoc includes several species forming centimetre-large gelatinous colonies in nutrient-poor freshwaters and harsh semi-terrestrial environments with extended drought or freezing. These
Nostoc species have filaments with normal photosynthetic cells and N2-fixing heterocysts embedded in an extensive
gelatinous matrix of polysaccharides and many other organic substances providing biological and environmental protection. Large colony size imposes constraints on the use of external resources and the gelatinous matrix represents
extra costs and reduced growth rates.
Scope The objective of this review is to evaluate the mechanisms behind the low rates of growth and mortality, protection against environmental hazards and the persistence and longevity of gelatinous Nostoc colonies, and their
ability to economize with highly limiting resources.
Conclusions Simple models predict the decline in uptake of dissolved inorganic carbon (DIC) and a decline in the
growth rate of spherical freshwater colonies of N. pruniforme and N. zetterstedtii and sheet-like colonies of
N. commune in response to a thicker diffusion boundary layer, lower external DIC concentration and higher
organic carbon mass per surface area (CMA) of the colony. Measured growth rates of N. commune and
N. pruniforme at high DIC availability comply with general empirical predictions of maximum growth rate (i.e. doubling time 1014 d) as functions of CMA for marine macroalgae and as functions of tissue thickness for aquatic and
terrestrial plants, while extremely low growth rates of N. zetterstedtii (i.e. doubling time 23 years) are 10-fold
lower than model predictions, either because of very low ambient DIC and/or an extremely costly colony matrix.
DIC uptake is limited by diffusion at low concentrations for all species, although they exhibit efficient HCO3
uptake, accumulation of respiratory DIC within the colonies and very low CO2 compensation points. Long light
paths and light attenuation by structural substances in large Nostoc colonies cause lower quantum efficiency and assimilation numberand higher light compensation points than in unicells and otheraquatic macrophytes. Extremely low
growth and mortality rates of N. zetterstedtii reflect stress-selected adaptation to nutrient- and DIC-poor temperate
lakes, while N. pruniforme exhibits a mixed ruderal- and stress-selected strategy with slow growth and year-long survival prevailing in sub-Arctic lakes and faster growth and shorter longevity in temperate lakes. Nostoc commune and its
close relative N. flagelliforme have a mixed stressdisturbance strategy not found among higher plants, with stress
selection to limiting water and nutrients and disturbance selection in quiescent dry or frozen stages. Despite profound
ecological differences between species, active growth of temperate specimens is mostly restricted to the same temperature range (035 8C; maximum at 25 8C). Future studies should aim to unravel the processes behind the extreme persistence and low metabolism of Nostoc species under ambient resource supply on sediment and soil surfaces.
Key words: Gelatinous colonies, cyanobacteria, Nostoc commune, Nostoc flagelliforme, Nostoc pruniforme, Nostoc
zetterstedtii, carbon use, carbon concentrating mechanisms, photosynthesis, light use, growth, long-lived, survival,
desiccation tolerance, nutrient-poor.
IN T RO DU C T IO N
The cyanobacterial genus Nostoc includes many species that are
highly diverse with respect to morphology, functional properties,
biotic relations and habitat distribution (Dodds et al., 1995).
Nostoc species have filaments with normal photosynthetic cells
and N2-fixing heterocysts and they periodically form resistant
akinetes for survival and short motile filaments (hormogonia)
for reproduction (Mollenhauer et al., 1994). Some species are
free-living and many species engage in loose or obligate cooperation with land plants and fungi (e.g. lichens; Mollenhauer,
1988; Kaasalainen et al., 2012). A third, fascinating Nostoc
type forms large gelatinous colonies of variable shape and
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18
Spain (Aboal et al., 2010) and recent DNA studies group those
two species together with N. sphaeroides and N. punctiforme
in a common clade (Arima et al., 2011; Gao et al., 2011),
which makes species identity dubious. Nonetheless, we maintain
the distinction between N. commune and N. flagelliforme here in
accordance with most available literature.
Nostoc pruniforme forms a beautiful, dark green, spherical
colony with a smooth surface like a plume. It is more common
and widely distributed both geographically and ecologically in
oligo- and mesotrophic freshwaters in temperate and subArctic regions than its rare freshwater cousin, N. zetterstedtii
(Dodds et al., 1995; Raun et al., 2009). Danish alkaline lakes
housing N. pruniforme contain .0.7 mM DIC (Sand-Jensen
et al., 2009b). In temperate lakes, N. pruniforme appears to
grow in diameter from 0.2 cm in late spring to 2 3 cm in midsummer and it can rapidly die off, supposedly because of attacks
by viruses or bacteria at high summer temperatures (K. SandJensen, unpubl. data). In contrast, in a cold (4 8C), nutrient-poor
spring in Oregon, USA, N. pruniforme reached a handball size of
15 17 cm in diameter and weighed 2.6 kg after sustained slow
growth for 9 14 years (Dodds and Castenholz, 1987). Very
large colonies are also found in cold transparent lakes in
Greenland (K. Sand-Jensen, unpubl. data). In addition to their
larger size and persistence, they differ from Danish temperate
specimens by having a more solid surface and a denser gel.
Two additional species, N. calcareous and N. sphaericus
(Mollenhauer et al., 1994) resemble N. pruniforme but are not
discussed further here.
The fourth species, N. zetterstedtii, is a rare, highly persistent
organism whose colonies resemble firm blackberries. It lives in
only 50 100 nutrient-poor soft-water lakes in Sweden and in a
few other lakes in neighbouring countries (Bengtsson, 1986,
1995; Mollenhauer et al., 1999). Soft-water lakes usually have
DIC concentrations of 0.02 0.3 mM and concentrations of
total phosphorus ,0.1 0.3 mM in open waters (Sand-Jensen
et al., 2009b). Among the freshwater phototrophic species
studied so far, Nostoc zetterstedtii has unprecedented low
growth and mortality rates (Sand-Jensen and Mller, 2011). In
oligotrophic Lake Varsjo, Sweden, it takes 3 years for
N. zetterstedtii to double its colony mass and 30 years to
reach the recorded maximum diameter of 7 cm (Sand-Jensen
and Mller, 2011). There is no apparent mortality of grazers
and pathogenic bacteria and viruses (Sand-Jensen and Mller,
2011). The persistence of N. zetterstedtii is confirmed by its
ability to survive for 14 months in the dark at 5 8C with intact
colony structure and unaltered fresh mass (K. Sand-Jensen,
unpubl. data).
All mentioned Nostoc species must have common structural
and functional properties linked to the large size and extensive
matrix of the colonies. However, the species differ with respect
to metabolism, growth, mortality, tolerance to environmental
stress and habitat preference. In this review, I first examine
some of the main structural properties of the three main
species (N. commune, N. pruniforme and N. zetterstedtii) with
supplementary data for N. flagelliforme related to the centimetrelarge size and gelatinous matrix of the colonies. Second, I evaluate theoretically the diffusive flux of DIC to the colony surface
for a set of environmental constraints on boundary layer thickness and external concentrations. Third, I examine the functional
consequences of the large colony size for the use of DIC and light
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behind the extremely low rates of growth and mortality and high
persistence, longevity and protection against environmental
hazards of gelatinous Nostoc colonies and their ability to economize with highly limiting resources.
The review focuses on four colonial Nostoc species: the sheetlike Nostoc commune, the closely related N. flagelliforme and
two species that form spherical colonies, N. pruniforme and
N. zetterstedtii. All four species resemble each other by
forming centimetre-large gelatinous colonies, but they differ in
distribution, habitat preference, growth rate, environmental tolerance and appearance (Fig. 1). Nostoc commune is a globally
widespread terrestrial and semi-aquatic species forming inactive
crusts when dry, but rapidly changing to 1 5-mm thick sheetlike gelatinous structures when wet (Scherer et al., 1984;
Marsh et al., 2006; Novis et al., 2007). Nostoc commune has unprecedented tolerance of environmental extremes (Satoh et al.,
2002; Tamaru et al., 2005; Sand-Jensen and Jespersen, 2012).
It tolerates desiccation during dry seasons and can survive for
.100 years on a museum shelf (Cameron, 1962). It tolerates
freezing to 60 8C in Antarctic deserts (Davey, 1989; Novis
et al., 2007) and to 269 8C in liquid helium in the laboratory
(Sand-Jensen and Jespersen, 2012), but rapidly resumes metabolism when rewetted at physiologically suitable temperatures
between 0 and 30 8C (Scherer et al., 1984; Taranto et al., 1993;
Sand-Jensen and Jespersen, 2012; Mller et al., 2014). Nostoc
flagelliforme is also widely distributed in arid and semi-arid
areas throughout the world (Gao et al., 2012; Ye et al., 2012).
It has a thread-like appearance but resembles N. commune in
its genetics, growth habitat, colony composition and extreme tolerance to and rapid recovery from desiccation, freezing and salt
stress (Gao and Zou, 2001; Qiu et al., 2004; Huang et al., 2005;
Yong-Hong et al., 2005; Liu et al., 2010; Arima et al., 2011). We
have observed Nostoc with the typical morphology of both
land,
N. commune and N. flagelliforme on the Great Alvar on O
Sweden (Sand-Jensen et al., 2010). Nostoc flagelliforme has
been classified as a variety of N. commune in arid regions of
Flat structure
N. pruniforme
Sphere
Nostoc zetterstedtii
N. trichomes
Sphere,
granulated surface
Cylinders
Submerged leaves
Flat structure
Single-celled algae or
cyanobacteria
Sphere
S I Z E , S HA P E AN D CO M PO S I T IO N
Centimetre-thick colonies with photosynthetic filaments embedded in a gelatinous matrix exert large physical constrains on
functional properties.
Shape
Diameter/
thickness (cm)
0.1
0.5
0.2
17.0
0.2
7.0
5 10 4
10 10 4
1 10 3
30 10 3
2 10 4
2 10 3
SA:V
(cm 1)
10 to 20
2 to 4
30
0.36
30
0.851.7
8000
4000
2000
70
30 000
3000
SA:V ratio is only 1.7 cm 1 for the largest N. zetterstedtii colonies. The granulated surface could, in theory, double the
diffusion-limited uptake of external solutes for N. zetterstedtii
by doubling the surface area compared with smooth colonies
of N. pruniforme of the same diameter (see section Size
effects, diffusive supply and loss of solutes). The granulated
surface could also contribute to the formation of thinner diffusion boundary layers (DBL) around the surfaces of
N. zetterstedtii when the granules increase micro-turbulence
(Boudreau and Jrgensen, 2001). The micro-topography of the
granulated surface can result in thinner DBLs at the protruding
tips of the granules and thicker DBLs in the crevices between
the granules (Carpenter and Williams, 1993; Jrgensen, 2001)
so the diffusion geometry is difficult to interpret. Although diffusive fluxes remain experimentally unexplored, they are, nonetheless, highly relevant considering that N. zetterstedtii usually
grows in lakes with lower concentrations of DIC, N and P than
N. pruniforme (Sand-Jensen et al., 2009b).
Composition of colony matrix
A high proportion of Nostoc colonies is composed of the extracellular matrix, primarily of polysaccharides of high viscosity
and molecular weight. The hydrolysed polysaccharides from
N. flagelliforme were mainly composed of glucose (43 %),
galactose (30 %), xylose (21 %), mannose (6 %) and small
amounts of glucuronic and uronic acids (Jia et al., 2007;
Pereira et al., 2009). Much the same main sugars were hydrolysed
from hot water extracts of polysaccharides from field samples of
N. commune, N. flagelliforme and N. sphaeroides, though small
amounts of arabinose appeared in N. flagelliforme and rhamnose
and fucose in N. sphaeroides (Huang et al., 1998). The composition of extracellular compared with intracellular polysaccharides was suggested to be quite different in N. commune and
N. flagelliforme, perhaps due to a selective mechanism for excretion of polysaccharides (Mehta and Vaidya, 1978). Different
studies of N. commune have shown the complex chemistry of
the hydrolysed matrix, which includes six to nine monosaccharides, uronic acid, deoxy-sugars, pyruvate, acetate and peptides
(Pereira et al., 2009). Scanning electron microscopy has revealed
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19
20
N. zetterstedtii
Relationship
CMA 184 + 47
(mean + s.e.)
Log CMA 0.0474 log
FM + 1.88
CMA for 0.1 g
FM colony 69
CMA for 4.0 g
FM colony 81
Log CMA 0.26 log
FM + 3.13
CMA for 0.1 g
FM colony 587
CMA for 4.0 g
FM colony 1531
Source
K. Sand-Jensen, unpubl. data
C. Mller and K. Sand-Jensen,
unpubl. data
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21
22
Equation
Fa r 2 (r(r + d) d 1) D (Cm Co) r 1 (1 + r/d) D (Cm Co)
Fa d 1 D (Cm Co); (r d)
Fa r 1 D Cm; (Co 0)
Fcol 4p r D Cm; (Co 0)
Fv 3 r 2 D Cm; (Co 0)
Fvs r 1 Ls 1 D Cm; (Co 0)
C (r) 1/3 Pv D 1 r 2; (Cm 0)
C (r) Pv Ls r D 1; (Cm 0)
10 000
20, 03
20, 10
20, 30
05, 03
05, 10
05, 30
01, 03
01, 10
01, 30
1000
100
10
01
10
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25
20
15
10
05
0
05
05
10
15
20
25
23
In addition to DIC, the metabolism and growth of Nostoc colonies could be constrained by the supply rate of dissolved inorganic phosphorus (DIP). Nitrogen can be fixed as elementary
N2 and is less likely to be limiting, although growth stimulation
by high external concentrations may occur, particularly for terrestrial species with unrestricted access to atmospheric CO2
(see later). Lakes and ponds with Nostoc species mostly have
DIP concentrations in the water column ranging from undetectable by standard chemical methods to 0.3 mM (Sand-Jensen
et al., 2009b), though higher concentrations can occur at the sediment surface. For a DIP gradient of 0.3 mM across a 1 mm thick
DBL, the estimated influx was 0.22 nmol P cm 2 h 1 for small
colonies (radius 1 mm) and 0.12 nmol P cm 2 h 1 for large colonies (radius 10 mm). These fluxes should permit a turnover time
of the P pool within 6 d for small and 72 d for large colonies of
N. zetterstedtii, supporting the hypothesis that growth is more
likely to be constrained by the supply rate of DIC across gradients
of 0.1 mM HCO3 . These calculations agreed with the observation
that growth was unaffected by P richness in the sediments of softwater Lake Varsjo (Sand-Jensen and Mller, 2011).
DIC supply is also important in dense epilithic communities
growing on inert substrata and covered by relatively thick boundary layers (Sand-Jensen, 1983). Thus, short epilithic algal communities in marine waters have DBL thicknesses similar to those
applied for Nostoc colonies and they appear to be constrained by
the DIC flux to photosynthesis despite high HCO3 concentration
(2 mM) in seawater. Larkum et al. (2003) showed that DBLs of
epilithic algal communities covering dead coral surfaces were
0.18 0.59 mm thick under moderate flow (8 cm s 1) and
.2 mm under quasi-stagnant conditions, and they generated
high resistance to DIC influx, limiting primary production.
Independent experiments with epilithic algal communities in
other coral reef environments appeared to support the conclusion
that DIC is a main limiting factor, as elevated nutrient levels had
no effect on primary production and growth (Larkum and Koop,
1997; Miller et al., 1999), while large macroalgae in such
nutrient-poor waters were stimulated by nutrient amendment
(Lapointe et al., 1987).
Resource supply solely by diffusion
The flux to Nostoc colonies may be controlled entirely by diffusion in a stagnant water layer overlying the sediment. A stagnant surface layer may exist almost permanently in deep water
with restricted turbulence and periodically in shallow water
during calm weather. The colonies could be buried in a viscous
boundary layer a few centimetres thick overlying the sediment
(Boudreau and Jrgensen, 2001). When the surrounding water
is virtually stagnant and the solute concentration is reduced to
zero at the colony surface, the flux per unit surface area is inversely scaled to colony radius, emphasizing the immense advantage
of being small (eqn 3 in Table 3). The calculated flux is 720 nmol
C cm 2 h 1 for small colonies (radius 1 mm) in water containing
2 mM HCO3 or half the flux that occurs when DBL is 1 mm thick
(eqn 1). For large colonies (radius 10 mm), however, the flux in
stagnant water is only 72 nmol C cm 2 h 1, or 11-fold lower than
in stirred water with a DBL of 1 mm. The potential biomass turnover time for large colonies as described above would then be 120
d for N. pruniforme under stagnant conditions in hard-water lakes
and 32 350 d (89 years) for N. zetterstedtii in soft-water lakes.
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24
The diffusive flux through stagnant water to a smooth, spherical colony follows the well-known formula often used for bacteria
(eqn 4 in Table 3; Fenchel et al., 1998) because the colonies are
usually so small relative to the thickness of DBL that the supply
rate is entirely determined by diffusion. When metabolic activity
and the demand for external resources are evenly distributed
throughout the colony volume, the flux relative to unit volume
(Fv) will be inverselyscaled to the second power of radius, emphasizing the likelihood of extreme limitation as the organisms grow
in size (eqn 5 in Table 3). The solutions to cope with this rapidly
increasing risk of resource limitation with larger size would be
either to reduce volume-specific requirements for metabolism
(in the case of N. zetterstedtii) or develop a hollow sphere
where all activity is restricted to an outer shell of thickness Ls
and volume 4/3p (r 3 (r Ls)3) 4p (r 0.5Ls)2 Ls. When r
is large relative to Ls, volume is close to 4p r 2 Ls and the flux relative to volume of the outer shell (Fvs) declines linearly with
colony radius (eqn 6 in Table 3).
Thus, a 10-fold increase in colony radius will reduce the flux
relative to the surface area and volume of a hollow spherical
colony by the same order of magnitude, while the flux relative
to the volume of a homogeneous, solid spherical colony declines
100-fold, emphasizing that if large colonies are indeed solid then
their central parts must be composed of recalcitrant matrix material and either have no cells or cells of low metabolism. Because
N. zetterstedtii colonies with a diameter of 10 20 mm absorb
96 % of incident irradiance from the surface to the centre
(Sand-Jensen et al., 2009b), there is no scope for photosynthesis
of Nostoc trichomes in the centre, but there is organic matter
present here that could potentially be used by heterotrophic bacteria. The colony matrix is persistent and protected by bactericides (Sand-Jensen et al., 2009a), however, implying that there
are no or very few active heterotrophic bacteria living within
N. zetterstedtii colonies. The year-long persistence and low respiration rates of the colonies in complete darkness support this
implication (see below).
Efflux of solutes
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Both values are very high, stressing that the water overlying the
sediment is either not entirely stagnant or is enriched with DIC
(CO2 and HCO3 ) from sediment decomposition. Maberlys
(1985) measurements 10 cm above the sediments in a shallow
bay covered by the moss Fontinalis antipyretica showed elevated
CO2 concentrations relative to surface waters between 0.05 and
0.26 mM on 14 different dates. Concentrations are higher directly
on the sediment surface and a near-bed CO2 concentration of, for
example, 0.3 mM CO2 could permit a 6-fold higher influx of CO2
than a HCO3 gradient of 0.1 mM because the diffusion coefficient
of CO2 is approximately twice that of HCO3 (Denny, 1993). The
resulting turnover time could then be 6.3 years for large colonies
of N. zetterstedtii if we assume that the granulated surface
doubles the influx and 3.2 years if the inward flux continues in
both light and darkness. Thus, we cannot exclude that large colonies of N. zetterstedtii could survive in an entirely diffusive environment provided available concentrations of CO2 and HCO3
were markedly higher than 0.1 mM. Small colonies a few millimetres in diameter can perform well by diffusive fluxes alone
and are likely to be fully embedded in a diffusive boundary
above the sediment surface.
25
Pmax
(nmol O2 cm
N. commune
N. pruniforme
N. zetterstedtii
353 376
552 654
206 409
h )
(mg O2 mg Chl
2.4
2.1
0.7
Pmax/dark respiration
Icomp (mmol m 2 s 1)
Quantum efficiency
(mmol O2/mol photons)
Absorption (%)
2.5
10
2.0 5.8
9.5
19
19.3
20
55
90
96
h )
The large size, long internal light paths and high densities of
trichomes within Nostoc colonies imply that light absorptance
and internal self-shading are high. Mean light absorptance
ranged from 55 % in N. commune to 96 % in N. zetterstedtii
(Table 4). Moreover, because the cells experience high O2 and
low CO2 concentrations within the colonies during photosynthesis, maximum photosynthesis relative to cell chlorophyll
(i.e. the assimilation number), maximum quantum efficiency
of photosynthesis and the ratio of photosynthesis to respiration
should be much lower than among free-living unicells. To the
extent that photons are absorbed by non-photosynthetic pigments and other coloured substances inside the colonies,
maximum quantum efficiency will decline further.
Quantum efficiency was indeed low for N. commune [average
19.1 mmol O2 (mol absorbed photon) 1] and N. zetterstedtii
(11.2 39.9 in three series; Table 4). A similarly low efficiency
[27 mmol O2 (mol photon) 1] was calculated for the thickwalled, balloon-like green macroalga Codium bursa (GeertzHansen et al., 1994) and microbial mats with extensive absorption (40 80 %) by structural components (Al-Najjar et al.,
2012). In contrast, quantum efficiencies are much higher for freeliving microalgae [70 120 mmol O2 (mol photon) 1], macroalgae and submerged plants [37 79 mmol O2 (mol photon) 1]
(Frost-Christensen and Sand-Jensen, 1992).
Nostoc zetterstedtii had particularly low light-saturated
photosynthesis relative to chlorophyll (average 0.5 0.7 mg O2
mg 1 chlorophyll a h 1) and values were also low for
N. commune (average 2.4) and N. pruniforme (average 2.1).
Likewise, photosynthesis relative to dark respiration (NP:R)
was low for N. zetterstedtii (2.0 5.8) and N. commune
(average 2.5), but not for N. pruniforme (average 10). Again freeliving unicells have higher rates of photosynthesis relative to
chlorophyll, typically between 2 and 20 (Harris, 1978) and
NP:R ratios from 5 to 20 (Harris, 1978; Geider and Osborne,
1992). High self-shading within Nostoc colonies is an important
constraint because photosynthesis at high irradiance increased
4-fold and NP:R increased 3-fold when self-shading was
reduced by cutting colonies of N. zetterstedtii into 1 2-mm
pieces (Sand-Jensen et al., 2009b).
Light attenuation by coloured substances, structural substances and dead or senescent cells within the colonies competes
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26
No. of
measurements
N. pruniforme*
72 + 4
82 + 3
56 + 3
16
12
5
N. zetterstedtii
74 + 9
16
Species
N. commune
Source
K. Sand-Jensen
(unpubl. data)
Raun (2006); Raun
et al. (2009)
Sand-Jensen et al.
(2009)
TA B L E 6. Final pH, final DIC, HCO3 and CO2 and final O2/HCO3 ratio of the four Nostoc species after 20 h of photosynthesis in
closed bottles. Ranges are shown from several experimental series with many replicates
Species
N. commune
N. pruniforme*
N. zetterstedtii
N. flagelliforme
Initial DIC
(mmol L 1)
Final pH
106310
570
149162
3300
10.6811.11
10.6
10.9411.06
10.8
Final DIC
(mmol L 1)
Final HCO3
(mmol L 1)
Final CO2
(nmol L 1)
O2/HCO3
No. of series
1290
260
77174
6 34
110
13 35
1 7
,30
3 10
960
5
18 29
5
1
4
*Maximum final pH and minimum final DIC, HCO3 and CO2 probably not attained.
Sources: N. commune (K. Sand-Jensen unpubl. data); N. pruniforme (Raun, 2006; Raun et al., 2009); N. zetterstedtii (Sand-Jensen et al., 2009); N. flagelliforme
(Gao and Zou, 2001).
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95 % CL
N. commune
5.8
6.5
9.0
10.2
8.67
8.57
16.3
24.5
1.1
0.5
1.7
2.3
1.33
0.84
2.9
5.6
N. pruniforme
N. zetterstedtii
Source
K. Sand-Jensen (unpubl. data)
2 0
Small colonies
1 5
1 0
2 0
Medium-sized colonies
1 5
1 0
05
2 0
Large colonies
1 5
1 0
0 5
1
2
External DIC (mM)
0 5
external DIC supply as photosynthetic rates at 0.1 mM DIC externally were 20 % of the maximum rate for N. commune, 11 %
for small, 13 % for medium-sized and 25 % for large colonies
of N. pruniforme and 60 % for N. zetterstedtii (Figs 4 and 5).
As the internal DIC pool in N. zetterstedtii colonies is gradually
exhausted during 18 h of light incubation in closed bottles, realized mean rates of O2 production are 1.8-fold lower in water initially containing 0.29 mM compared with water initially
containing 0.99 mM DIC (Fig. 3). In N. pruniforme, which has
higher rates of photosynthesis and DIC requirements per
surface area than N. zetterstedtii and apparently 2-fold lower internal DIC pools, the dependency of photosynthesis on external
DIC was stronger, showing half-saturation constants of 0.78 mM
for small colonies (0.1 g FM) and 1.24 mM for larger colonies
(2.5 g FM) in 2-h experiments under well-stirred conditions
(Fig. 4). Large colonies have higher rates of photosynthesis
(164 nmol O2 cm 2 h 1) at near-zero external DIC than small
colonies (55 nmol O2 cm 2 h 1), probably because of a larger internal DIC pool (being scaled to colony volume) relative to
photosynthetic activity (being scaled to colony surface area).
The more favourable SA:V ratio in small colonies causes photosynthesis to increase more steeply with increasing external DIC
(a-CO2, 319 nmol O2 cm 2 h 1 for a 1-mmol L 1 increase in external DIC) than in large colonies [a-CO2, 197 nmol O2 cm 2 h 1
(mmol DIC L 1) 1] (Fig. 4).
The terrestrial and semi-terrestrial N. commune and
N. flagelliforme can use CO2 and HCO3 under water and CO2
alone in air. Under water, N. commune experiences limitation
of photosynthesis at low DIC as rates rise to at least 1 mM. The
diffusion coefficient of CO2 in air is 2 104 times higher
than that of HCO3 in water, and for the same DBL thickness
and with complete DIC depletion at the colony surface the CO2
gradient is 3050 times lower in air (external CO2 0.02 mM)
than in water containing 0.6 1.0 mM HCO3 . Thus, the potential
flux would be substantially higher (500- to 700-fold) in air than in
water through a diffusive boundary layer of the same thickness
overlying the colony surface, but this is followed by the same resistance through the colony to the Nostoc filaments in both terrestrial and aquatic habitats. At high irradiance and twice daily
800
N. commune
N. pruniforme
N. zetterstedtii
600
400
200
0
0
1000
HCO3
2000
concentration (mol
3000
L1)
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Species
27
28
TOL E R A N C E O F E N V I RO N M E N TA L E X T R E M E S
Freshwater Nostoc species do not experience extreme temperatures like those experienced by terrestrial species. Active growth
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