Supplemental Method S1. Detailed description of spectral decomposition analyses.
We collected 1,625 fluorescence spectra from individual Anabaena variabilis cells under excitation conditions based
on pulsed 808 nm two-photon excitation (TPE) or 785 nm continuous-wave one-photon excitation (OPE) lasers. We
analyzed vegetative cells and cells at different stages of heterocyst differentiation to select a reasonable set of component
spectra that were necessary and sufficient to reproduce all of the observed fluorescence spectra. The three subunits of
phycobilisomes (PBS), phycoerythrocyanin (PEC), phycocyanin (PC), and allophycocyanin (APC), have different
fluorescence peaks (Bryant et al., 1976). The chlorophyll fluorescence spectra of cyanobacteria can be described by at
least photosystem II (PSII) and photosystem I (PSI) at physiological temperatures (Vermaas et al., 2008). Thus, the
minimal set of component spectra should be PEC, PC, APC, PSII, and PSI.
We found that these five spectra were sufficient to describe all experimentally observed single-cell fluorescence
spectra with the aid of singular value decomposition (SVD) analysis. All of the single-cell spectra with 83 wavelength
channels (580–753 nm range) were analyzed using SVD and minimization functions in Mathematica 5.2 (Wolfram
Research, Champaign, IL, USA). The five SVD spectra with the largest singular values, SVDi ( ) (i =1, 2,.., 5), as
shown in Supplemental Figure S2, were necessary and sufficient to reproduce the original single-cell spectra under
various conditions.
5
cell ( , n)   f ni SVDi ( ) ,
(eq. 1)
i 1
where cell(,n) and fni represent 1,625 single-cell spectra (n=1,2,3,…..,1625) and optimized coefficients given by the
SVD, respectively. The 83 singular values are shown in Supplemental Text S1.
In general, SVD spectra can be negative in amplitude at some wavelength channels. Physically meaningful
fluorescence component spectra with non-negative amplitudes must be prepared to reproduce the five SVD spectra
through linear combinations. The spectra of the three subunits of PBS (PEC, PC, and APC) were essentially equal to
those for isolated subunits reported in the literature (Zehetmayera et al., 2004; Seibert et al., 1984; Molecular Probe
Handbook, respectively). We compared slightly different spectra reported in different papers (Bryant et al. 1976;
Grabowski and Gantt 1978; Zhao et al. 1999; Stadnichuk et al., 2012) and assumed that the three publications listed
above gave typical spectra. The PSII fluorescence spectrum was taken from that of the green alga Parachlorella kessleri
obtained using the same microspectroscopic system under 808 nm TPE. In that spectrum, there was no PBS fluorescence
and only a small contribution from PSI (Hasegawa et al., 2011). The PSI fluorescence spectrum was selected from
spectra of mature heterocysts of A. variabilis under 785 nm OPE, as shown in Figure 5C. PSI showed the weakest
fluorescence intensities around the 650–680 nm region, compared with its presumed peak around 730 nm (Mannan and
Pakrasi, 1993). The shapes of the PEC, PC, APC, and PSII component spectra were slightly modified from their originals
through global minimization with the following sum of squares of the differences between linear combinations of the
five component spectra and the five SVD spectra (SVDi(), i =1, 2,.., 5).
 SVD ( )  c CS ( )
5
83
5
i 1 n 1 j 1
2
i
n
ij
j
n
,
(eq. 2)
where CSj() (j = 1, 2,..., 5 ) represents non-negative fluorescence component spectra corresponding to PEC, PC, APC,
PSII, and PSI; cij is a fitting coefficient that can be positive or negative; and n (n=1,2,....,83) represents wavelength
channels. This modification of the spectral shapes was necessary because the original spectra were obtained from
different organisms or from isolated pigment–protein complexes with different spectroscopic systems. The original
reference spectra of PEC, PC, and APC were fitted by the sums of two or three Gaussian functions. The peak
wavelengths and spectral widths of the constituent Gaussian functions were optimized using (eq. 2), while energy
differences, relative peak amplitudes, and relative spectral widths between the constituent Gaussian functions for each
component spectrum were kept constant. The global minimization also led to a shift in the peak wavelength of the
component spectrum corresponding to PSII (from 687.7 nm to 685.6 nm). The resultant fluorescence component spectra
are shown in Supplemental Fig. S1 and formed the basis for all spectral decomposition analyses in this work.
Supplemental Text S1. Eighty-three singular values obtained in SVD analyses of 1,625 single cell spectra.
{160.475, 72.9426, 19.4042, 7.5402, 4.57093, 3.80724, 2.59871, 2.28853, 2.25071, 2.17249, 1.98124, 1.92178, 1.80585,
1.75254, 1.68272, 1.6046, 1.58774, 1.57658, 1.54283, 1.4916, 1.44971, 1.41783, 1.33329, 1.31024,
1.27731, 1.24625, 1.21698, 1.19912, 1.11174, 1.09321, 1.08841, 1.04115, 1.01269, 0.997438, 0.989919, 0.972824,
0.966465, 0.937698, 0.903766, 0.867798, 0.831711, 0.786282, 0.7635, 0.743982, 0.730066, 0.727267, 0.716286,
0.688729, 0.671312, 0.641553, 0.63187, 0.622513, 0.616366, 0.610846, 0.591085, 0.565813, 0.549806, 0.520436,
0.514574, 0.489691, 0.466417, 0.445681, 0.428441, 0.416726, 0.401421, 0.373294, 0.365148, 0.358288, 0.351325,
0.333834, 0.325884, 0.32151, 0.315789, 0.30385, 0.295434, 0.288043, 0.27967, 0.276639, 0.270394, 0.26639, 0.253661,
0.249124, 0.241957}
Supplemental Text S2. Note on independence and synchronization between APC and PSII.
Given the very similar temporal behavior between APC and PSII, one may suspect that our spectral decomposition
did not allow the two components behave independently. The PSII and APC fluorescence spectra behave as inseparable
components in the first two SVD spectra (SVD1 and SVD2; Supplemental Fig. S1 and S2), because the sign of the SVD
spectral amplitude was constant between 660 and 685 nm (Supplemental Fig. S2). On the other hand, SVD3 consisted of
a negative peak around 685 nm (PSII), positive peaks at 620–645 nm (PEC and PC), and little amplitude around APC
fluorescence (660 nm). In addition, both SVD4 and SVD5 spectra showed negative and positive peaks at around 660 and
685, respectively, indicating that an increase in PSII fluorescence was accompanied by a decrease in APC fluorescence
and vice versa (Supplemental Fig. S1 and S2). A simultaneous increase in PSII with a decrease in APC was indeed
observed in vegetative cells (Fig. 3, B and C). Overall, our spectral analyses showed that APC and PSII were intrinsically
independent components, but their degradation during differentiation was synchronized.
Supplemental Text S3. Note on whole-cell integrated PSI fluorescence intensities.
Ideally, estimates of total quantities of PSI in single cells should be obtained by integrating the fluorescence between
700 and 753 nm under 785 nm OPE over the whole 3D region. Because we performed fluorescence intensity
measurements at only three z-sections (three focal points with an interval of 0.6 μm), we estimated fluorescent region
volumes of single cells based on measured 2D areas as follows.
Whole 2D cell sizes of heterocysts observed in bright-field microscope images, whether in white or monochromatic
illumination, were typically larger than those of vegetative cells (Figs. 1, 4, and 9A; Supplemental Fig. S10A) because
heterocysts have a thick layer of polysaccharides and glycolipids outside the outer membrane (Maldener and
Muro-Pastor 2010). The PSI fluorescent region in heterocysts under 785 nm OPE did not reflect the whole-cell size, but
showed the distribution of PSI in thylakoid membranes. The fluorescent regions in which average fluorescence spectra
were estimated were therefore limited to the volume of the cytoplasm where thylakoids were present. The abundance of
PSI in a single cell was thus proportional to the product of the average fluorescence intensity on a per-pixel basis, as
shown in several figures and tables, and PSI-fluorescent cytoplasmic volume over which average fluorescence was
calculated. The PSI-fluorescent cytoplasmic volume of a single heterocyst cell, which was estimated from the area of the
fluorescent region under 785 nm OPE, was on average equal to those of nearby vegetative cells for intercalary
heterocysts and approximately 27% smaller for terminal heterocysts (Supplemental Table S2).
Supplemental Text S4. Estimation of absolute quantity of chlorophyll a in single cells.
The absolute quantity of chlorophyll a could be derived from absorbance values of the microscopic absorption
spectra (Fig. 2). We focused only on whole-cell average chlorophyll quantities in individual cells. If we assumed that all
chlorophyll a remaining in the heterocyst was attributable to PSI, we could estimate the total quantity of PSI in single
heterocyst cells. The apparent absorbance values of a mature heterocyst based on microscopic absorbance at 680 nm
were approximately 70% of those in vegetative cells when the two cell types were compared in filaments grown
diazotrophically for longer than 10 d (Fig. 2D). The decrease in absorbance was primarily attributed to the decrease in
chlorophyll concentration in single cells, because even the longest-wavelength absorbing subunit of the phycobilisome,
APC, showed only 5–7% of the peak absorbance at around 650 nm (Grabowski and Gantt 1978; Murakami et al., 1981;
Rolinski et al., 1999; MacColl et al., 2003; Supplemental Table S2). The width of heterocyst cells (perpendicular to the
filament axis) was comparable to that of vegetative cells in the fluorescence map generated under 785 nm OPE (Fig. 9B;
Supplemental Fig. S10B); however, the heterocyst appeared to be thicker than vegetative cells because of the thick layer
of polysaccharides and glycolipids. The cross-section of cytoplasm perpendicular to the filament axis was thus assumed
to be constant between heterocysts and vegetative cells. Based on the above reasoning and the model detailed in
Supplemental Table S2, we estimated that the average concentration of chlorophyll a in heterocysts was 70% of that of
vegetative cells. On average, the cytoplasmic volume of intercalary heterocysts estimated from fluorescence under 785
nm OPE was as large as that of vegetative cells (Supplemental Table S2). The fluorescent volume of terminal heterocysts
estimated in the same way was approximately 27% less than that of vegetative cells (Supplemental Table S2). Because of
the polar distribution of thylakoid membranes in the terminal heterocyst, only the periphery close to its adjacent
vegetative cell was bright in the fluorescence image (Supplemental Fig. S10B). Although the volume of the whole
cytoplasmic region of the terminal heterocyst thus had to be estimated by another method, we estimated the total PSI
quantity in the single terminal heterocyst from the PSI-rich fluorescence area (Supplemental Table S1). Thus, the total
amount of chlorophyll per terminal or intercalary heterocyst cell was approximately 57% or 74%, respectively, of that in
vegetative cells (Supplemental Table S2).
Supplemental Table S1. Average area of PSI-rich fluorescent regions under 785 nm OPE.
These average values were calculated from two types of micro-spectroscopic data. The first type is based on 15 filaments
of cells grown under nitrogen-depleted conditions for longer than 10 d in a shaken flask then transferred to a
glass-bottomed dish just before microscopic experiments. Data from these experiments is also shown in Supplemental
Figure S9. The other type is based on filaments at 72 or 96 h after the start of nitrogen deprivation. Data from these
experiments are also shown in Figure 8 in the main text.
Cell type
PSI fluorescent area
Standard deviation
(m2)
(m2)
Het, terminal (n=23)
12.1
2.9
Het, intercalary (n=7)
16.6
3.3
Veg. 1 (n>30)
16.1
3.7
Veg. 2 (n>30)
15.9
3.3
Veg. 3 (n>30)
16.1
3.3
Veg. 4 (n>25))
16.4
3.7
Veg. 5 (n>25)
17.6
4.1
Veg. 1, Veg. 2,… Veg. 5 represent sequential cell positions beginning at the vegetative cell adjacent to a heterocyst in the
same filament.
Supplemental Table S2. Estimates of absolute amounts of PSI and PSII monomer units in single cells.
PSI Fluorescent areaa
Terminal
Intercalary
Vegetative
heterocyst
heterocyst
cell
12.1 (±2.9) m2
16.6 (±3.3) m2
16.4 (±3.6) m2
33.2 m3
45.6m3
45.1m3
(0.73)
(1.01)
(1.00)
S  dL
Volumeb (ratio)
2
d 
V      L  t eff  d  L
2
Offset absorbance at 680 nmc
0.092
A680730
0.131
(upper limit of PBS contribution
A680730,Het   Chl,680cChl,Het teff
  Chl, 680cChl t eff   APC,680cAPCt eff
0.074×0.07=0.005)d,e
A680730,Veg
  Chl,680cChl,Veg teff  0.005
Offset absorbance at 650 nmc
0.026
0.100
(upper limit of PBS
contribution
0.100 × 0.026=0.074)e
Mass of chlorophylls in single cell
0.13 pg (0.54)
(ratio)
M term, Het 
893  cChl  V 10
15
Number of PSI monomer units
893cChl,HetVterm, Het 10
8.8 × 105
0.17 pg (0.74)
0.23 pg (1.00)
M veg 
M inter,Het 
15
893cChl,HetVinter,Het  10
1.2 × 106
in single cellf
15
893cChl,Veg Vveg 10 15
1.2 × 106
(assumption)h
cChl
 V  10 15  6.02  10 23
96
Number of PSII monomer units in
single cellg,j
0 (assumption)i
0 (assumption)i
1.2 × 106
M
Veg
 M inter,Het 
893  35
aAreas
 6.02 10 23
are taken from Supplemental Table S1. In our model, the cytoplasmic volume of cells was tentatively assumed to
be a cylinder with a diameter of d and a height (or length) of L. The area here was thus assumed to be given by: S = d ×
L. The diameter (d) was also tentatively assumed to be 3.5 m for both heterocysts and vegetative cells, based on our
observation that the terminal heterocyst appeared to be shorter than the intercalary heterocyst and vegetative cells along
the filament axis in the PSI-rich fluorescence images, but the dimension of cells perpendicular to the filament axis was
similar among the three cell types (terminal heterocyst, intercalary heterocyst, and vegetative cell) (Fig. 9B,
Supplemental Fig. S10B).
b
In our model, the different volumes of cytoplasm in different cell types were assumed to be related to the different
lengths L along the filament axes. We also assumed a rectangular parallel shape with dimensions of teff, d, and L with the
same volume as that of the model cylinder. teff is the effective optical path length for microscopic absorbance.
c
Offset absorbance values were obtained from the microscopic absorption spectra shown in Figure 2D. The extinction
coefficient of chlorophyll a at 680 nm was 7.9×104 cm-1 dm3 mol-1 (Porra et al. 1989).
d
Maximum offset absorbance at 680 nm contributed by PBS was estimated from absorption spectrum of APC
(Grabowski and Gantt 1978; Murakami et al., 1981; Rolinski et al., 1998; MacColl et al., 2003) and offset absorbance at
650 nm (Fig. 2D).
eUpper
limit of PBS contribution to offset absorbance at 650 nm was assumed to be given by the difference in offset
absorbances between vegetative cells (0.100) and heterocysts (0.026).
fPSI
monomer contains 96 chlorophyll a molecules, according to the crystal structure of PSI from Synechococcus
elongatus (Jordan et al., 2001).
gPSII
monomer contains 35 chlorophyll a molecules, according to the crystal structure of PSII from
Thermosynechococcus vulcanus (Umena et al., 2011).
hNumber
of PSI monomer units was assumed to be the same in intercalary heterocyst and vegetative cells, as supported
by data shown in Figures 4, 5, and 8 and Supplemental Figures S7, S8, and S9. Similar volumes between these two cell
types were supported by data shown in Supplemental Table S1.
iPrevious
studies have reported that some PSII remains in the heterocyst. Although small amounts of PSII may be
detected in the heterocyst under 785 nm OPE (Fig. 8; Supplemental Fig. S7), we have no quantitative measurement for
this value.
PEC,
PC,
APC,
PSII,
PSI
fluorescence intensity (a.u.)
1.0
0.8
0.6
0.4
0.2
0.0
580
600
620
640
660
680
wavelength (nm)
700
720
740
Supplemental Figure S1. Fluorescence spectra of PEC, PC, APC, PSII, and PSI. The sum of these five component
spectra reproduced all single-cell fluorescence spectra observed in this study. See Supplemental Method S1 for details
and Figure 6 in the main text for spectral decomposition examples.
Supplemental Figure S2. Five spectra (dots) derived by singular value decomposition of 1,625 single-cell spectra. The
single-cell spectra included both vegetative cells and heterocysts at different stages of differentiation. The solid line is
the best fit given by the sum of the five component spectra in Supplemental Figure S1. Amplitudes were normalized with
the maximum absolute value set to 1.0.
Supplemental Figure S3. Time dependence of relative peak amplitudes of five normalized spectral components in six
Anabaena variabilis filaments, including heterocysts and adjacent vegetative cells. Average values are connected by
solid lines (±SD). Broken lines show maximum and minimum values. Amplitudes were normalized against that of APC
in the vegetative cell adjacent to the heterocyst in the same filament. Graphs were drawn using data on filaments under
nominally identical experimental conditions to those used for the data in Figure 7 (Supplemental Fig. S4). Note that
decays of APC and PSII were delayed by about half a day compared with those in Figure 7. Normalization based on APC
amplitude in the adjacent vegetative cell was used so that all data sets obtained under 808 nm TPE shared common
features, as described in the main text. Het., heterocyst; Veg. 1, vegetative cell adjacent to heterocyst; Veg. 2, vegetative
cell adjacent to Veg. 1.
Supplemental Figure S4. Normalized amplitudes of data shown in Figure 7. Data show the time dependence of five
normalized spectral components of Anabaena variabilis filaments, including heterocysts and adjacent vegetative cells.
Average values are connected by solid lines. Error bars show SD. Maximum and minimum values are connected by
broken lines. Plots are based on the same data shown in Figure 7 in the main text, but amplitudes were normalized to that
of APC in vegetative cells adjacent to heterocysts in the same filament to allow comparison with Supplemental Figure S3.
Het., heterocyst; Veg. 1, vegetative cell adjacent to heterocyst; Veg. 2, vegetative cell adjacent to Veg. 1.
PC
fluorescence
intensity (a.u.)
fluorescence
intensity (a.u.)
fluorescence
intensity (a.u.)
fluorescence
intensity (a.u.)
PEC
APC
PSII
30
PSI
20
20
20
15
15
15
10
10
10
5
5
5
0
0
0
0
20
20
20
30
15
15
15
10
10
10
5
5
5
0
20
0
0
0
20
20
30
15
15
15
10
10
10
5
5
5
0
0
0
0
250
200
150
100
50
0
20
20
20
30
250
15
15
15
10
10
10
5
5
5
0
0
0
60
time (hour)
20
10
60
time (hour)
Het.
250
200
150
100
50
0
20
10
20
10
Veg.1
Veg.2
200
20
150
Veg.3
100
10
50
0
0
0
250
200
150
100
50
0
0
60
time (hour)
0
0
60
time (hour)
0
60
time (hour)
Supplemental Figure S5. Time dependence of five fluorescence components obtained from eight Anabaena variabilis
filaments with heterocysts in the same glass-bottomed dish under 785 nm OPE. Unnormalized average amplitudes are
shown by solid lines. Error bars show SD. Broken lines show maximum and minimum values. Het., heterocyst; Veg. 1,
vegetative cell adjacent to heterocyst; Veg. 2, vegetative cell adjacent to Veg. 1; Veg. 3, vegetative cell adjacent to Veg. 2.
This figure is essentially the same as Figure 8 in the main text, except the addition of Veg. 2 and Veg. 3 data.
Supplemental Figure S6. Time dependence of fluorescence components in single-time experiments under 808 nm TPE
(See Materials and Methods). Average values are connected by solid lines. Error bars show SD. Maximum and minimum
values are connected by broken lines. Graphs are analogous to Figure 7, but different target cells were analyzed at each
time. Five glass-bottomed dishes were prepared at t = 0 h. Filaments in one glass-bottomed dish were observed only once.
Ten filaments were investigated at each time point. Het., heterocyst; Veg. 1, vegetative cell adjacent to heterocyst; Veg. 2,
vegetative cell adjacent to Veg. 1.
Supplemental Figure S7. Time dependence of fluorescence components in single-time experiments under 785 nm OPE
(See Materials and Methods). Solid lines connect average values (±SD). Broken lines show maximum and minimum
values. Data are shown as in Figure 8, but different target cells were analyzed at each time. Five glass-bottomed dishes
were prepared at t = 0 h. Filaments in one glass bottom dish were observed only once. Ten filaments were investigated at
each time point. Het., heterocyst; Veg. 1, vegetative cell adjacent to heterocyst; Veg. 2, vegetative cell adjacent to Veg. 1.
Supplemental Figure S8. Cell position dependence of relative spectral amplitudes of fluorescence components under
808 nm TPE in cells grown diazotrophically for longer than 10 d. Average amplitudes of 21 filaments are shown by solid
lines (±SD). All average values were normalized to that of APC in the vegetative cell adjacent to heterocyst in the same
filament. Broken lines show maximum and minimum values. H, heterocyst; V1, vegetative cell adjacent to H; V2, cell
adjacent to V1; V3, cell adjacent to V2; V4, cell adjacent to V3.
Supplemental Figure S9. Cell position dependence of relative spectral amplitudes of fluorescence components under
785 nm OPE in cells grown diazotrophically for longer than 10 d. Solid lines show average amplitudes of 15 filaments (±
SD). All average values were normalized to that of APC in the vegetative cell adjacent to heterocyst in the same filament.
Broken lines show maximum and minimum values. H, heterocyst; V1, vegetative cell adjacent to H; V2, cell adjacent to
V1; V3, cell adjacent to V2; V4, cell adjacent to V3.
Supplemental Figure S10. Polar distribution of PSI fluorescence in terminal heterocyst. (A) Bright field image using a
conventional illumination spectrum without a narrow bandpath filter. (B) PSI-rich fluorescence (700–753 nm) image
obtained under 785 nm OPE. (C) Intensity profile calculated from image in panel B along the dotted line in panel A. PSI
showed a polar distribution in the terminal heterocyst, as characterized by its narrower peak in C compared to vegetative
cells. Numbered arrowheads in panels A and C (1–6) show corresponding positions between cells.
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