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Biochemical composition and fatty acid content of filamentous nitrogen-fixing

cyanobacteria

Article  in  Journal of Phycology · September 2002

DOI: 10.1046/j.1529-8817.1998.340812.x

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J. Phycol. 34, 812–817 (1998)

BIOCHEMICAL COMPOSITION AND FATTY ACID CONTENT OF FILAMENTOUS

NITROGEN-FIXING CYANOBACTERIA1

M. A.Vargas,2 H. Rodrı́guez, J. Moreno, H. Olivares, J. A. Del Campo, J. Rivas, and M. G. Guerrero

Instituto de Bioquı́mica Vegetal y Fotosı́ntesis, Universidad de Sevilla y Consejo Superior de Investigaciones Cientı́ficas, Centro de
Investigaciones Cientı́ficas Isla de la Cartuja, Americo Vespuccio, s/n, E- 41092 Sevilla, Spain

ABSTRACT (EPA). Essential fatty acids are precursors of pros-

The biochemical composition and fatty acid content of taglandins and, as such, are becoming increasingly
twelve strains of filamentous, heterocystous, nitrogen-fixing important in the pharmaceutical industry (Borowitz-
cyanobacteria have been determined. When grown under ka 1988, Becker 1994). Except for linoleic acid and
diazotrophic conditions, protein, carbohydrate, lipid, and ALA, these compounds are usually rare in plants
nucleic acids comprised 37–52%, 16–38%, 8–13%, and and animals but are present in relatively large
8–11% of the dry weight, respectively. The presence of a amounts in some species of algae and fish (Rich-
combined nitrogen source resulted in an increase in the mond 1990, Becker 1994, Caughey et al. 1996). An
protein content of the cells and a decrease in the levels of essential fatty acid that merits special attention is
lipids and carbohydrates, although biomass productivity GLA, which is becoming recognized as a promising
was not affected significantly. Biochemical composition therapeutic agent for numerous health disorders.
also changed during culture growth, with the highest levels Clinical studies demonstrate that dietary GLA has a
of proteins and lipids occurring as the culture entered sta- beneficial effect on heart disease, Parkinson disease,
tionary phase, whereas the highest levels of carbohydrate multiple sclerosis, inflammatory diseases, premen-
and nucleic acids were found during the exponential strual syndrome, plasma cholesterol levels, and oth-
phase. Total fatty acid levels in the strains assayed ranged er disorders (Borowitzka 1988, Callegari 1989, Hen-
between 3 and 5.7% of the dry weight. With regard to rikson 1989, Richmond 1990, Rodrı́guez and Guer-
fatty acid composition, all strains showed high levels of rero 1992). Because GLA is very rare (the few known
polyunsaturated fatty acids (PUFAs) and saturated fatty sources include human milk, oil extracts of the eve-
acids (SAFAs), with values of 24–45% and 31–52% of ning primrose plant, black currant, borage seeds,
total fatty acids, respectively, whereas the levels of monoun- and some fungi), alternative sources for this fatty
saturated fatty acids (MUFAs) were in general lower (11– acid are being sought. The cyanobacterium Spiruli-
32%). Palmitic acid (16:0) was the most prevalent SAFA, na, used extensively as a health food, is a concen-
whereas palmitoleic (16:1n- 7) and oleic acid (18:1n-9) trated natural source of GLA, which constitutes ap-
were the most abundant MUFAs in all the strains. Among proximately 1% of its dry weight (Cohen et al. 1987,
PUFAs, g-linolenic acid (GLA, 18:3n-6) was present at Richmond 1988, Cohen et al. 1992, 1993a, b, Cerdá-
high levels (18% of total fatty acids) in Nostoc sp. (Chile) Olmedo and Avalos 1994).
and at lower levels (3.6% of total fatty acids) in Ana- Most reports on fatty acids in cyanobacteria indi-
baenopsis sp. The presence of GLA has not been previ- cate an acyl chain length of 18 or fewer carbon at-
ously reported in these genera of cyanobacteria. The rest of oms, with 16:0, 16:1, 18:2, and ALA present as the
the strains exhibited high levels (12–35% of total fatty major fatty acids. Based on their fatty acid compo-
acids) of a-linolenic acid (ALA, 18:3n-3). Linoleic acid sition, cyanobacteria have been classified into four
(18:2n-6) was also present at a substantial level in most groups. Strains in the first group contain only satu-
of the strains. Eicosapentaenoic acid (EPA, 20:5n-3) was rated fatty acids (SAFAs) and monounsaturated fatty
also detected in Nostoc sp. (Albufera). Some filamentous acids (MUFAs), whereas strains in the other groups
nitrogen-fixing cyanobacteria therefore represent potential contain polyunsaturated fatty acids (PUFAs) in ad-
sources of commercially interesting fatty acids. dition to SAFAs and MUFAs. The second group is
characterized by the presence of ALA, the third
Key index words: biochemical composition, blue-green al- group by GLA, and the fourth group by 18:4. There-
gae, fatty acids, g-linolenic acid, nitrogen-fixing cyanobac- fore, cyanobacteria are quite variable in their fatty
teria acid composition, with marked differences occur-
ring even within the same genus (Kenyon 1972,
Microalgae represent a valuable source of a wide Kenyon et al. 1972, Wood 1974, Materassi et al.
spectrum of lipids with different potential applica- 1980, Murata and Nishida 1987, Alvarez-Cobelas and
tions. Especially interesting are the polyunsaturated Zarco-Lechado 1989, Ahlgren et al. 1992, Murata et
fatty acids, including the essential fatty acids linoleic al. 1992).
acid, a-linolenic acid (ALA), g-linolenic acid (GLA), Among the different groups of cyanobacteria, the
arachidonic acid (AA), and eicosapentaenoic acid filamentous nitrogen-fixing species are particularly
attractive for the production of biomass and chem-
1 Received 2 October 1997. Accepted 4 June 1998. icals, since they are able to synthesize all of their cell
2 Author for reprint requests; Fax 134-954460065. using solar energy, water, air, and a few mineral
812
 FATTY ACID IN CYANOBACTERIA 813

salts. This group of cyanobacteria is especially rele- nations, aliquots of the cell culture were centrifuged at 2500 3 g
vant, since they can perform effective N2 fixation for 10 min, and the pellet was washed twice with distilled water,
resuspended in ethanol, and maintained at 08–48 C for 1 h. The
under aerobic conditions. Nitrogen fertilizer is not ethanolic suspension was centrifuged as before, and the super-
required as a component of the growth medium for natant was used for lipid determination according to the test for
these organisms, since they can use atmospheric ni- total lipids of Boehringer- Mannheim. For RNA and DNA deter-
trogen as the sole nitrogen source. In addition, the minations, the lipid-free pellet was subjected to the orcinol meth-
od (Lin and Schjeide 1969), and the diphenylamine method
filamentous nature of these microalgae confers an (Burton 1968), respectively. Chlorophyll a was determined follow-
advantage for harvesting the cells. The lack of fixed ing the method of Mackinney (1941). For dry weight determi-
nitrogen in the growth medium has positive eco- nations, 100–200 mL aliquots of the cell culture were filtered
nomic implications and restricts the problem of con- through Whatman GF/C paper, washed twice, and the filters con-
tamination by other microorganisms (Rodrı́guez taining the algae were dried at 808 C for 24 h. For ash determi-
nations, about 10-mg (dry weight) samples of biomass were main-
and Guerrero 1992). Despite these clear advantages tained at 4008 C for 6 h in a muffle furnace.
and their potential significance to biotechnology, For fatty acid analysis, freeze-dried samples of biomass (10 mg)
there has been very little applied research carried were treated with 1 ml of methanol-acetyl chloride (20:1) accord-
out with filamentous nitrogen-fixing cyanobacteria ing to Lepage and Roy (1984). Nonadecanoic acid was added as
an internal standard, and the mixture was heated to 1008 C for 1
(Regan 1988). h. The fatty acid methyl esters were analyzed by gas chromatog-
This paper describes the biochemical composi- raphy using a flame ionization detector. A Supelco SP-2330 fused
tion and fatty acid content of twelve strains of fila- silica capillary column (30 m 5 0.25 mm ID, 0.2 mm film thick-
mentous, heterocystous, nitrogen-fixing cyanobac- ness) was used. The oven temperature was 1508 C for 8 min,
teria, most of which were recently isolated by our followed by an increase of 38 C·min21 until 1908 C, then held at
1908 C for 23 min (injector and detector temperatures were 2208
group from natural environments. Several of these and 2508 C, respectively; split ratio, 100:1; flow rate of N2 carrier,
strains have been successfully grown outdoors, with 0.8 ml·min21). Fatty acid methyl esters were analyzed and quan-
high biomass productivities (Rodrı́guez et al. 1989, tified by cochromatography with standards (Sigma Chemical Co.,
1992, Moreno et al. 1995). St. Louis, Missouri). Identities of the fatty acid methyl esters were
determined by means of gas chromatography–mass spectrometry
MATERIALS AND METHODS (GC-MS) analysis, using a Hewlett-Packard 5890 Series II gas chro-
matograph interfaced, via an open coupling system, to an MAT
Anabaena sp. ATCC 33047 and Anabaena variabilis ATCC 29413 95 high- resolution mass spectrometer. The spectra were record-
were obtained from the American Type Culture Collection, Rock- ed at an ionization voltage of 70 eV and an ion source tempera-
ville, Maryland, and Nostoc commune came from the Culture Col- ture of 2008 C. The transfer line was held at 2508 C. Identification
lection of Göttingen University, Germany. The remaining strains of methyl esters was based on comparison with standards analyzed
were isolated and classified by our group. Nostoc paludosum, Nostoc under identical GC-MS conditions. The unknown mass spectra
sp. (Albufera), and Anabaenopsis sp. were isolated from the coastal were matched by computer with the reference mass spectra of
lagoon Albufera de Valencia, Spain. Nodularia sp. (Chucula), Nos- the NIST Data Base installed on a Finnigen Mat Data Station.
toc sp. (Chucula), and Nostoc sp. (Chile) were isolated from lakes The double bond positions of fatty acids were confirmed through
in the Andes Mountains in Chile. Nostoc sp. (Caquena) and Nostoc the formation of their 2-substituted 4,4-dimethyloxazolines
sp. (Llaita) were isolated from the Caquena River and Parinacota (DMOX) derivatives, as described by Yu et al. (1989).
sector, respectively, in Lauca National Park, Chile. Nostoc sp.
(Loa) was isolated from the Loa River in Chile. Nostoc paludosum, RESULTS AND DISCUSSION
Nostoc sp. (Albufera), Anabaenopsis sp., Nostoc sp. (Chile), Nostoc
sp. (Chucula), and Nostoc sp. (Loa) have been deposited in the The biochemical compositions of several strains
Pasteur Culture Collection, Paris, France, and designed as PCC of nitrogen-fixing cyanobacteria are shown in Table
9206, PCC 9202, PCC 9215, PCC 9205, PCC 9201, PCC 9203, and
PCC 9204, respectively. 1. The protein content ranged between 37% and
Anabaena sp. ATCC 33047 was grown on the medium described 52% of the dry weight and was above 40% for most
by Moreno et al. (1995). For the other strains, the culture me- strains. The high protein levels correlated with a
dium of Arnon et al. (1974) was used, with the modifications high nitrogen content (i.e. 8%–13% of the dry
described by Moreno et al. (1995). For Nostoc sp. (Caquena) and
Nostoc sp. (Llaita) the medium was supplemented with 30 mM
weight); C/N ratios were 4 to 5 (data not shown).
NaHCO3. The medium was further modified to contain 1 mM Carbohydrate content was about half that of protein
K2HPO4 for Nostoc sp. (Caquena) and 4 mM K2HPO4 for Nostoc for most of the strains. Total lipids ranged from 8%
sp. (Loa). When a combined nitrogen source was utilized, the to 13% of the dry weight, with Nodularia sp. (Chu-
medium was supplemented with either 20 mM KNO3 or 5 mM cula) and Nostoc sp. (Llaita) having the highest val-
NH4Cl. The ammonium concentration was kept at a constant lev-
el by adding an amount equivalent to that consumed by the cells ues. Nucleic acids represented about 10% of dry
once a day. weight in all the strains and ash accounted for 5.5%
Cells were grown photoautotrophically at 308–358 C in 5-cm to 11.2%.
deep 1-L capacity Roux flasks, laterally illuminated at the indicat- The biochemical compositions of these cyanobac-
ed surface irradiances, either in semicontinuous cultures subject- teria are similar to those reported for several strains
ed to a 12:12 h LD cycle or in batch cultures with continuous
illumination. Cultures were bubbled with air (50–100 L·[L cul- of Spirulina, which is considered to have high nutri-
ture]21·h21) supplemented with 0.4–1% (v/v) CO2. Semicontin- tional value (Becker and Venkataraman 1982, Cifer-
uous cultures were diluted with fresh medium once a day to a ri 1983, Henrikson 1989). In fact, several of our iso-
cell density of 0.6 g (dry weight)·L21. lates (Nostoc sp. [Chile], Nostoc sp. [Chucula], No-
Protein was estimated by the Bradford method (Bradford 1976)
using bovine serum albumin as a standard. Carbohydrate was an- dularia sp. [Chucula], and Nostoc sp. [Llaita]) are
alyzed by the phenol-sulfuric acid method (Dubois et al. 1956) used as food by locals in the Andes Mountains in
with glucose as a standard. For lipid and nucleic acid determi- Chile. The cyanobacteria studied in this work have,
814 M. ANGELES VARGAS ET AL.

TABLE 1. Biochemical composition of several nitrogen-fixing cyanobacteria grown in semicontinuous culture at 180 mmol photon·m22·s21 (fluorescent
lamps). Each value is a mean 6 SD; n is shown in parentheses. n.d. 5 not determined.
Content (% dry weight)
Strain Protein Carbohydrate Lipids RNA DNA Ash

Anabaena sp. ATCC 33047 45.0 6 1.8 (4) 28.0 6 2.0 (4) 10.0 6 0.9 (4) 8.8 6 0.4 (4) 0.5 6 0.02 (4) 7.1 6 0.5 (4)
Anabaena variabilis 47.2 6 1.1 (4) 22.3 6 2.5 (4) 10.5 6 1.1 (4) 8.2 6 1.0 (4) 2.2 6 0.07 (4) 4.2 6 0.3 (4)
Anabaenopsis sp. 52.2 6 2.5 (4) 16.3 6 1.5 (3) 11.4 6 0.6 (4) 8.9 6 0.2 (4) 1.1 6 0.05 (4) 6.5 6 0.2 (3)
Nodularia sp. (Chucula) 42.9 6 2.5 (4) 16.9 6 2.6 (4) 12.6 6 1.5 (4) 9.1 6 0.4 (4) 1.3 6 0.01 (4) 7.3 6 0.1 (3)
Nostoc commune 39.9 6 1.0 (3) 37.6 6 2.5 (3) 8.4 6 0.4 (4) 8.2 6 0.8 (4) 0.4 6 0.01 (4) 6.7 6 0.5 (3)
Nostoc paludosum 40.4 6 4.5 (3) 26.6 6 1.9 (4) 10.4 6 1.0 (4) 8.4 6 0.5 (4) 0.5 6 0.03 (4) 5.5 6 0.1 (3)
Nostoc sp. (Albufera) 47.0 6 3.5 (6) 26.8 6 4.0 (6) 7.9 6 1.2 (4) 8.4 6 0.1 (3) 0.6 6 0.10 (6) 9.1 6 0.6 (3)
Nostoc sp. (Caquena) 44.9 6 3.1 (9) 23.3 6 1.7 (9) 11.1 6 1.0 (9) 5.6 6 0.1 (9) 1.3 6 0.10 (9) n.d.
Nostoc sp. (Chile) 47.3 6 3.9 (4) 23.3 6 2.0 (4) 10.4 6 2.5 (4) 7.5 6 0.4 (4) 0.9 6 0.01 (4) 5.4 6 0.1 (3)
Nostoc sp. (Chucula) 37.3 6 0.5 (3) 15.7 6 1.8 (4) 8.4 6 0.3 (4) 9.6 6 0.6 (4) 1.0 6 0.04 (4) 11.2 6 0.6 (3)
Nostoc sp. (Llaita) 47.7 6 3.0 (9) 20.2 6 1.5 (9) 12.1 6 0.1 (9) 7.2 6 0.1 (9) 0.6 6 0.10 (9) n.d.
Nostoc sp. (Loa) 37.5 6 0.4 (4) 32.1 6 1.2 (3) 8.5 6 0.5 (3) 7.3 6 0.1 (3) 0.8 6 0.02 (3) n.d.

moreover, the substantial advantage of being nitro- growth of batch cultures. As shown in Table 3, the
gen-fixing organisms. In fact, as shown in Table 2, net protein, total lipid, nucleic acid, and chlorophyll
specific growth rate and biomass productivity of Nos- contents of Nostoc paludosum doubled from lag to
toc paludosum were similar when air was the sole ni- transition phase, whereas carbohydrate content de-
trogen source and when in the presence of a com- creased by about 50%. A similar pattern was ob-
bined nitrogen source, NO32 or NH41. Although served for the rest of the strains (data not shown).
combined nitrogen did not enhance the biomass Cell density indirectly affects the amount of light
productivity of the nitrogen-fixing cyanobacterium available to each cell in the suspension, thus signif-
Nostoc paludosum, it influenced significantly the bio- icantly affecting the pigment (chlorophyll and phy-
chemical composition of the cells. The protein con- cobiliproteins) content of cyanobacterial cells (Rod-
tent of the cells grown with air as the sole nitrogen rı́guez et al. 1991). Therefore, the observed increase
source was lower than that of cells grown with a in protein content during culture growth is probably
combined nitrogen source. Conversely, lipid and due to an increase in phycobiliproteins, which rep-
carbohydrate contents were higher in cells grown in resent about 50% of the total cell protein. These
air than in cells grown in the presence of NO32 or observations are in agreement with other reports
NH41. The highest RNA content was obtained in (Richmond 1986).
cells grown with NH41, whereas DNA content was Green algae seem to have a higher capacity than
about the same in all cultures. Similar effects of ni- cyanobacteria to modify their lipid content in re-
trogen source on growth and biochemical compo- sponse to different factors, such as the nitrogen con-
sition were observed for the rest of the strains (data centration in the culture medium and the growth
not shown). In accordance with these results, it has phase (Materassi et al. 1980, Piorreck and Pohl
been reported that the protein content in Nostoc 1984, Piorreck et al. 1984). Nevertheless, according
muscorum is higher with NO32 than with air as the to our results with Nostoc paludosum, the lipid con-
sole nitrogen source (Bagchi et al. 1985). This be- tent of the cells doubled from lag to transition phase
havior is in agreement with the logic of cell econo- (Table 3) and increased by about 70% in response
my, since the energy requirement for the assimila- to the absence of a combined nitrogen source (Ta-
tion of the different nitrogenous substrates increases ble 2). Irradiance and dissolved oxygen concentra-
in the order NH41, NO32, N2 (Guerrero and Lara tion in the culture also affected lipid levels in the
1987). cyanobacteria examined in this study. For example,
Biochemical composition also changed during the lipid content of Anabaena sp. ATCC 33047 in-

TABLE 2. Effect of the nitrogen source on specific growth rate, biomass productivity, and biochemical composition of Nostoc paludosum grown in
semicontinuous culture in the absence or presence of a combined nitrogen source at 1380 mmol photon·m22·s21 (metallic halide lamps). Each value is a
mean 6 SD; n is shown in parentheses.

Air Air, KNO3 Air, NH4Cl

Specific growth rate (d21) 0.69 6 0.11 (4) 0.76 6 0.05 (4) 0.74 6 0.08 (4)
Biomass productivity (g dry weight·m22·d21) 22.5 6 1.9 (4) 23.4 6 2.0 (4) 24.8 6 0.2 (4)
Component (% dry weight)
Protein 43.1 6 2.5 (5) 53.6 6 0.8 (3) 55.5 6 2.0 (3)
Carbohydrate 27.1 6 2.0 (4) 22.5 6 2.2 (3) 16.9 6 1.3 (3)
Lipid 8.5 6 0.4 (4) 6.0 6 0.7 (3) 4.9 6 0.7 (3)
RNA 9.4 6 0.7 (4) 9.2 6 0.9 (3) 11.7 6 0.8 (3)
DNA 0.4 6 0.04 (4) 0.5 6 0.04 (3) 0.5 6 0.04 (3)
 FATTY ACID IN CYANOBACTERIA 815

TABLE 3. Biochemical composition of Nostoc paludosum at different tal fatty acids. The levels of cis-vaccenic acid (18:1n-
growth phases in a batch culture at 1380 mmol photon·m22·s21 (metallic 7) were very low in all cases.
halide lamps). Each value is a mean 6 SD, n 5 4.
With regard to linolenic acid, the strains assayed
Content (% dry weight) contained either ALA (18:3n-3) or GLA (18:3n-6),
Lag Exponential Transition except for Anabaenopsis sp., which contained both of
Component phase phase phase these fatty acids. Nostoc sp. (Chile) had a high level
Protein 23.0 6 1.7 48.0 6 2.0 52.6 6 3.2 of GLA (18% of total fatty acids; 1.1% of ash-free
Carbohydrate 36.5 6 1.5 26.5 6 0.5 20.3 6 1.6 dry weight), which is similar to that reported for
Lipid 4.9 6 0.3 6.4 6 0.2 10.2 6 0.3 Spirulina (Cohen et al. 1987, 1992, 1993a, b). The
Nucleic acids remaining strains contained high levels of ALA
RNA 5.8 6 0.2 9.0 6 0.3 10.8 6 0.6
DNA 0.5 6 0.01 0.5 6 0.01 0.6 6 0.02 (12%–35% of total fatty acids). High levels of ALA
Chlorophyll 0.6 6 0.04 0.9 6 0.03 1.4 6 0.05 have also been reported in cyanobacteria belonging
to the genera Nostoc and Anabaena. Conversely, to
our knowledge, GLA has not been reported previ-
ously in Nostoc or Anabaenopsis and seems to be un-
creased by about 50% in response to an increase in common among nitrogen-fixing strains (Kenyon et
oxygen tension that was obtained by replacing air al. 1972, Wood 1974, Zepke et al. 1978, Murata and
(21% O2) with 75% O2 and doubled when irradi- Nishida 1987, Alvarez-Cobelas and Zarco- Lechado
ance was increased from 180 to 3000 mmol pho- 1989, Ahlgren et al. 1992, Murata et al. 1992).
ton·m22·s21 (data not shown). Linoleic acid (18:2n-6) was also present at high
The total fatty acid content in the strains assayed levels in all strains (15%– 23% of total fatty acids),
ranged between 3% and 5.7% of the dry weight except for Nostoc sp. (Albufera), Anabaena sp. ATCC
(data not shown). The fatty acid compositions of sev- 33047, and Anabaena variabilis; however, the two lat-
eral nitrogen-fixing cyanobacteria are summarized ter strains had the highest ALA content.
in Table 4. All strains had a high content of PUFAs, With respect to other interesting PUFAs,
with values of 24%–45% of the total fatty acids. 6,9,12,15-octadecatetraenoic acid (18:4n-3) was only
These data are in agreement with other reports in present in Anabaenopsis sp. and Nostoc sp. (Chile),
the literature indicating that cyanobacteria, especial- whereas 8,11,14-octadecatrienoic acid (18:3n-4) was
ly the filamentous strains, have a high content of only found in Nostoc sp. (Albufera), which also con-
PUFAs (Borowitzka 1988, Becker 1994). The levels tained a high level (19%) of 8,11,14,17-octadecate-
of SAFAs and MUFAs ranged from 31% to 52% and traenoic acid (18:4n-1). EPA (20:5n-3), which has
from 11% to 32% of total fatty acids, respectively, in recognized commercial value, was only found in Nos-
all the strains, except in Nostoc sp. (Albufera) and toc sp. (Albufera) at 1.4% of total fatty acids. It has
two other strains of Nostoc (Caquena and Loa), been reported only recently that cyanobacteria can
which exhibited a lower (6%) and a higher (35%– synthesize fatty acid chains longer than 18 carbon
40%) content of MUFAs, respectively. In all strains, atoms. However, this capability does not seem to be
palmitic acid (16:0) was the most abundant fatty a general feature of cyanobacteria, and when these
long-chain fatty acids are present, their levels are low
acid. Palmitoleic acid (16:1n-7) and oleic acid (18: (Alvarez-Cobelas and Zarco-Lechado 1989, Ahlgren
1n-9) were the most abundant MUFAs in all the et al. 1992)
strains, with Nostoc paludosum, Nostoc sp. (Caquena),
Nostoc sp. (Chucula), Nostoc sp. (Llaita), and Nostoc CONCLUSIONS
sp. (Loa) exhibiting the highest levels: 18%–22% From our data, it can be concluded that some
(palmitoleic acid) and 10%–18% (oleic acid) of to- filamentous nitrogen-fixing cyanobacteria represent

TABLE 4. Fatty acid composition of several nitrogen-fixing cyanobacteria in the late exponential phase of batch cultures grown at 180 mmol pho-
ton·m22·m21 (fluorescent lamps). Each value is a mean of three independent measurements, SD , 10%. — 5 not detected.

Fatty acid content (% total) Fatty acid

18:3n-3 18:3n-6 20:5n-3
Strain 14:0 16:0 16:1n-7 16:2n-4 16:4n-1 18:0 18:1n-7 18:1n-9 18:2n-6 (ALA) 18:3n-4 (GLA) 18:4n-1 18:4n-3 (EPA)

Anabaena sp. ATCC 33047 0.4 42.3 7.8 0.3 3.7 0.9 0.9 2.6 5.7 35.3 — — — — —
Anabaena variabilis 0.4 37.4 15.8 0.2 — — 0.9 4.3 8.6 32.3 — — — — —
Anabaenopsis sp. 0.3 45.5 3.7 0.3 — 0.9 — 8.2 16.2 16.8 — 3.6 — 4.6 —
Nodularia sp. (Chucula) 0.3 42.8 9.5 0.4 — 1.1 0.6 4.2 22.8 18.5 — — — — —
Nostoc commune 0.3 39.5 10.3 0.4 0.4 1.4 1.1 5.2 17.6 24.0 — — — — —
Nostoc paludosum 0.4 35.4 18.0 0.2 0.2 1.0 1.3 11.9 19.1 12.4 — — — — —
Nostoc sp. (Albufera) 0.3 50.8 3.3 0.3 0.1 0.7 0.2 2.6 6.5 11.6 3.2 — 19.0 — 1.4
Nostoc sp. (Caquena) 0.4 34.2 20.9 0.3 — 1.4 1.7 17.9 23.2 — — — — — —
Nostoc sp. (Chile) 0.3 43.1 8.8 0.2 — 0.9 0.8 9.6 15.7 0.5 — 18.0 0.3 1.9 —
Nostoc sp. (Chucula) 0.3 30.9 19.5 0.3 0.3 1.0 2.5 10.0 19.3 15.8 — — — — —
Nostoc sp. (Llaita) 0.5 30.7 20.2 0.4 0.2 1.2 1.9 9.5 15.9 19.5 — — — — —
Nostoc sp. (Loa) 0.4 30.1 21.9 0.4 1.3 1.0 1.6 11.5 15.5 16.4 — — — — —
816 M. ANGELES VARGAS ET AL.

a source of essential fatty acids that are of commer- Cohen, Z., Vonshak, A. & Richmond, A. 1987. Fatty acid and com-
cial interest, including linoleic, and a- and g-linolen- position of Spirulina strains grown under various environ-
mental conditions. Phytochemistry 26:2255–8.
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