Plant Product Research Journal (2009), Volume 13: 8 – 14.
ECOLOGICAL IMPLICATIONS AND ROLES OF CYANOBACTERIA
(CYANOPHYTA) IN FOOD SECURITY – A REVIEW
Nweze, N. O.
Department of Botany, University of Nigeria, Nsukka, Enugu State, Nigeria.
Email: [email protected] Phone: +234 8064664556
.
ABSTRACT
Cyanobacteria (Cyanophyta), commonly called blue green algae, are prokaryotes that inhabit a wide
variety of habitats as free living, epiphytic, symbiotic or parasitic plants. They form a component of the
base of the aquatic food chain, and their photosynthetic activity aerates the habitat. Hence, they are of
great importance in aquaculture. Spirulina and Nostoc commune are sources of single cell proteins,
edible to man. Nitrogen fixing forms (Anabaena, Nostoc, etc) increase the nitrogen content of the habitat
and supply nitrates in symbiotic relationships where they enhance the nutritive quality of the host plant,
which could be used as green manure, fodder, and fish feed. Some act as bio-fertilizers, a fact that can
be utilized effectively in improving plant nutrition, especially in rice and wheat production. As producers
of growth hormones, they improve yield of rice (e.g. Phormidium tenue). Consequently they are essential
in rice based economies. Some are capable of producing antibiotics (Microcystis, Nostoc and
Scytonema). Cyanobacteria prevent soil erosion; help in soil water retention, sodium removal and act as
the first colonizers in land reclamation. Blooms of some species release toxins and lead to anoxia in the
habitat to the detriment of biota. Phormidium is known to reduce the quality of brine. Some of these
Cyanobacteria have been observed in Nigerian environment. There is therefore the need to harness them
or combat the obnoxious forms. Control of blooms is expensive hence the need for research into their
biological control.
Keywords: Blue-green algae, Single–cell proteins, Bio-fertilizers, Growth hormones, Algal blooms, toxins
INTRODUCTION
more than 3.5 billion years ago) when there was the
absence of free oxygen (18, 41).
Also, they are capable of taking up
ammonia through passive diffusion or as
ammonium ion by specific uptake system and fixing
atmospheric nitrogen (N2), using nitrogenase
enzyme to reduce molecular nitrogen to ammonia in
the presence of hydrogen (21,41). Consequently,
unlike most plants they are not limited by nitrogen.
These qualities have been employed extensively in
Asia to enhance agricultural production. Some
examples of blue-green algae are presented in
Plate 1 (10).
Cyanobacteria, commonly called blue–green algae
(BGA), are found worldwide in diverse habitats.
Taxonomically they are classified as Cyanophyta
but recently as Cyanobacteria (18, 41, 44). They
are found in freshwater (lakes, ponds, reservoirs,
rivers, streams, marshlands etc), terrestrial (soil,
walls, tree barks, rocks, stones and plant pots)
brackish, and marine habitats (41). Occasionally,
they may form blooms, e.g. Microcystis,
Trichodesmium erythraeum Ehrenberg (which gives
the Red Sea its colour), Anabaena, Spirulina,
Anabaenopsis, and others (18). Anabaena and
Nostoc form symbionts with bryophyte such as
Anthoceros,
pteridophyte
such
as
Azolla
(gymnosperm such as Cycas, angiosperm such as
Trifolium alexandrium L. (an important forage
legume), and fungi to form lichen. Anabaenolium is
an intestinal parasite of man and some animals.
Although BGA are photosynthetic, many
are facultative phototrophic anaerobes. Many
Cyanophyceae (e.g. Oscillatoria limnetica Lemm.)
are capable of photosynthesizing under both
aerobic and anaerobic conditions, unlike the
eukaryotic algae that can only photosynthesize
under aerobic conditions (photoaerobic). BGA are
therefore important in their habitat. Under anaerobic
conditions, in the presence of sulphur, the
photoautotrophic blue green algae derive electrons
by reduction of sulphur. Dissolved carbon dioxide
reacts with hydrogen sulphide in the presence of
light and chlorophyll to produce sugar, water and
sulphur. For this reason, sulphur rich ecosystems
contain high numbers of Cyanophyceae. This
phenomenon must have favoured the presence of
Cyanophyceae during the Precambrian era (2 to
MATERIALS AND METHODS
An in-depth literature search was made from the
Internet and serial materials of Nnamdi Azikiwe Elibrary, University of Nigeria, Nsukka. Various
journal articles, proceedings of learned societies of
Botany and Phycology, and Food and Agricultural
Organization documents and textbooks were
consulted with regards to the ecological implications
and roles of cyanobacteria in food security. The
data collected were presented in figure and tables.
RESULTS AND DISCUSSION
Ecological Roles
Aeration of habitat: Irrespective of their colour, all
algae have chlorophyll a, and by their
photosynthetic action they take up carbon dioxide
and aerate their habitat. The blue green algae thus
participate actively in aeration of fish ponds. Fish
piping (gulping air at the surface) may be observed
when dissolved oxygen falls below 2 mg/L (14).
8
Nweze
Oscillatoria princeps
9
Anabaena flos-aquae
Phormidium uncinatum Cylindrospermum muscicola
Anabaena azollae
Trichodesmium sp.
Fig. 1: Photomicrograph of some species of Cyanobacteria. http://wwwcyanosite.bio.purdue.edu/index.html.
Antibiotics: Nostoc is known to secrete an
antibiotic known as bacteriocin that can kill related
strains of alga. Bacteriocin is a proteinaceous
antibiotic that is active against prokaryotic strains
closely related to the organism that produces the
antibiotic. Scytonema hofmanni Agardh is known to
secrete cyanobacterin, a chlorine containing
gamma lactone (33). These antibiotics play a role in
inhibiting the growth of competing organisms (18).
Microcystis has been observed to inhibit the growth
of Staphylococcus (a bacterium) and Closterium (a
green alga).
Land reclamation: Blue green algae are useful in
land reclamation as the first colonizers of
marshlands. They hold soil and dust particles as
they dry up. Thus they are important in ecological
succession. Also, saline-alkali soils are generally
unsuitable for raising crops but blue green algae
have been shown to help in reclamation of such
soils. This is because of the preferential absorption
or adsorption of sodium by them. The growth of
these blue green algae in saline – alkaline habitats
reduces salinity by 25-30%, pH, electrical
conductivity and exchangeable sodium. They also
increase aggregation, hydraulic conductivity, soil
nitrogen and permeability. However, the mechanism
by which the blue green algae scavenge sodium is
not properly understood (15). Investigations on soil
indicators of land-use have shown that
Cyanobacteria such as Cylindrospermum sp.,
Calothrix spp., Pseudoanabaena sp., Scytonema
sp. and Thricomus sp. are highly sensitive to
disturbance (47) and as such, their absence
indicate highly disturbed soils. Pseudoanabaena
and Scytonema have been recorded in Nigeria (30).
Effect on soil properties: The ability of
Cyanobacteria (Scytonema, Oscillatoria) to bind
sand and soil particles helps prevent erosion. These
have been reported by many investigators in
Nigeria (6, 16, 30). Kaushik (17) observed that their
growth in soil seems to influence the physical and
chemical properties of the soil. Their growth
significantly increases the water-stable aggregates;
and the soil aggregation and arrangement influence
infiltration rate, aeration and soil temperature.
Consequently the physical environment of the crop
is improved (17). They consequently help to
maintain the moisture content of the soil by
reducing direct evaporation of water from open
lands (e.g. Oscillatoria). The effect of blue green
algal inoculation on water stable soil aggregates is
presented in Table 1 (35).
Blue green algal blooms: Blue-green algae
usually account for as much as 50 to 75 percent of
blooms in the summer time (2). Excessive growth of
some species (blooms), especially those of
Microcystis, leads to anoxia (lack of oxygen) in
water. The algae have a shading effect on the lower
layers, resulting in more respiratory activities below
the surface and suffocation of fauna (24). They also
lead to unpleasant odours in water produced by
substances such as geosmin, rendering it useless
for domestic use and recreation (24, 31, 41).
Ecological implications and role of Cyanobacteria in food security
10
Table 1: Effect of blue – green algal inoculation on water stable soil aggregates (35)
Soil
Sandy loam
Loam
Silty clay loam
Water-stable aggregates (50um)
Algae inoculated
4.1
6.0
9.1
Control
2.2
2.6
3.5
% Increase
85
130
160
Table 2: Chemical composition (% of dry matter) of selected algae (32)
Alga
Spirulina platensis
Spirulina maxima
Chlorella vulgaris
Chlorella pyrenoidosa
Scenedesmus obliquus
Scenedesmus quadricauda
Dunaliella salina
Synechococcus
Euglena gracilis
Hormidium
Ulothrix
Protein
46 – 50
60 – 71
51 – 58
57
50 – 56
47
57
63
39 – 61
41
45
Table 3: Amino-acid profile of selected algae (32)
Amino Acid
FAO
Egg
Std
1
Ile
4.0
6.6
6.8
Leu
7.0
8.8
10.9
Val
5.0
7.2
7.5
Lys
5.5
7.0
5.3
Phe
6.0
5.8
5.7
Tyr
4.2
5.9
Met
3.5
3.2
2.3
Cys
2.3
0.7
Try
1.0
1.7
1.5
Thr
4.0
5.0
5.6
Ala
9.0
Arg
6.2
7.2
Asp
11.0
12.2
Glu
12.6
17.4
Gly
4.2
6.6
His
2.4
2.0
Pro
4.2
4.1
Ser
6.9
4.9
2
6.7
9.8
7.1
4.8
5.3
5.3
2.5
0.9
0.3
6.2
9.5
7.3
11.8
10.3
5.7
2.2
4.2
5.1
Lipids
4–9
6–7
14 – 22
2
12 – 14
2
6
11
14 – 20
38
1
Carbohydrates
8 – 14
13 – 16
12 – 17
26
10 – 17
32
15
14 – 18
Alga (g/16g N)
3
4
3.6
4.5
7.3
9.3
6.0
7.9
5.6
5.9
4.8
4.2
3.2
1.7
1.5
0.6
0.6
0.7
0.3
5.1
4.9
9.0
12.2
7.1
5.8
8.4
8.8
10.7
10.5
7.1
10.4
2.1
1.7
3.9
5.0
3.8
5.2
5
3.2
9.5
7.0
6.4
5.5
2.8
1.3
5.3
9.4
6.9
9.3
13.7
6.3
2.0
5.0
5.8
6
4.2
11.0
5.8
7.0
5.8
3.7
2.3
1.2
0.7
5.4
7.3
7.3
10.4
12.7
5.5
1.8
3.3
4.6
Table 4: Effect of Cyanobacterial Biofertilizer inoculation on rice grain yield at a farmer’s field (21)
Name of Village
(Area)
Asoda Todran (7 ha)
Asoda Shivan (4 ha)
Jahoda (9ha)
Uninoculated
19.25
13.06
17.93
Grain yield (Quintals per hectare)
Inoculated
23.00
15.22
20.13
% Increase
18.48
15.81
12.26
Table 5: Avena growth test for bioassay of extracellular cyanobacterial auxins vis a vis known auxin
(IAA) (Average of 10 replications) (17)
IAA (mg/l)
0
0.001
0.01
0.1
1
Coleoptiles length (mm)
8.60
9.1
9.15
9.8
9.65
Increase over control (%)
0
5.81
6.39
13.95
12.21
9.25
9.05
9.0
7.56
5.23
4.65
10.0
Nostoc muscorum
Haplosiphon fontinalis
Moreover such waters are unsuitable for industrial
use as raw material and as coolant since they may
block filters. Other prominent bloom formers include
Trichodesmium found in the Caribbean Sea.
Trichodesmium has been reported in Ikogosi warm
springs (16). BGA are often associated with offflavor problems in fish because they produce
substances called geosmin (7, 24) and
methylisoborneal (MIB), which impart undesirable
flavors in fish (7).
Nweze
Some species of blue-green algae produce
toxins that affect farm animals, birds, fish and
humans negatively thereby reducing food
production. Symptoms such as skin irritation, eye
irritation, rashes, stomach cramps, vomiting,
nausea, diarrhea, asthma, fever, sore throat,
headache, muscle and joint pain, blisters of the
mouth and nose and liver damage have been
associated with them (44). For instance, Lyngbya
majuscula Gomont (fireweed) is responsible for
swimmers’ itch in Hawai, a disease characterised
by inflammation and swelling of the mucous
membranes of the eyes and nose, and pus on the
skin
(23).
The
toxin
implicated
is
debromaophysiatoxin which coincidentally has been
found to have anti-leukemic activity, and
suppresses other forms of cancer (25).
Also a wide range of unicellular and
filamentous genera are hepatotoxic (Microcystis,
Anabaena,
Nodularia,
Nostoc,
Oscillatoria,
Umezakia), neurotoxic (Aphanizomenon and
Oscillatoria), tetratoxic and carcinogenic (24, 27, 34,
44, 45). Microcystis is known to cause death of pets
and cattle that drink from infested ponds. It may
also lead to large-scale death of fish through
blocking of gills. Microcystis contains hepatipeptide
toxin known as microcystins (a polypeptide of ten
amino acids, lethal dose = 0.5 mg per kilogramme
of body weight). About 65 microcystins have been
isolated from cyanobacteria (8). Mazur and Plinski
(20) and Morris (24) noted that microcystins and
nodularin are produced as secondary metabolites
within cyanobacterial cell but are released in the
water column after lysis of the cell. Anabaena flosaquae (Lyngb.) Breb. contains a neurotoxin,
anatoxin A (low molecular weight nitrogen
containing compound, an alkaloid), B, C, and D.
Aphanizomenon flos-aquae (L.) Ralfs contains
saxitoxin and three related toxins. Saxitoxin is
responsible for paralytic shellfish poisoning in
humans (lethal dose = 10 microgramme per
kilogramme of body weight (18). Microcystis
aerugenosa Kutz. has been implicated in
rhinosporidiosis (polyp of the nasal cavity), and as
causative agent in diarrhoea, renal failure (during
dialysis)
and
gastroenteritis
(3,
44).
Cylindrospermopsis raciborski (Woloszynka) Subba
Raju may produce toxic alkaloids that cause
gastroenteritis symptoms or kidney disease in
humans (44). Bioaccumulation of these toxins has
been observed mostly in brackish and marine
foods, such as clams, oysters and predatory fish
(24).
Phormidium bloom is known to spoil salt
by imparting red colour and bad odour on brine. It
also gelatinizes brine resulting in inability of brine
solution to crystallize into salt (18).
Blooms control: The control of blooms is
expensive. Algicides such as copper sulphate (1,
24) at 9.2 mg/l may be used. This may become
problematic in waters rich in dissolved organic
matter because copper sulphate could complex with
organic matter to become ineffective against the
target organisms (18). Moreover, copper sulphate
may deteriorate water quality for consumption and
use since the toxins are released into the water as
the algal cells die (24). Biological control using
11
Cyanophages (blue-green algal viruses) are
effective except for Microcystis with thick
mucilaginous sheath that makes it impenetrable by
fungi and viruses (18). The use of ultrasound with
LG SONIC algae control equipment is a reliable
environmentally friendly method (19).
Cyanobacteria as biological control agents:
Israeli scientists (5) have successfully carried out
transgenic experiments with Anabaena and Bacillus
thuringiensis ssp. israelensis de Barjac (Bti), a biopesticide, in an attempt to biologically control
mosquitoes which otherwise are controlled by the
use of chemicals. The shortcoming of Bti’s short
half life is overcome by the transfer of lethal gene in
Bti into Anabaena which releases the toxin into the
water, thereby killing mosquitoes.
Roles in Food Security
Food for fauna: Non-toxic forms are sources of
food for many aquatic organisms such as
zooplankton (mini-crustaceans, protozoa, rotifers,
ostracods), frogs, fly larvae, water boatman, fish
etc., thereby forming the base of the aquatic food
chain /web. Examples are Oscillatoria, Anabaena
flos-aquae, and Spirulina. Spirulina is rich in amino
and fatty acids and vitamins (32, 41, 42). While
other groups of algae contain saturated and
monounsaturated
fatty
acids
abundantly,
Cyanophyta
contain
large
amounts
of
polyunsaturated lipids. Table 2 shows the chemical
composition (% of dry matter) of selected algae
(32).
In aquaculture, in the Philippines, a
filamentous blue-green alga, Lyngbya aestuarii
(Mert.) Leibmann is used in fish culture as feed for
fry (9). Phormidium valderianum BDU 30501 has
been successfully used as a complete aquaculture
feed source in India (41). Microcytis, though a
nuisance blue green when it forms blooms, has
been found to be more digestible than green algae
by Tilapia (9). Phang (32) observed that B carotene
in algae is a precursor of vitamin A, commercially
available as colour enhancer for fish and they are
good sources of nutrients having a high amino acid
profile (about eighteen). As noted by Becker (4),
they are the only vegetable protein that can replace
fish meal. Table 3 shows the amino acid profile of
selected algae (32).
Single cell proteins (SCP): BGA are sources of
single cell protein. Some species are delicacies in
human diet. Nostoc commune Vaucher and
Aphanothece sacrum (Suringar) Okada are
delicacies in Chile, Mexico, Peru, Philippines China
and Japan. Spirulina is eaten in Lake Chad region
of Africa (18). Spirulina is now sold as food
supplement by food supplement manufacturers. It
contains 60 – 70% protein, 20 % carbohydrate, 5 %
lipids, 7 % minerals and 6 % moisture. Moreover, it
is a rich source of beta-carotene, thiamine and
riboflavin and is one of the richest sources of
vitamin B12 (41).
Fixing of nitrogen to boost agricultural
production: Complex interacting factors such as
Ecological implications and role of Cyanobacteria in food security
low soil fertility, conditions favouring a wide range of
pests, prevalence of low performance crop/animal
varieties, economic restrains and cultural factors
severely constrain agricultural outputs in the tropics
(13). Biological systems that contribute to improved
yield are essential in the economy of this zone.
Some Cyanobacteria, especially those with
heterocysts, are involved in nitrogen fixation. For
instance Anabaena, Nostoc, Cylindrospermum,
Gloeocapsa, Rivularia and some members of
Scytonemataceae and Rivulariaceae etc., fix
atmospheric nitrogen into their bodies. Some
species of Oscillatoria (O. princeps Vaucher),
Trichodesmium and Gloeocapsa, though without
heterocysts have also been observed to fix
atmospheric nitrogen (18, 41).
Nilsson et al., (28) and Nanjappan et al.,
(26) noted that some species are biofertilizers and
have plant growth promoting abilities. Diazotrophic
heterocystous cyanobacteria are known to possess
the ability to form associations with vascular/nonvascular plants such as rice and form the
rhizosphere of wheat thereby producing growthpromoting substances. Algalization of rice crop has
been found to solubilize insoluble phosphate and
supplement nitrogenous fertilizers to the extent of
30-40 kg N/ha/season (15, 37, 40).
BGA fix nitrogen into inundated fields for
growing rice (paddy fields). This is recycled into
water and the soil when they die. They form a
source of slow release of nitrogen for the crop
plants. They have also been found to protect a part
of the applied fertilizer nitrogen from being lost.
Studies using N15 have shown that the nitrogen
fixed by the blue green algae is actually taken up by
the crop plants (26). This suggests that chemical
nitrogen fertilizer could be saved through biological
sources. Table 4 shows the effect of cyanobacterial
biofertilizer inoculation on rice grain yield at a
farmer’s field in India. Higher yields were obtained
in inoculated fields (21).
In India, Aulosira fertilissima Ghose,
Anabaena, Nostoc, Plectonema and Tolypothrix
species are grown in small 2 - meter ponds for two
months and dried. The dry flakes are applied at the
rate of 6 – 8 kg/hectare in rice fields, one week after
transplanting seedlings (15). On the other hand, a
bloom of filaments over seeded rice could be
deleterious by inhibiting rice seed emergence
through water (40). Microcystis flos aquae and M.
aerugenosa have been recorded in the lower River
Niger, and streams in Ekiti State and lakes in South
– Eastern Nigeria (16, 29, 30). On-going research
activities on flooded rice farms in Omor and Adani
rice fields in Anambra and Enugu States
respectively, have observed their abundance in
these areas.
Also, Anabaena growing symbiotically on
Azolla spp. (fern bryophyte) enriches the symbiotic
relationship with nitrogen. The Azolla plant contains
about 20 – 30% crude protein and high amino acid
content and as such is good fodder for cattle (to
increase milk yield), fish, poultry and pigs (13, 42),
for or as organic nitrogen, phosphate, and
potassium fertilizer source (green manure) in
farmlands. This bryophyte was observed in
inundated farms around Nike Lake (30). Van Howe
12
(42), Esiobu and Van Howe (13) and Van Howe and
Lejeune (42) highlighted the use of Azolla –
Anabaena azollae symbiosis in integrated
agricultural production of rice and fish, pig and fish
and poultry and fish. Other uses of Azolla include
weed suppression (11); water conservation by
reducing evapouration (12); decontamination by
desalination (38) and treatment of polluted waters
or sewage effluents (39).
Source of growth hormones: It has been found
that rice seeds pre-soaked in Phormidium tenue
(Menegh.) Gomont before planting have improved
tillering and hence improved yield (36).
Cylindrospermum musicola Kutz., Scytonema
hofmanni Ag. Ex Born. et Flahault, Nostoc
muscorum Agardh and Haplosiphon fontinalis
(Agardh) Born have been shown to synthesize
auxin - like (3 Indole acetic acid) and cytokinin –
like substances which stimulate the growth of
seedlings, regeneration and bulblet formation (22,
26, 41). Analysis of the growth - promoting
substances liberated by N. muscorum and H.
fontinalis showed the presence of amino acids such
as sereine, arginine, glycine, aspartic acid,
theonine, glutamic acid, cystine, proline, valine,
ornithine, lysine, histidine and iso-leusine (41).
Table 5 shows the results of bioassay of extracellar
cyanobacterial auxins vis a vis known auxin (IAA)
(17).
Conclusion: Cyanobacteria may sometimes be a
nuisance, but they are of great ecological and
agricultural significance. High input technologies
have resulted in high agricultural productivity, but
there is concern about the adverse effect of
indiscriminate fertilizer
application on soil
productivity and environmental quality. The
cosmopolitan nature of cyanobacteria makes them
readily available for research and utilization. They
offer an economically attractive and ecologically
sound alternative to chemical fertilizer for improved
crop production. There is therefore the need to
enlighten us on their potentials in order to stimulate
interdisciplinary research, harness the indigenous
species of economic and ecological importance,
combat the obnoxious forms, investigate their
potentials in biotechnology, disease causing ability
and maximize their potentials.
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