Spirulina

2008-10-06

A literature review on the biology of the blue-green algae of genus Spirulina

Spirulina Turpin 1872 is a cosmopolitan genus of cyanobacteria (also known as blue-green algae or Cyanophyta) that is found in water of various temperatures and salinities in the tropical to temperate areas of the Americas, Africa, and Eurasia. Its members form distinctive helically coiled filaments. The last twenty years have seen many increases in understanding of the systematics of the cyanobacteria thanks to molecular evidence, and, as such, the phylogenetic relationships of the genus Spirulina are still the subject of debate. Research is sure to continue, as there is interest in cultivating algae of this group on a large scale for their purported nutritive value.

Taxonomy and systematics

To date, very few of the cyanobacterial taxa have been officially recognized under either the Bacterial Code or the Botanical Code, although such attempts are under way.1 There is as yet no consensus on which of the other groups of bacteria is most closely related to the cyanobacteria + prochlorophyta; the best-supported suggestions are that they diverged from (i) all other photosynthetic bacteria, (ii) the green sulphur and filamentous bacteria, (iii) the purple sulphur or non-sulphur bacteria, or (iv) the purple non-sulphur bacteria, as shown in Figure 1.2

Figure 1: Possible evolutionary divergence points of the cyanobacteria
Figure 1: Possible evolutionary divergence points of the cyanobacteria

Rippka et al. 1979 classified the cyanobacteria into five groups based on morphology. “Spirulina” was included in Group III: the filamentous blue-greens that divide in only one plane and do not form heterocysts.3 In the 2001 edition of Bergey’s Manual of Systematic Bacteriology, Castenholz4 again placed the form-genera Spirulina and Arthrospira in Subsection III: Oscillatoriales, which all have helically coiled trichomes.5

There has been some debate over which species belong to the genus Spirulina. The morphologically similar genus Arthrospira Stizenberger 1892 was combined into genus Spirulina by Geitler in 1932, as both groups are coiled along their entire lengths. They were previously distinguished by the thickness of the cell wall, with Arthrospira spp. having visible septa, whereas Spirulina spp. had septa that were invisible under the light microscope.6

Figure 2: <i>Spirulina subsalsa</i>
Figure 2: Spirulina subsalsa
Figure 3: <i>Arthrospira platensis</i> with visible septa
Figure 3: Arthrospira platensis with visible septa

This distinction was reaffirmed when Castenholz 1989 separated the two groups into different genera once more, with the abundant species S. platensis and S. maxima being reassigned to genus Arthrospira. A new diagnostic feature is the production of γ-linolenic acid by Arthrospira species only.6,7 Other criteria are helix pitch (the degree of inclination) and the distribution of pores between adjoining cells.5 Spirulina is also distinctly more tightly coiled, and has been shown to be genetically distinct by 16S rRNA analysis by Nelissen et al. 1994, and by Nübel et al. 2000 in their description of gen. nov. Halospirulina.8

The most common species in the genus are S. subsalsa Oersted, S. labyrinthiformis Gomont, and S. major Kützing; they are distinguished phenetically on the basis of trichome diameter, tightness of spiral, and colour, which may range from yellow-green to blue-green to purple.

Morphology and ultrastructure

Spirulina spp. form trichomes, i.e. multicellular uniseriate filaments, composed of cylindrical cells. There is no constriction between cells, and the walls between cells are too thin to be seen by light microscopy in Spirulina (sensu Castenholz 1989). The trichome may be ensheathed in a polysaccharide secretion, which is not usually visible.9

The shape of the filaments is, however, dependent on environmental conditions. Salinity and temperature may cause the helix to become spiral6 or induce a change in colour.9 Drouet 1968 found a positive correlation between salinity and tightness of the spiral, though the significance of this adaptation is unclear.9 This indicates the necessity of genetic analysis to resolve the phylogeny of this group.

As in all cyanobacteria, Spirulina cells contain no distinct nucleus or membrane-bound plastids, are enveloped in a Gram-negative cell wall containing peptidoglycan, and have thylakoids — photosynthetic membranes with attached phycobilisomes.6 (A. platensis and A. geitleri are distinctive in having thylakoids arranged perpendicularly to the longest cell wall.10)

Neither Spirulina nor Arthrospira spp. produce heterocysts (hence their classification in Group III of the Cyanobacteria by Rippka et al. 1979); they have also never been found to manufacture nitrogenase, and are thus unable to fix atmospheric nitrogen.11

Motility

Spirulina spp. are motile: They glide by turning in a corkscrew motion. It has been found that this motility is controlled by neuromuscular effector molecules related to the contractile proteins of other prokaryotes, including Escherichia coli. Norepinephrine stimulates Spirulina motility, and it is hindered by the absence of Ca²⁺ ions.12

Reproduction and life history

Spirulina spp., being prokaryotic, do not reproduce sexually. They also do not form akinetes. Reproduction is vegetative, by means of intercalary division. This involves fission of the trichome along the cell wall between adjoining cells in the filament.9 Thus, they have a single-phase life history.

Biochemistry

Photosynthesis takes place using chlorophyll a and Photosystems I and II. The phycobilisomes on the thylakoids produce combinations of carotenoids, phycoerythrin, and phycocyanin. These pigments serve to increase the range of light frequencies that can be absorbed by the organism. The relative concentrations of the pigments, and thus the appearance of the cyanobacterium, are influenced by the light quality in which it grows. For example, in strong light, S. subsalsa appears blue-green, while in deep water, where mostly short-frequency light penetrates, more phycoerythrins are produced and the colour changes to maroon.9

Several species, including S. labyrinthiformis and A. platensis, are found in hot springs with high concentrations of hydrogen sulphide. H₂S has been found to stimulate photosynthesis in these species, and may be involved as an electron donor.13

Cyanobacteria do not manufacture the fatty acid arachidonic acid, which is found in red algae. However, A. platensis does synthesise γ-linolenic instead of α-linolenic acid. The eukaryotic algae make this as a precursor to arachidonic acid, which has led Nichols to suggest that this group may be a relic of this step in the evolution of the algae.11

Ecology

Spirulina” in the broad sense is found in shallow seas in North America, and in freshwater worldwide.9 It produces significant biomass in tropical and subtropical lakes, with Lake Chad containing large amounts of A. platensis, and A. maxima dominating Lake Texcoco in Mexico. These lakes are characterized by being shallow and alkaline, containing relatively high concentrations of sodium carbonate and bicarbonate.6

S. labyrinthiformis occurs in hot springs in Yellowstone Park, and A. platensis is found in volcanic lakes in India, where thick blooms take place at hydrogen sulphide concentrations as high as 0.3 mM. They may thrive in these conditions because the sulphide stimulates photosynthesis, as discussed above.

Flocculose mats of mainly Oscillatoria and “Spirulina” grow in the sheltered, nutrient-rich subtidal zone of the East Coast of North America. In the Florida Keys, intertidal rock pool communities form stratified algal mats. A gelatinous matrix is secreted to house two main layers, the upper containing Schizotrix spp. and Spirulina subtilissima, and the lower consisting of Lyngbya semiplena. Below this layer are found anaerobic purple sulphur bacteria.14

Uses

The composition of cyanobacterial communities in a river can serve as an indicator for the level of water pollution. Calothrix spp. only occur in unpolluted water, while the oscillatorians Oscillatoria chlorina and Arthrospira jenneri grow when the amount of organic pollutants in the river has caused the water to become deoxygenated.15

Spirulina” have been consumed by humans for centuries. It is thought that A. maxima was collected and sun-dried by the Aztecs for food, and cakes named dié made of A. platensis are still sold in modern times on the banks of Lake Chad. It is currently used as cattle fodder in Mexico, and as a health food supplement in the developed world. These algae consist of 62% protein and contain all the amino acids essential to humans.16

However, the Wellness Guide to Dietary Supplements of the University of California, Berkeley, points out that very large amounts of the alga must be eaten to derive adequate nutrition from it, and concludes that “the few nutrients in blue-green algae are more plentiful and cheaper in foods”.17

There is also concern over the possible presence of toxins. This is especially an obstacle to large-scale cultivation of the food, as ponds would have to be managed in such a way as to prevent the growth of other cyanobacteria, such as the bottom-dwelling Cylindrospermopsis raciborskii, which produces the hepatotoxin cylindrospermopsin.18


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  2. Doolittle WF. 1982. Molecular evolution. Ch. 12 in: Carr et al. 1982.19  ↩

  3. Cyanosite. http://www-cyanosite.bio.purdue.edu. Accessed 30 September 2008.  ↩

  4. Castenholz RW. 2001. Phylum BX. Cyanobacteria. Oxygenic photosynthetic bacteria. In Garrity G, Boone DR, Castenholz RW, eds. Bergey’s Manual of Systematic Bacteriology. 2nd ed. Vol. 1: The Archaea and the Deeply Branching and Phototropic Bacteria. Springer–Verlag: New York.  ↩

  5. Vonshak A, Tomaselli L. 2000. Arthrospira (Spirulina): systematics and ecophysiology. Ch. 18 in: Whitton BA, Potts M, eds. 2000. The Ecology of Cyanobacteria: Their Diversity in Time and Space. Kluwer Academic: Boston.  ↩

  6. Tomaselli L. 1997. Morphology, ultrastructure, and taxonomy of Arthrospira (Spirulina) maxima and Arthrospira (Spirulina) platensis. In: Vonshak A, ed. 1997. Spirulina platensis (Arthrospira): Physiology, Cell–biology, and Biotechnology. Taylor & Francis: London.  ↩

  7. Mühling M, Belay A, Whitton BA. 2005. Variation in fatty acid composition of Arthrospira (Spirulina) strains. Journal of Applied Phycology 17: 137–146.  ↩

  8. Nübel U, Garcia–Pichel F, Muyzer G. 2000. The halotolerance and phylogeny of cyanobacteria with tightly coiled trichomes (Spirulina Turpin) and the description of Halospirulina tapeticola gen. nov., sp. nov. International Journal of Systematic and Evolutionary Microbiology 50: 1265–1277.  ↩

  9. Humm HJ, Wicks SR. 1980. Introduction and Guide to the Marine Bluegreen Algae. John Wiley & Sons: New York.  ↩

  10. Lang NJ, Whitton BA. 1973. Arrangement and structure of thylakoids. In: Carr et al. 1973.20  ↩

  11. Nichols BW. 1970. Comparative lipid biochemistry of photosynthetic organisms. Ch. 6 in: Harborne JB, ed. 1970. Phytochemical Phylogeny. Academic Press: London.  ↩

  12. Castenholz RW. 1982. Motility and taxes. Ch. 16 in: Carr et al. 1982.19  ↩

  13. Padan E, Cohen Y. 1982. Anoxygenic photosynthesis. Ch. 9 in: Carr et al. 1982.19  ↩

  14. Golubić S. 1973. Relationship between blue–green algae and carbonate deposits In: Carr et al. 1973.20  ↩

  15. Fogg GE, Stewart WDP, Fay P, Walsby AE. 1973. The Blue–Green Algae. Academic Press: London.  ↩

  16. Fay P. 1983. The Blue–Greens. Edward Arnold: London.  ↩

  17. UC Berkeley Wellness Guide to Dietary Supplements. Blue–Green Algae. http://www.wellnessletter.com/html/ds/dsBlueGreenAlgae.php. Accessed 2008–09–30.  ↩

  18. Wisconsin Department of Natural Resources website. Blue–Green Algae in Wisconsin: Frequently Asked Questions. http://dnr.wi.gov/lakes/bluegreenalgae. Accessed 2008–09–30.  ↩

  19. Carr NG, Whitton BA, eds. 1982. The Biology of Cyanobacteria. UC Press: Berkeley.  ↩

  20. Carr NG, Whitton BA, eds. 1973. The Biology of the Blue–Green Algae. Blackwell: London.  ↩