REFERENCES

The Glaucophyta include those algae that have endosymbiotic cyanobacteria in the cytoplasm instead of chloroplasts. Because of the nature of their symbiotic association, they are thought to represent intermediates in the evolution of the chloroplast. The endosymbiotic theory of chloroplast evolution, first proposed by Mereschkowsky in 1905, is the one most widely accepted. According to this theory, a cyanobacterium was taken up by a phagocytic organism into a food vesicle. Normally the cyanobacterium would be digested by the flagellate, but by chance a mutation occurred, with the flagellate being unable to digest the cyanobacterium. This was probably a beneficial mutation because the cyanobacterium, by virtue of its lack of feedback inhibition, secreted considerable amounts of metabolites to the host flagellate. The flagellate in turn gave the cyanobacterium a protected environment, and the composite organism was probably able to live in an ecological niche where there were no photosynthetic organisms (i.e., a slightly acid body of water where free-living cyanobacteria do not grow; see Chapter 2). Pascher (1914) coined terms for this association; he called the endosymbiotic cyanobacteria cyanelles; the host, a cyanome; and the association between the two, a syncyanosis. In the original syncyanosis the cyanelle had a wall around it. Because the wall slowed the transfer of compounds from the cyanelle to the host and vice versa, any mutation that resulted in a loss of wall would have been beneficial and selected for in evolution. Most of the cyanelles in the

Glaucophyta lack a wall and are surrounded by two membranes – the old food vesicle membrane of the cyanome and the plasma membrane of the cyanelle. As evolution progressed, these two membranes became the chloroplast envelope, the cyanome cytoplasm took over the formation of the storage product and the polyhedral bodies containing ribulose-1,5-bisphosphate carboxylase/ oxygenase differentiated into the pyrenoid.

There are a number of similarities between cyanobacteria and chloroplasts that support the endosymbiotic theory: (1) they are about the same size; (2) they evolve oxygen in photosynthesis;

(3) they have 70S ribosomes; (4) they contain circular prokaryotic DNA without basic proteins;

(5) nucleotide sequencing of rRNA or of DNA encoding rRNAs have shown similarities; (6) they have chlorophyll a as the primary photosynthetic pigment.

The pigments of the Glaucophyta are similar to those of the Cyanophyceae: both chlorophyll a and the phycobiliproteins are present; however, two of the cyanobacterial carotenoids, myxoxanthophyll and echinenone, are absent (Chapman, 1966).

Although similar to cyanobacteria, the cyanelles should be regarded as organelles rather than endosymbiotic cyanobacteria (Helmchen et al., 1995; McFadden, 2001). Cyanobacteria have over 3000 genes whereas cyanelles have about the same number of genes as plastids (about 200 genes). It is clear the cyanelles (and plastid) genomes have undergone substantial reduction

during endosymbiosis. Many of the missing genes eventually relocated to the nucleus, while other genes were lost – made redundant in the cyanelles’ new role as an endosymbiont. For example, cyanobacteria have a respiratory electronchain whereas plastids do not, the respiratory electron-chain is coded by the nucleus in eukaryotic algae.

The organisms in the Glaucophyta are very old; McFadden (2001) calls them the coelocanths of endosymbiosis. The Glaucophyta probably branched off the evolutionary tree before the divergence of red and green algae from one another (Keeling, 2004).

The fact that in such syncyanoses one is dealing with composite organisms that exhibit features altogether new and no longer characteristic of either partner alone, led Skuja in 1954 to establish the phylum Glaucophyta. It must be appreciated that the organisms in the phylum represent a very old group, and that, when evolving, they were very plastic and undergoing a great deal of change in the attempt to reach the relatively stable level of a cell with a chloroplast. Such a dynamic group was formed consisting of a large number of organisms not well suited to compete with their more highly developed progeny. Such a situation led to the demise of many of the original members of the Glaucophyta, resulting in the existence today of few extant members of the group.

Cyanophora paradoxa is a freshwater flagellate with two cyanelles in the protoplasm, each cyanelle with a central dense body (Fig. 3.1(a)). Nitrate reduction, photosynthesis, and respiration in the cyanelles of Cyanophora paradoxa are similar to the corresponding processes of chloroplasts and dissimilar to those of cyanobacteria (Floener and Bothe, 1982; Floener et al., 1982). This fact is cited as evidence that the cyanelles of Cyanophora paradoxa are close to chloroplasts in evolution. However, the cyanelles of Cyanophora paradoxa are primitive in regard to where ribulose-1,5-bisphosphate carboxylase/ oxygenase is produced. Ribulose-1,5-bisphosphate carboxylase/oxygenase, the carbon dioxide-fixing

enzyme in photosynthesis, consists of 16 subunits, 8 large and 8 small. In higher plants the large subunits are encoded by DNA of the plastids, whereas the small subunits are encoded by nuclear DNA. In Cyanophora paradoxa, both sizes of subunits are encoded by cyanelle DNA. This non-cyanobacterial ribulose-1,5-bisphosphate carboxylase/oxygenase in cyanelles is now rationalized as lateral gene transfer or gene substitution from a mitochondrion or plastid (McFadden, 2001). The mechanism of division of cyanelles in Cyanophora paradoxa is intermediate between the division of cyanobacteria and that of plastids. Plastids have an inner and outer ring of electrondense material in the area of the dividing organelle. In division of cyanelles of Cyanophora paradoxa, however, there is only an inner ring in the “stroma” inside the plasma membrane (“inner envelope”) of the cyanelle. The outer ring, normally outside the outer chloroplast envelope, is missing (Fig. 3.2) (Iino and Hashimoto, 2003).

Glaucocystis is also a freshwater organism, found sparingly in soft-water lakes (lakes low in calcium). It has two groups of cyanelles, one on each side of the nucleus (Fig. 3.1(b)). The derivation of Glaucocystis from a biflagellate ancestor is evident from the two reduced flagella found inside the cell wall. Both of these organisms have starch formed in the cytoplasm, outside of the cyanelles, indicating that the host has accepted responsibility for the formation of the storage product.

There are other organisms that have endosymbiotic cyanobacteria that are not placed in the Glaucophyta because they represent evolutionary dead ends that did not lead to the evolution of chloroplasts. These organisms have cyanelles that still have a cell wall and are cytologically similar to cyanobacteria, such as the cyanelles of the fungus Geosiphon (Schnepf, 1964).