Chapter 2

Cyanobacteria

CYANOPHYCEAE

Morphology

The Cyanophyceae or blue-green algae are, today, usually referred to as the cyanobacteria (bluegreen bacteria). The term cyanobacteria acknowledges that these prokaryotic algae are more closely related to the prokaryotic bacteria than to eukaryotic algae. For the last quarter century, cyanobacteria were thought to have evolved about 3.5 billion years ago. These reports were based on interpretation of microfossils, difficult at best with such small organisms. It now appears that these investigators selected specimens that fit the assumptions of the authors, with most phycologists now rejecting their claims. Based on other reports, the actual time of evolution of cyanobacteria is thought to be closer to 2.7 billion years ago (Buick, 1992; Brasier et al., 2002; Dalton, 2002).

Cyanobacteria have chlorophyll a (some also have chlorophyll b or d), phycobiliproteins, glycogen as a storage product, and cell walls containing amino sugars and amino acids.

At one time, the occurrence of chlorophyll b in cyanobacteria was used as a criterion to place the organisms in a separate group, the Prochlorophyta. Modern nucleic-acid sequencing, however, has shown that chlorophyll b evolved a number of times within the cyanobacteria and the term Prochlorophyta has been discarded (Palenik and Haselkorn, 1992; Urback et al., 1992).

The simplest morphology in the cyanobacteria is that of unicells, free-living (see Figs. 2.19(c), 2.20) or enclosed within a mucilaginous envelope (Figs. 2.48, 2.56(a), (b)). Subsequent evolution resulted in the formation of a row of cells called a trichome (Fig. 2.16). When the trichome is surrounded by a sheath, it is called a filament (Fig. 2.10). It is possible to have more than one trichome in a filament (Figs. 2.56(e), 2.58(b)). The most complex thallus is the branched filament (Fig. 2.58(a)). Such a branched filament can be uniseriate (composed of a single row of cells) or multiseriate (composed of one or more rows of cells).

Cell wall and gliding

The cell wall of cyanobacteria is basically the same as the cell wall of Gram-negative bacteria (Fig. 2.1). A peptidoglycan layer is outside of the cell membrane. The peptidoglycan is an enormous polymer composed of two sugar derivatives, N-acetylglucosamine and N-acetylmuramic acid, and several different amino acids (Fig. 2.2). Outside of the peptidoglycan is a periplasmic space, probably filled with a loose network of peptidoglycan fibrils. An outer membrane surrounds the periplasmic space.

Some cyanobacteria are capable of gliding, that is, the active movement of an organism on a solid

34 THE PROKARYOTIC ALGAE

Fig. 2.1 Transmission electron micrographs of sections of the wall of the cyanobacterium Phormidium uncinatum. The cell wall (CW) contains layers similar to those of a Gram-negative bacterium, e.g., the cytoplasmic membrane (CM), peptidoglycan layers (P), periplasmic space (PS) and outer membrane (OM). In addition, the cyanobacterium contains the additional two external layers typical of a motile cell, the serrated external layer (EL) and hair-like fibers (F). (CJ) Circumferential junction; (JP) junctional pore. (From Hoiczyk and Baumeister, 1995.)

substrate where there is neither a visible organ responsible for the movement nor a distinct change in the shape of the organism (Jarosch, 1962). Gliding is a slow uniform motion (up to 600 m s 1 in Oscillatoria; Bhaya, 2004) at a direction parallel

Fig. 2.2 The structure of a peptidoglycan molecule in the

cell wall of cyanobacteria.

to the long axis of the cell and is occasionally interrupted by reversals in direction. Gliding is accompanied by a steady secretion of slime, which is left behind as a mucilaginous trail. Some cyanobacteria (Phormidium, Oscillatoria) rotate during gliding while other cyanobacteria (Anabaena) do not rotate.

The cell wall of gliding bacteria has two additional layers outside of the cell wall (Figs. 2.1, 2.3, 2.4). A serrated external layer (S-layer) and a layer of hair-like fibers occur outside of the outer membrane of the cell wall of gliding cyanobacteria. The hair-like fibers of the outermost layer are composed of a rod-like glycoprotein called oscillin (Hoiczyk and Baumeister, 1998; Hoiczyk, 2000).

The cross walls of neighboring cells of gliding cyanobacteria contain junctional pores that are 15 nm in diameter and radiate outward from the cytoplasm at an angle of about 30–40° relative to the plane of each septum (Figs. 2.1, 2.5, 2.6). The number of rows of junctional pores around each side of the septum varies from one circumferential ring in Phormidium to several rows of pores that girdle the septum in Anabaena. The junctional pore is 70–80 nm long and spans the entire multilayered cell wall. The junctional pore is composed of a tube-like base and an outer pore complex.

Gliding occurs by slime secretion through the circumferential junctional pores on one side of the septum (Hoiczyk and Baumeister, 1998; Hoiczyk, 2000). The slime passes along the surface of the oscillin fibers of the outer layer of the cell wall and onto the adjacent substrate, propelling the filament forward. The orientation of the

CYANOBACTERIA 35

Fig. 2.3 Cross sections of a wall of a cyanobacterium that is not capable of gliding and a cross section of a wall of a cyanobacterium that is capable of gliding. Cyanobacteria that can glide have an additional two wall layers on the outside. (From Hoiczyk and Baumeister, 1995.)

Fig. 2.4 A model of the junctional pore complex of a cyanobacterium. Extrusion of slime through the

circumferentially arranged junctional pores on one side of the cross wall results in forward movement of the filament in contact with the substrate. The arrangement of the oscillin fibers in the outer layer of the cell wall determines whether the filament rotates as it glides over the surface. In the

drawing, the oscillin fibers are spiraled so the filament rotates as it glides. (Modified from Hoiczyk and Baumeister, 1998.)

oscillin fibers of the outer layer determines whether the filament rotates during gliding. In Anabaena, the spiral oscillin fibers produce a clockwise rotation while in Oscillatoria princeps and Lyngbya aeruginosa the oscillin fibers are spiraled in the opposite direction and produce a counterclockwise rotation during gliding

36 THE PROKARYOTIC ALGAE

Fig. 2.5 Transmission electron micrographs of Phormidium uncinatum. (A) Isolated cell wall with the outer membrane and external layer (EL) still attached. On both sides of the cross wall, the ring-shaped counterpart of the junctional pores with their central pores are visible. (B) Negatively stained isolated wall showing the junctional pores (JP) filled with slime. (CW) cross wall. (C) Isolated outer membrane with the ring-shaped parts of the junctional pores. (From Hoiczyk and Baumeister, 1995.)

(Hoiczyk and Baumeister, 1995) (Fig. 2.7). In Phormidium, the oscillin fibers are not spiraled and the filament does not rotate during gliding.

The arrangement of hair-like fibers thus serves as a passive screw as the slime passes over their surface in gliding. Reversal of gliding occurs when slime stops coming out of the ring of junctional pores on one side of the septum, and when slime begins coming out of the ring of junctional pores on the other side of the septum.

Pili and twitching

Pili are proteinaceous appendages that project from the surface of cyanobacterial cells (Fig. 2.8). There are two types of pili in the unicellular cyanobacterium Synechocystis (Bhaya, 2004). The cell is covered uniformly with a layer of thin- brush-like pili with an average diameter of 3–4 nm and a length of 1 m. Cells also have thick flexible pili with a diameter of 6–8 nm and length of 4–5m that often make connections with other cells. The pili are composed of 500 to 1000 units of the polypeptide pilin. Each pilin unit consists of between 145 and 170 amino acids (Bhaya et al., 1999). The pilin molecule is similar to the oscillin molecule involved in gliding. Synechocystis is able to move across a surface at 1 to 2 m s 1 using a mechanism called twitching that utilizes change in configuration of the pili (Wall and Kaiser, 1999). The pili probably move the cell body along a sur-

Fig. 2.6 Structure of the organelles of the junctional-pore complex in Phormidium uncinatum. Transmission electron micrograph of a negatively stained isolated outer membrane patch showing the ring-shaped orifices of the junctional pores that would be circumferentially arranged in the cross wall in the cell. Inset shows a number of superimposed images of junctional-pore complexes. (From Hoiczyk, 2000.)