Chapter 10

Heterokontophyta

The algae in the Heterokontophyta usually have cells with an anterior tinsel and posterior whiplash flagellum (Fig. 10.1). The plastids contain chlorophylls a and c along with fucoxanthin. The storage product is usually chrysolaminarin in cytoplasmic vesicles.

The following classes are commonly recognized (Andersen, 2004):

Chrysophyceae (golden-brown algae) (Chapter 10)

Synurophyceae (Chapter 11) Eustigmatophyceae (Chapter 12) Pinguiophyceae (Chapter 13)

Dictyochophyceae (silicoflagellates) (Chapter 14)

Pelagophyceae (Chapter 15)

Bolidophyceae (Chapter 16)

Bacillariophyceae (diatoms) (Chapter 17) Raphidophyceae (chloromonads) (Chapter 18) Xanthophyceae (yellow-green algae)

(Chapter 19)

Phaeothamniophyceae (Chapter 20)

Phaeophyceae (brown algae) (Chapter 21)

CHRYSOPHYCEAE

The Chrysophyceae are distinguished chemically by having chlorophylls a, c1, and c2 (Andersen and Mulkey, 1983) and structurally by two flagella inserted into the cell perpendicular to each other, one photoreceptor on the short flagellum that is usually shaded by an eyespot in the anterior portion of the chloroplast, contractile vacuoles in the

anterior portion of the cell, chloroplast endoplasmic reticulum, and radially or biradially symmetrical silica scales (if they are present). The storage product is chrysolaminarin. Many members of the class produce statospores enclosed in a silicified wall with a terminal pore.

Most of the species in the Chrysophyceae are freshwater and occur in soft waters (low in calcium). Many of the freshwater species are in the plankton of lakes where they are present in abundance. The coccoid and filamentous genera are found mostly in cold springs and brooks, where they occur as gelatinous or crustous growths on stones and woodwork. Most of the Chrysophyceae are sensitive to changes in the environment and survive the unfavorable periods as statospores.

Cell structure

Flagella and eyespot

Many of the Chrysophyceae have a tinsel flagellum that is inserted at the anterior end of the cell parallel to the cell axis (Fig. 10.1) and a whiplash flagellum that is inserted approximately perpendicular to the tinsel flagellum. The whiplash flagellum is often reduced to a short stub. The hairs on the tinsel flagellum are usually tripartite microtubular hairs (Hill and Outka, 1974), although tripartite and fibrillar hairs have been reported in Ochromonas (Bouck, 1971) (Fig. 10.2). Flagellar scales have been seen in a couple of genera (Andersen, 1982). The posterior whiplash flagellum is usually the shorter flagellum and has a swelling at its base on the side toward the cell

334 CHLOROPLAST E.R.: EVOLUTION OF TWO MEMBRANES

Fig. 10.1 Semidiagrammatic drawing of a light and electron microscopical view of the basic organization of a cell of the Chrysophyceae. (C) Chrysolaminarin vesicle; (CE) chloroplast envelope; (CER) chloroplast endoplasmic reticulum; (CV) contractile vacuole;

(E) eyespot; (FS) flagellar swelling;

(G) Golgi body; (H) hair of the anterior flagellum; (MB) muciferous body; (MR) microtubular root of flagellum; (N) nucleus. (Adapted from Hibberd, 1976.)

(Fig. 10.1). This flagellar swelling contains an elec- tron-dense area referred to as the photoreceptor. The flagellar swelling contains retinal, the chromophore of rhodopsin-like proteins, suggesting that a rhodopsin-like protein is the photoreceptor in the Chrysophyceae (Walne et al., 1995). The flagellar swelling fits into a depression of the cell immediately beneath which, inside the chloroplast, is the eyespot. The eyespot consists of lipid globules inside the anterior portion of the chloroplast, between the chloroplast envelope and the first band of thylakoids.

In Ochromonas, the long tinsel flagellum beats in one plane and pulls the cell forward, whereas the shorter flagellum is flexed over the anterior eyespot and appears to play little role. During forward movement the cell rotates because of the shape of the body.

Internal organelles

The chloroplasts are parietal and usually only a few in number, often only one or two. Chlorophylls a, c1, and c2 are present, with the main carotenoid being fucoxanthin. The chloroplasts are surrounded by two membranes of chloroplast E.R., the outer membrane of which is usually continuous with the outer membrane of the nuclear envelope (Fig. 10.1). The thylakoids are usually grouped three to a band.

The chloroplast of Ochromonas danica will form a small proplastid if the cells are grown in the dark (Gibbs, 1962). The proplastid contains a single thylakoid, a few small vesicles, and a large number of dense granules. The chlorophyll a content of the proplastid is about 1.2% of the mature chloroplast. On exposure of the proplastid to light, vesicles appear that fuse to form the thylakoids. After 2 days

HETEROKONTOPHYTA, CHRYSOPHYCEAE	335

Fig. 10.2 Ochromonas danica. (B) Basal attachment region; (C) chloroplast; (E) eyespot; (FM) fibrillar hair;

(L) leucosin; (LF) lateral filament; (MM) microtubular hair; (Mt) microtubule; (N) nucleus; (TF) terminal filament. (After Bouck, 1971.)

in the light, the chloroplasts have reached their mature form, although it takes 8 days for them to acquire their full complement of chlorophyll.

Pyrenoids are common in chloroplasts of the Chrysophyceae. They consist of a granular area that is different in appearance from the stroma. Few, if any, thylakoids traverse the pyrenoid area.

The storage product is chrysolaminarin (leucosin), a -1,3 linked glucan, supposedly found in a posterior vesicle (Fig. 10.1). The actual function of the so-called chrysolaminarin vesicle may be more complex than supposed with the discovery of microorganisms in the chrysolaminarin vesicle

of Ochromonas (Daley et al., 1973; Dubowsky, 1974). The chrysolaminarin vesicle is much larger in organisms grown in the dark on a synthetic medium than in cells grown in the light. The opposite would be expected if the vesicle stored chrysolaminarin, the accumulation product of photosynthesis in the light. It may be that the structure may also function as a digestive vesicle, breaking down material taken up by the cell into building blocks for metabolism and growth.

The single nucleus is pear-shaped (pyriform), with its narrow anterior end extended in the direction of the basal bodies (Fig. 10.1). There is a single, large Golgi body which lies against the nucleus in the anterior part of the cell, often in a concavity in the nuclear envelope. Contractile vacuoles are common, usually occurring in the anterior part of the cell next to the Golgi apparatus. There is often a complex system of vesicles associated with the contractile vacuoles similar to the pusule system in the Dinophyceae. Lipid bodies can also be found in the protoplasm. In young cells there are usually few lipid bodies; however, as the cell ages, the lipid bodies become larger and more numerous until they fill the protoplasm.

Two different types of projectiles occur in the Chrysophyceae, muciferous bodies and discobolocysts, the former like the muciferous bodies in the Prymnesiophyceae, Raphidophyceae, and Dinophyceae. The muciferous bodies (Fig. 10.1) contain granular material and are bonded by a single membrane. On discharge the contents of the vesicle often form a fibrous network outside the cell. The discobolocysts are similar to the muciferous bodies and have been described in the most detail by Hibberd (1970), in Ochromonas tuberculatus (Fig. 10.3). The discobolocysts are in the outer layer of cytoplasm and consist of a single membranebounded vesicle with a hollow disc in the outwardfacing part of the vesicles. The discharge of the discobolocyst is explosive, taking place by the expansion of the projectile into a thin thread 6 to 11 m long, the disc being at the tip of the mucilage. As the discharge occurs, the cell jerks violently under the recoil to a distance of 5 m. After the discharge of either muciferous bodies or discobolocysts, the protoplast recovers without any deleterious effects. Both of the projectiles originate in the area of the Golgi apparatus.

336 CHLOROPLAST E.R.: EVOLUTION OF TWO MEMBRANES

Fig. 10.3 (a) Ochromonas tuberculatus. (b) Charged and discharged discobolocysts. (CE) Chloroplast envelope; (CER) chloroplast endoplasmic reticulum; (CV) contractile vacuole; (D) discobolocyst; (E) eyespot; (FS) flagellar swelling;

(G) Golgi body; (LF) long flagellum; (N) nucleus; (Nu) nucleolus; (O) oil; (P) plastid. (After Hibberd, 1970.)

Extracellular deposits

Cell walls composed of cellulose (Herth and Zugenmaier, 1979), loricas, and silicified scales and walls, occur in some of the Chrysophyceae (Preisig, 1994). Silica scales, such as those in Paraphysomonas (Fig. 10.4), are radially or biradially symmetrical. The scales are arranged loosely outside the plasma membrane without any clearly defined pattern. Like the Bacillariophyceae and Synurophyceae, the scales of the Chrysophyceae are formed inside a silica deposition vesicle that is derived from endoplasmic reticulum (Schnepf and Deichgraber, 1969). This arrangement differs from that of the calcified scales of the Prymnesiophyceae and the Chlorophyta, which are formed by the Golgi apparatus. Scale formation is also similar to frustule formation in the diatoms in that the addition of germanium (a competitive inhibitor of silicon utilization) to the growth medium results in inhibition of growth (Lee, 1978). Organic scales without mineralization also occur in the Chrysophyceae. In Chromulina placentula, there is a single layer of

organic scales covering the posterior portion of the cell, the scales being very similar to those found in the Prymnesiophyceae (Throndsen, 1971).

In one of the orders (Parmales), silicified walls occur which are composed of five or eight parts (Figs. 10.14, 10.15) (Booth and Marchant, 1987). Loricas, such as those in Pseudokephyrion pseudospirale and Kephyrion rubri claustri, can also be mineralized. Manganese can occur in loricas as needle-like structures, whereas iron occurs as granular deposits (Dunlap et al., 1987).

Some of the species have a lorica (an envelope around the protoplast, but not generally attached to the protoplast as a wall is). In Dinobryon (Fig. 10.11), the lorica is composed of an interwoven system of microfibrils (Kristiansen, 1969). The formation of the lorica begins when a small funnelshaped piece arises from the cell. The protoplast then rotates on its axis following a spiral course and secreting the remainder of the lorica. When the lorica is complete, the protoplast withdraws to its base. Several strains of Ochromonas malhamensis and O. sociabilis produce a delicate lorica consisting of a 10to 20- m hollow stalk and a cup-shaped envelope that encloses a long protoplasmic filament and the basal half of the cell, respectively. The lorica of O. malhamensis is composed of the polysaccharide chitin (Herth et al., 1977). The lorica can be mineralized as is the case with