Chapter 18

Heterokontophyta

RAPHIDOPHYCEAE

The Raphidophyceae, or chloromonads, have chlorophylls a and c, and two membranes of chloroplast endoplasmic reticulum. The anterior flagellum is commonly tinsel, whereas the posterior flagellum is naked (Figs. 18.1, 18.2, 18.3). The freshwater species of the Raphidophyceae are green, whereas the marine forms are yellowish and contain the carotenoid fucoxanthin (Vesk and

Moestrup, 1987). The closest relatives of the Raphidophyceae are the Eustigmatophyceae and the Chrysophyceae (Cavalier-Smith and Chao, 1996).

Marine species are euryhaline and eurythermic (tolerant of a wide salinity and temperature range) and occur in temperate and subtropical waters worldwide. Marine genera are Chattonella (Fig. 18.3), Fibrocapsa (Fig. 18.1(b)), and Heterosigma (Fig. 18.1(a)). Many of the marine species produce neurotoxic compounds that are similar to brevetoxin (Fig.18.2).

Fig. 18.1 (a) Heterosigma carterae. (b) Fibrocapsa japonica.

(C) Chloroplast; (M) mucocyst. ((a) after Leadbeater, 1969;

(b) after Hara and Chihara, 1985.)

(b)

(a)

410 CHLOROPLAST E.R.: EVOLUTION OF TWO MEMBRANES

Fig. 18.2 The chemical structure

of brevetoxin.

Uptake of the toxin by fish results in depolarization of nerves supplying the heart. This reduces the heart rate, thereby lowering blood pressure, which in turn affects the transfer of oxygen to the gill lamellae, creating hypoxic conditions that lead to fish mortality (Tyrrell et al., 2001).

Toxic red-tide blooms of the marine Chattonella antiqua and Heterosigma carterae (Taylor, 1992) have occurred in the Seto Inland Sea in Japan (Watanabe et al., 1988). These red tides occurred in the summer when a salinity and temperature stratification occurred at a depth of 5–10 meters. There was little mixing of waters above and below the stratified layer resulting in the upper layer being deficient in nutrients while the bottom layer was anaerobic. Heterosigma carterae flourishes under these conditions because it has a daily vertical migration of 10 to 15 meters and this allows the alga to move between the stratified layers. This migration enables H. carterae to use the nutrients in the lower layers, and light and oxygen in the upper layer, resulting in the red-tide blooms of the organism. The migration is correlated with the production and degradation of cytoplasmic fat particles (Wada et al., 1987). Heterosigma carterae has a wide salinity tolerance in culture (3 to 50%) and loses its motility at temperatures below 10 °C. At 5 to 10 °C, the alga forms non-motile masses capable of surviving in continuous darkness for up to 15 weeks (Han et al., 2002). This is a far longer dark period than the motile cells can tolerate and still live. In Narragansett Bay, Rhode Island, blooms of H. carterae occur during a period of low nitrogen concentration, but at a time when phosphate levels are near a yearly maximum (Tomas, 1979).

Chattonella antiqua is a marine raphidophyte that produces blooms in coastal Japan. In 1972, a bloom killed 500 million dollars worth of caged yellow-tail fish in the Seto Inland Sea (Okaichi, 1989). C. antiqua has the highest toxicity during the early to mid-logarithmic phase. After reaching the stationary phase, the toxicity decreases markedly (Khan et al., 1996). The life cycle of Chattonella antiqua involves a vegetative propagation phase and a non-motile dormant phase (Fig. 18.3) (Yamaguchi and Imai, 1994). The vegetative diploid cells grow by binary fission under normal growth conditions. Small haploid cells are produced when the nutrients are depleted in the medium. These haploid cells change into cysts under low-light conditions and spend several months dormant in bottom sediments. The period of dormancy usually lasts from the end of summer to the following spring and is enforced by low temperatures (Imai and Itoh, 1987). Swarmers germinate from the cysts and somehow become diploid, although how diploidization occurs is not known. The resulting diploid vegetative cells complete the life history.

In freshwater, Raphidophyceae are associated with mud bottoms or ponds with abundant macrophytes. Vacuolaria contains chlorophylls a and c as well as the carotenoid -carotene and the xanthophylls lutein epoxide and antheraxanthin (Chapman and Haxo, 1966; Guillard and Lorenzen, 1972). The numerous chloroplasts have three thylakoids per band, and there are two membranes of chloroplast E.R. around the chloroplasts (Koch and Schnepf, 1967; Mignot, 1967). Vacuolaria (Fig. 18.4(a)) can be free-swimming or in a palmelloid state. In the palmelloid condition,

HETEROKONTOPHYTA, RAPHIDOPHYCEAE	411

Fig. 18.3 The life cycle of

Chattonella antiqua. (Adapted from

Yamaguchi and Imai, 1994.)

Fig. 18.4 (a) Vacuolaria virescens, showing chloroplasts (c), mucilaginous bodies (m), flagella, contractile vacuoles (cv), and the nucleus (n); (b) Gonyostomum semen with chloroplasts, trichocysts (t), contractile vacuoles, and the nucleus. (After Mignot, 1967.)

412 CHLOROPLAST E.R.: EVOLUTION OF TWO MEMBRANES

the cells are more or less spherical, 35 to 50 m in diameter, yellow-green with each cell surrounded by a thick gelatinous matrix. In the freeswimming state, the organisms vary considerably in shape from broadly ovate to elongate. The flagella emerge from a simple notch slightly to one side of the anterior ventral region. The anteriorly directed flagellum has microtubular hairs, whereas the posteriorly directed flagellum is whiplash. There is no stigma, but the organism is positively phototactic. Vacuolaria divides only in the palmelloid state. Mitosis is typically eukaryotic, with the nuclear membrane remaining intact (Heywood and Godward, 1972). No sexual reproduction has been reported in Vacuolaria. Occasionally the cells form cysts with the resistant sheaths surrounding the cells (Spencer, 1971).

Vacuolaria has muciferous bodies (mucocysts) in the peripheral cytoplasm (Fig. 18.4(a)), which are similar in structure to those in the Prymnesiophyceae and Chrysophyceae. The genus Gonyostomum (Fig. 18.4(b)) has trichocysts similar to those in the Dinophyceae (Mignot, 1967).

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