PRYMNESIOPHYCEAE

The Prymnesiophyta are a group of uninucleate flagellates characterized by the presence of a haptonema between two smooth flagella. The Prymnesiophyta have two membranes of chloroplast endoplasmic reticulum, as do the Cryptophyta and the Heterokontophyta, but differ in having flagella without mastigonemes. Molecular data also show that the Prymnesiophyta are distinct from the Cryptophyta and Heterokontophyta (Bhattacharya and Ehlting, 1995; Medlin et al., 1994). Until 1962, the organisms were considered part of the Chrysophyceae, at which time Christensen split them off into a separate class, the Haptophyceae (named after the presence of the haptonema). The name Haptophyceae was a descriptive name and not based on a genus in the class; thus the name was later changed to Prymnesiophyceae, based on the genus Prymnesium (Fig. 22.7) (Hibberd, 1976). The fossil record of the Prymnesiophyceae is known from the Carboniferous (approximately 300 000 000 years ago) (Faber and Preisig, 1994; Jordan and Chamberlain, 1997).

The cells are commonly covered with scales. In many cases, the scales are calcified, thereby producing coccoliths. The chloroplasts lack girdle lamellae and most contain chlorophylls a and c1/c2, -carotene, diadinoxanthin, and diatoxanthin (Zapata et al., 2004). The storage product is chrysolaminarin (leucosin) in vesicles in the posterior end of the cell ( Janse et al., 1996). The anterior end of the cell has a large Golgi apparatus and sometimes a contractile vacuole.

The Prymnesiophyceae are primarily marine organisms, although there are some freshwater representatives. They make up a major part of the marine nannoplankton and constitute about 45% of the total phytoplankton cells in the middle latitudes of the South Atlantic. They decrease in frequency toward the poles although some still occur in polar waters (Manton et al., 1977).

Cell structure

Flagella

Most of the Prymnesiophyceae have two smooth flagella of approximately the same length (Figs. 22.1, 22.3(a)). The Pavlovales is the exception, where one flagellum is longer than the other and is usually covered by small cylindrical to clubshaped hollow scales 70 nm long and 20 nm wide (Fig. 22.3(b)) (van der Veer, 1969; Green and Manton, 1970). Because the class is characterized by two more or less equal, smooth flagella, a number of genera, such as Diacronema (Fig. 22.4), Isochrysis (Fig. 22.18(b)), and Dicrateria, which have rudimentary or no haptonema, are grouped in the Prymnesiophyceae (Green and Pienaar, 1977). There is usually no flagellar swelling associated with an eyespot as occurs in many other goldenbrown flagellates with two membranes of chloroplast E.R. (Hibberd, 1976), although there are exceptions (Green and Hibberd, 1977).

During swimming, the flagellar end of the cell can be forward with the flagella sweeping outward and backward down the sides of the body (Fig. 22.5(a)), or the flagellar end may be directed

backward (Fig. 22.5(b)). Movement is usually rapid, the cells swimming only for a short distance in one direction, after which they rapidly change the position of the flagella and move off in the opposite direction. In Pavlova (Fig. 22.3(b)), the flagellar action is a little different, with the longer flagellum directed forward and the shorter flagellum trailing or directed outward.

Haptonema

A haptonema is a filamentous appendage arising near the flagella but thinner and with different properties and structure. The haptonema ranges from a few profiles of E.R. that represent a reduced haptonema in Imatonia rotunda (Fig. 22.18(c), (d))

(Green and Pienaar, 1977) to a short bulbous structure in Hymenomonas roseola (Fig. 22.6(a)) to the 80- m-long whip-like structure in

Chrysochromulina parva (Fig. 22.6(b)) (Manton, 1967a). The haptonema of Prymnesium parvum has an internal structure similar to the haptonema of other Prymnesiophyceae and will be used as an example of haptonemal structure (Fig. 22.7) (Manton, 1964). In transverse section the haptonema is composed of three concentric membranes surrounding a core containing seven microtubules. The core is covered by the innermost of the three membranes so that there is no contact between the core microtubules and the outer portion of the haptonema. The space

Fig. 22.2 Irene Manton 1904–1988. Dr. Manton was a graduate of Cambridge University. She was a lecturer in botany at the University of Manchester from 1929 to 1945 and Professor of Botany at the University of Leeds from 1945 to 1969. Dr. Manton was one of the foremost cytologists during the 1950s and 1960s when the new science of electron microscopy was adding vast amounts of new information to the understanding of algae. The work of Dr. Manton and her colleagues led to the distinct features

of the haptophytes and the recognition of these organisms as a distinct group of algae.

between the innermost and middle membranes is a vesicle continuous over the tip of the core. The haptonema is commonly covered with small body scales.

The microtubules in the haptonema slide, relative to one another, probably through the calcium-binding protein centrin (Lechtreck, 2004), to produce two basic movements, coiling and bending (Greyson et al., 1993):

1Coiling is a sensory response to obstacles (Kawachi and Inouye, 1994). The haptonema coils instantly when forward-swimming cells

encounter obstacles. The flagella are thrown backward and generate propulsive forces, resulting in backward swimming.

2Bending by the haptonema occurs during food capture by the cells (Inouye and Kawachi, 1994; Kawachi et al., 1991). Prey particles adhere to the haptonema as the cells swim with the haptonema projecting ahead of the cell, and the flagella beating alongside. The adhering particles are transported down to a particular point on the haptonema, about

2 m distal from the base, called the particleaggregating center (Fig. 22.8). The particles accumulate at the particle-aggregating center, resulting in the production of a massive aggregate. In the aggregate, individual particles tightly adhere to one another, suggesting that some sort of cementing material is secreted. After reaching a certain size, the aggregate moves to the tip of the haptonema. The haptonema bends into a sigmoid shape and eventually delivers the aggregate to the posterior end of the cell, where the aggregate is injected into a food vacuole.

Chloroplasts

Usually there are two elongate discoid chloroplasts in each cell (Fig. 22.1). Each chloroplast is surrounded by four membranes: the two membranes of the chloroplast envelope, and outside of them the two membranes of the chloroplast E.R. The thylakoids are aggregated into bands of three. A girdle band of thylakoids is usually absent (Hibberd, 1976). A pyrenoid is commonly present in the center of the chloroplast or as a bulge to one side. Eyespots are not common in the Prymnesiophyceae although Pavlova has an eyespot, which consists of a group of lipid droplets inside the anterior end of a chloroplast (Green, 1973) (Fig. 22.21).

Other cytoplasmic structures

Two types of membrane-bounded vesicles are in the cytoplasm, the first containing lipids and the second the storage product. The storage product is usually stated as being chrysolaminarin (leucosin) (Janse et al., 1996), although in a study of Pavlova mesolychnon (Fig. 22.3(b)) it was found that one of

the storage products present in the cells was a - 1,3 linked glucan similar to paramylon in the Euglenophyceae (Kreger and van der Veer, 1970).

In some of the Prymnesiophyceae and particularly the genus Chrysochromulina, muciferous bodies are under the plasma membrane (Figs. 22.1, 22.5(a), 22.10(b)). They have the same structure as

the muciferous bodies in the Raphidophyceae, Dinophyceae, and Chrysophyceae, and consist of a single-membrane-bounded vesicle filled with semi-opaque contents. When they are discharged outside the cell, they appear as substantial cylinders of opaque material of uniform diameter. The function of muciferous bodies is not known.

Fig. 22.6 (a) Hymenomonas roseola, a dried cell showing the flagella and the short bulbous haptonema (which actually arises between the two flagella). (b) A slowly gliding cell of

Chrysochromulina parva. (c) Chloroplast; (cv) contractile vacuole; (f) flagellum; (h) haptonema; (l) leucosin;

(m) muciferous body; (s) scale. ((a) after Manton and Peterfi, 1969; (b) after Parke et al., 1962.)

Phaeocystis globosa has vesicles that contain tightly-wound filaments of chitin (ChrétiennotDinet et al., 1997). Each vesicle contains five chitin filaments that attach near the base of another chitin filament (Fig. 22.9). The chitin filaments produce a five-sided star at their base when they are released from their vesicles.

Fig. 22.8 The sequence of events by which food particles adhere to a haptonema and are moved toward the particle aggregation center. The mass of particles at the particle aggregation center then moves to the tip of the haptonema; the haptonema bends to deposit the mass of particles at the posterior end of the cell where the particles are taken up in food vacuoles. (Adapted from Kawachi et al., 1991.)

Surface protrusions containing cytoplasm are common in the Prymnesiophyceae; they are called pseudopodia. Also, cells can extrude slender trailing filaments from their surfaces, which can be straight or branched. These filaments,

Fig. 22.7 Prymnesium parvum. (a) Drawing of two cells dried and shadow-cast showing the two smooth flagella (f) and the short haptonema (h) on each cell. (b) Transverse section of a haptonema showing the structure of the middle region of seven microtubules in the core surrounded by the membranebounded cavity and the haptonemal wall bounded by the plasmalemma externally. (c) Transverse section of a haptonema near the point of union with the cell showing the crescentric shape of the core characteristic of this region. (d) Progressive levels of haptonema tubules from immediately below the plasmalemma to the distal points of the microtubules. (e) Longitudinal section of a tip of a haptonema.

((a) after Manton, 1966; (b)–(e) after Manton, 1968.)

called filopodia, eventually become segmentally constricted and break up into droplets. Many of the organisms are phagocytic and consequently have food vesicles in the cytoplasm in which they digest bacteria and other small algae. They are not selective in taking up material into the food vesicles, and will take up indigestible detritus as rapidly as bacteria and other algae.

Like many of the other algal groups, the Prymnesiophyceae participate in symbiotic events. Invertebrate radiolaria can harbor prymnesiophyte algal symbionts (Anderson et al., 1983).