398 CHLOROPLAST E.R.: EVOLUTION OF TWO MEMBRANES

(c)

(d)

(b)

(a)

(e)

(f)

(g)

Fig. 17.40 (a) Melosira arenaria. (b) Cyclotella antique.

(c) Rhopalodia gibba. (d) Gyrosigma attenuatum. (e) Cymatopleura elliptica. (f) Campylodiscus clypeus. (g) Frustulia rhomboides.

Campylodiscus, Fig. 17.40(f)) indicating leaching of base-rich components from surrounding rocks into the lakes. The next area of sediments showed a decrease in alkaline-water species and an increase in acid-water species (Eunotia, Fig. 17.2(b);

Anomoeoneis; Frustulia, Fig. 17.40(g); Tabellaria, Figs. 17.3(b), 17.33(d), (e)), a trend that has continued up to recent times. This trend is related to a decrease in bases being leached from the rocks because no new rock surfaces have been exposed, and to a decline in the stands of birch/pine on the land. At the top of the sediments are remains of Asterionella formosa, indicating a recent change of waters to less acidic, more eutrophic conditions, a state related to man’s activities. A. formosa is a diatom that grows readily in eutrophic waters and shows changes in colony morphology, depending on nutrients in the water. Under optimum growth conditions, the colonies average eight cells, whereas under phosphate limitation the number of cells per colony drops to two, and under silicate limitation the number of cells per colony increases to 20. Under

both P and Si limitations, there is a decrease in growth rate (Tilman et al., 1976).

Classification

The diatoms probably originated about 200 million years ago in the late Permian (Medlin et al., 1997) from a scaly member of the Chrysophyceae or Bolidophyceae (Guillou et al., 1999). Two scales evolved into valves, while other scales formed the girdle bands. The first diatom had a centric organization with two dome-shaped valves and many scale-like bands (Round et al., 1990). The first recognizable fossils are centric diatoms from the early Cretaceous with pennate diatoms being recorded from the late Cretaceous. The first pennate diatom fossils were araphid (no raphe) with raphid diatoms appearing in the middle Eocene.

The Bacillariophyceae can be divided into two orders as follows:

Order 1 Biddulphiales: radial or gonoid ornamentation; many chloroplasts; no raphe; resting spores formed; motile spermatozoids with a single tinsel

HETEROKONTOPHYTA, BACILLARIOPHYCEAE	399

flagellum; oogamous sexual reproduction.

Order 2 Bacillariales: pennate or trellisoid ornamentation; one or two chloroplasts; raphes possibly present with gliding; no flagellated spermatozoids; sexual reproduction by conjugation.

Biddulphiales

The Biddulphiales or Centrales is primarily a marine planktonic group having cells with gonoid or centric ornamentation (Fig. 17.2). Melosira, a common golden-brown diatom found in marine and freshwater environments, consists of cylindrical cells with a greater length than breadth (Figs. 17.35, 17.40, 17.41, 17.42). There are a number of girdle bands which form incomplete rings around the cell without their ends meeting. Both the valve and the girdle bands are ornamented with small spines. The diatom is usually filamentous, with the cells joined end to end by their valves so that to the inexperienced eye it resembles a filamentous chrysophycean alga with the cells always in girdle view. Gametogenesis is initiated after the cells have undergone a number of mitotic cell divisions that have reduced the size of the frustule below a certain critical limit. Von Stosch (1951) has elucidated the following events in the life cycle of Melosira varians (Fig. 17.42). In the male cells, gametogenesis starts with the nucleus undergoing two meiotic divisions to produce four

haploid nuclei. A plasma membrane is formed around each nucleus and a small amount of parent cell protoplasm. The remaining protoplasm of the mother cell now lacks a nucleus and begins to degenerate. A single flagellum is produced by each male gamete, the epitheca separates from the hypotheca, and the male gametes are released into the medium. In the female cells, while the nucleus is undergoing the first meiotic division, one of the girdle bands separates from the edge of the valve, leaving an area of protoplasm open to the medium. The male gamete swims to the area of the female cell where the girdle band has separated from the valve edge. During telophase of the first meiotic division of the female cell, the cytoplasm of the male gamete fuses with that of the female cell. One of the nuclei of the first meiotic division in the female cell degenerates while the other nucleus undergoes a second meiotic division. From the second meiotic division, one of the female nuclei again degenerates, and the other becomes the egg nucleus. The male nucleus fuses with the egg nucleus to form the zygote or auxospore nucleus. The resulting auxospore (Fig. 17.43) then swells, pushing apart the hypotheca and epitheca until the auxospore is attached to both or one theca by a small protuberance only. The auxospore has an outer organic wall and an inner wall made of siliceous scales (Crawford, 1974). A new cell wall of maximum dimensions is now produced within

Fig. 17.41 Semidiagrammatic representation of a cell of

Melosira varians composed of two valves, V and V , two girdle band series: 1, 2, 3, and, underlapping these, the younger series 1 , 2 , 3 . (After Crawford, 1971.)

400 CHLOROPLAST E.R.: EVOLUTION OF TWO MEMBRANES

Fig. 17.42 The life cycle of Melosira varians. (Adapted from

von Stosch, 1951.)

HETEROKONTOPHYTA, BACILLARIOPHYCEAE	401

Fig. 17.43 Electron micrographs of an auxospore of

Melosira nummuloides (left) showing the scales covering the auxospore (right). (From Medlin et al., 1993.)

the auxospore. This cell divides to give rise to a new filament.

Melosira is capable of producing dormant cells in freshwater environments. The dormant cells have the protoplasm condensed to a dark-brown protoplasmic mass in one part of the frustule (Sicko-Goad et al., 1986). The dormant cells settle into the sediment, where they are capable of surviving for up to 20 years. Normally, however, the dormant cells are swept up by normal recirculation of lake waters during lake overturns (Lund, 1959). Within 24 hours of being swept out of the sediments, the dormant cells of Melosira differentiate into vegetative cells.

Chaetoceros (Figs. 17.6(a), 17.32, 17.44, 17.45) has more than 160 species, the largest number of any planktonic diatom. The genus is widespread in warm and cold waters. The life cycle of Chaetoceros diadema has been elucidated by Hargraves (1972) (Fig. 17.44). Chaetoceros diadema is a colonial marine diatom, with cells united by their long setae to form filaments. The different phases of the life cycle are characterized by different sizes and shapes of cells. Gametogenesis is initiated at temperatures between 2 and 5 °C (French and Hargraves, 1985). The cells that produce the male gametes are about 1.5 to 2 times as wide as high.

These cells divide to produce 32 male gametes, presumably by meiosis, which are released as uniflagellate swarmers. The cells that produce the female gametes are about twice as high as wide. The exact nuclear events that lead to the production of the egg are not known, but the male gamete (Fig. 17.45) swims to the girdle area of the female cell, casts off its flagellum, and fuses with the female gamete inside the frustule. The cell contents of the auxospore-forming cell are then extruded through the girdle region into a thin hyaline envelope. This cell then produces the auxospore, which, in turn, produces new cells with frustules of maximum size. These large daughter cells remain attached to the auxospore parent wall through two divisions of the daughter cells. The hyaline envelope of the auxospore is sloughed off after the first division. Any of the vegetative cells have the ability to produce resting spores after nitrogen depletion of the culture medium at temperatures that allow vegetative growth (French and Hargraves, 1985). The resting spores germinate to produce cells larger than the original cells. The resting spores occur within the parent cell as heavily siliceous bodies, having usually convex, often dissimilar, upper and lower surfaces bearing spines.

Bacillariales

The Bacillariales or Pennales order contains cells that occur both in freshwater and in marine

402 CHLOROPLAST E.R.: EVOLUTION OF TWO MEMBRANES

Fig. 17.44 The life cycle of Chaetoceros diadema. (Adapted

from Hargraves, 1972.)

HETEROKONTOPHYTA, BACILLARIOPHYCEAE	403

Fig. 17.45 Chaetoceros laciniosus. A transmission electron micrograph of a shadowed preparation of a whole mount of a spermatozoid showing the single tinsel flagellum. (From Jensen et al., 2003.)

environments. These cells have either pennate or trellisoid ornamentation (Fig. 17.2). The life cycle of these organisms involves fusion of two gametes by conjugation and common genera such as Nitzschia (Figs. 17.26(b), 17.35), Pseudo-nitzschia (Figs. 17.27, 17.29), Navicula (Figs. 17.2(d), 17.16, 17.25, 17.26(a), 17.33(b), 17.35), Amphora (Figs. 17.22(c), (d), 17.35), Cymbella, and Pinnularia (Figs. 17.3(a), 17.12, 17.18, 17.46) have essentially the same life cycle. In Pinnularia, the cells have rounded poles with more or less parallel sides (Fig. 17.46). Auxospore formation is a sexual process initiated after cell divisions have reduced the cell to a certain critical size. Two cells come together and invest themselves in a mucous envelope (Hendey, 1964). The nucleus in each cell undergoes two meiotic divisions followed by cytokinesis into two cells. Two gametes are thus formed per mother cell, each protoplast receiving one functional and one degenerating nucleus. One gamete from each mother cell moves to the contiguous mother cell to fuse with the passive gamete. In this manner, one zygote (auxospore) is formed within each mother cell. These auxospores become greatly enlarged, and eventually new siliceous frustules

Fig. 17.46 Auxospore formation in Pinnularia. (a) Two cells lie next to each other. (b)–(d) Meiosis occurs in each mother cell, resulting in two gametes per mother cell, each with one functional nucleus (N) and one degenerate nucleus (DN). (e) One gamete from each mother cell passes to the other mother cell.

(f) There is one auxospore (A) per mother cell frustule. (g) Each auxospore has produced a new large daughter cell (NW), with the old cell walls (OW) of the mother cells still embedded in the mucilage. (C) Chloroplast. (After Hendey, 1964.)