326 CHLOROPLAST E.R.: EVOLUTION OF TWO MEMBRANES

Fig. 9.6 The location of the McMurdo Dry Valleys in

Antarctica.

receive only about 10 cm of snow a year. The lakes are fed by glacial melt streams that flow for 6–10 weeks during the brief austral (southern) summer. The lakes are perennially covered by debris-containing ice caps up to 5 m thick that reduce light penetration. In addition, the sun does not arise above the horizon for a number of months during the austral winter. These lakes are highly stratified because of a lack of forces that could generate turnover of the water column (e.g., wind, water temperature changes). Cryptophytes dominate the lower stratified levels where they live heterotrophically during winter months, taking up about one bacterium per hour by phagocytosis (Roberts and Laybourn-Parry, 1999). During the summer months, the cryptophytes are mixotrophic (combining heterotrophy and autotrophy by photosynthesis). A key to the survival of cryptophytes in this environment is maintaining the population in the vegetative state, rather than entering a resting state. The cryptophyte population can respond quickly when “good” conditions return in the short Antarctic summer.

Symbiotic associations

Mesodinium rubrum is a marine planktonic holotrich ciliate of extremely wide geographical

distribution that colors the water in which it is growing red. It has been recorded from neritic locations such as bays and fjords; away from the coast it is usually associated with regions of upwelling and in such conditions the blooms have been recorded as extending over areas as large as 100 square miles. The color of the ciliate (Fig. 9.7) is due to numerous reddish-brown chloroplasts, which belong to a single cryptophycean alga that lives symbiotically inside the ciliate (Gustafson et al., 2000). The cryptophyte is surrounded by a single membrane, and has a nucleus and the normal cytology and pigments of the Cryptophyceae. The endosymbiotic cryptophyte is able to fix 14C in the light, evolve oxygen in photosynthesis, and assimilate 32P, indicating that it is a functioning autotroph. The association is probably similar to that of symbiotes in other classes, with the endosymbiont providing the host with photosynthate and the host providing the endosymbiont with a protected environment. Blooms of Mesodinium rubrum are a regular feature of upwelling ecosystems. The organism has three characteristics that enable it to compete effectively with other autotrophic plankton (Smith and Barber, 1979). (1) It is motile, swimming at rates of 2.0 to 7.2 m h 1, an order of magnitude greater than the maximum swimming speeds attained by dinoflagellates. (2) It has strong phototropisms, being positively phototactic in an increasing light regime in the morning and negatively phototactic in decreasing light and in nutri- ent-depleted waters. (3) It has extremely high photosynthetic rates (1000 to 2000 mg C m 3 h 1), equaling the highest ever observed for oceanic plankton. Conventional dinoflagellate or diatom blooms typically have only 60 to 70 mg C m 3 h 1.

Classification

There are three recognizable groups within the Cryptophyceae (Marin et al., 1998; Deane et al., 2002):

Order 1 Goniomonadales: colorless cells with no plastids.

Order 2 Cryptomonadales: cells usually reddish in color with chloroplasts containing the phycobiliprotein Cr-phycoerythrin.

CRYPTOPHYTA 327

Fig. 9.7 Mesodinium rubrum with its cryptomonad symbiont. (a) Light micrograph of the ciliate showing the chloroplast (C) and pyrenoid

(P) of the cryptomonad endosymbiont. (b) Transmssion electron micrograph. The dotted lines indicate the boundary between the cytoplasm of the ciliate and the cryptomonad symbiont; the difference in density of the two cells is particularly clear. The symbiont nucleus, one of the macronuclei, and the micronucleus of the ciliate are out of the plane of the section. (CM) Ciliate mitochondrion;

(ER) endoplasmic reticulum; (Mac) macronucleus; (P) pyrenoid; (SM) symbiont mitochondrion;

(V) vacuole. The large arrowhead indicates a possible region of Golgi activity. 4500.

(From Hibberd, 1977.)

Order 3 Chroomonadales: the remainder of the cryptophyte algae, often blue-green in color due to chloroplasts containing the phycobiliprotein Cr-phycocyanin.

Goniomonadales

Goniomonas (Figs. 9.8, 9.9(c)), a colorless alga with freshwater and marine species, is the sole alga in the order. Goniomonas is colorless and does not contain a plastid. Food organisms are taken up by an anterior tubular invagination, the infundibulum, and digested in food vacuoles in the cytoplasm. Storage granules occur inside an extension of the outer membrane of the nuclear envelope. Large ejectisomes occur under the anterior plasma membrane and small ejectisomes occur between the periplast plates.

Cryptomonadales

Cryptomonas (Figs. 9.9(a), 9.10, 9.11) and Chilomonas (Fig. 9.9(b)) are the only two genera in the order. Cryptomonas spp. are reddish in color due to the presence of the phycobiliprotein Cr-phycoerythrin in a bilobed chloroplast joined in the center by a pyrenoid. Chilomonas is a reduced form of Cryptomonas (Hoef-Emden and Melkonian, 2003) containing a leucoplast without photosynthetic pigments.

Cryptomonas has an asymmetric shape, which can be attributed, in part, to a subapical depression called the vestibulum which may extend internally to form a gullet or progress along the ventral surface into a furrow (Fig. 9.10(b)) (Kugrens and Lee, 1991). Large ejectosomes occur in rows under the furrow. Sexual reproduction occurs in Cryptomonas (Fig. 9.11) (Kugrens and Lee, 1988).

328 CHLOROPLAST E.R.: EVOLUTION OF TWO MEMBRANES

Fig. 9.8 Reconstruction of a cell of Goniomonas truncata. (f) Flagellar roots; (s) storage granules;

(e) ejectisome; (dv) digestive vacuole; (i) infundibulum. (After Mignot, 1965.)

Fig. 9.9 (a) Cryptomonas erosa.

(b) Chilomonas paramecium.

(c) Goniomonas truncata.

(d) Rhodomonas lacustris.

(e) Chroomonas nordstedtii.

CRYPTOPHYTA 329

Fig. 9.10 Scanning electron micrographs of Chroomonas oblonga

(a) and Cryptomonas sp. (b).

Chroomonas oblonga has multiple periplast plates (P) under the plasma membrane, no furrow is present, and the flagella (F) arise from an anterior vestibular depression.

Cryptomonas sp. has a smooth surface that is produced by a single periplast plate under the plasma membrane. The furrow (Fu) is an extension of the anterior vestibulum. A vestibular ligule (VL) overlaps the vestibulum. (From Kugrens et al., 1986.)

Fig. 9.11 The life cycle of

Cryptomonas sp. (Adapted from

Kugrens and Lee, 1988.)